S^Q^^QQ^^^^Q^^Ea

I Marine Biological Laboratory Library

Woods Hole, Mass.

[0

Presented Ly

Miss Mildred Moses
(3 Oct '52)

il
II

T

[D

a^^^^s^^^s^^^^sai

'kP^

,^ VJ

THE DEVELOPMENT OF THE C^HICK

AN INTRODUCTION TO EMBRYOLOGY

THE DEVELOPMENTu^
OF THE CHICK ^^

AN INTRODUCTION TO EMBRYOLOGY

BY

FRANK R. LILLIE

PROFESSOR IN THE UNIVERSITY OP CHICAGO

SECOND EDITION, REVISED

NEW YORK
HENRY HOLT AND COMPANY

1919

-<»

«

Copyright, 1908, 1919,

BY

HENRY HOLT AND COMPANY

PREFACE TO FIRST EDITION

This book is a plain account of the development of the never-
failing resource of the embryologist, the chick. It has been neces-
sary to fill certain gaps in our knowledge of the development
of the chick by descriptions of other birds. But the account
does not go beyond the class Aves, and it applies exclusively
to the chick except where there is specific statement to the
contrary. Projected chapters on the integument, muscular sys-
tem, physiology of development, teratology, and history of the
subject have been omitted, as the book seemed to be already
sufficiently long. The account has been written directly from
the material in almost every part, and it has involved some
special investigations, particularly on the early development
undertaken by Doctor Mary Blount and Doctor J. T. Patterson,
to whom acknowledgments are due for permission to incor-
porate their results before full publication by the authors. As
the book is meant for the use of beginners in embryology, refer-
ences to authors are usually omitted except where the account
is based directly on the description of a single investigator. A
fairly full list of original sources is published as an appendix.

Figures borrowed from other publications are credited in
the legends to the figures. The majority of the illustrations are
from original preparations of the author: Figures 46, 48, 50, 51,
52, 58, 59, 60, 61, 62, 63, 64, 65, 66, 67, 71, 72, 73, 74, 75, 99,
105 and 106 were drawn by Mr. K. Hayashi; the remainder of
the original drawings were executed by Mr. Kenji Toda. The
photographs in Figures 118, 119, 120, 168, 181, 182, 189, 194, 197,
and 231 are the work of Mr. Willard C. Green. Some of the
figures may be studied with advantage for points not described
in the text.

Acknowledgments are also due my colleague, Professor W. L.
Tower for much assistance, and to Doctor Rov L. Moodie for
special work on the skeleton, and photographs of potash prep-
arations reproduced in Figures 242, 246, 249 and 250.

The best introduction to the problems opened up by the study

iii

iv PREFACE

of embryology is a careful first-hand study of some one species.
It is in this sense that the book may serve as an introduction to
embryology, if its study is accompanied by careful laboratory
work. In some respects it is fuller, and in others less complete,
than other books with which it might be compared. On its
comparative and experimental sides, embryology is the only key
to the solution of some of the most fundamental problems of
biology. The fact that comparative and experimental embry-
ology receive bare mention is not due to any lack of appreciation
of their interest and importance, but to the conviction that the
beginner is not prepared to appreciate these problems at the
start; to the belief that our teachers of embryology are com-
petent to remedy omissions; and finally to the circumstance
that no one book can, as a matter of fact, cover the entire field,
except in the most superficial way.

The development before laying and the first three days of
incubation are treated by stages as far as possible, and this mat-
ter constitutes Part I of the book. It involves the study of the
origin of the primordia of most of the organs. The matter
concerning the later development is classified by the organs
concerned, which seems to be the only possible way, and this
constitutes Part II. The first part is complete in itself, so far
as it goes, and no doubt it will be the only part consulted by
some students.

The attempt to present a consecutive account of the develop-
ment of the form on which so many classics in the history of
embryology have been based is no slight undertaking. The
author can hardly hope that he has avoided omissions and errors,
and he will be sincerely grateful to those who call such to his
attention.

COXTEXTS

IXTRODUCTION

PAGE

I. The Cell Theory . 1

II. The Recapitulation Theory 3

III. The Physiology of Development 6

IV. Embryonic Primordia and the Law of Genetic Restric-

tion 8

V. General Characters of Germ-cells 9

The Spermatozoon 9

The Ovum 10

Comparison of the Germ-cells 12

VI. Polarity and Organization of the Ovum .... 14

PART I

THE EARLY DEVELOPMENT TO THE END OF THE

THIRD DAY

CHAPTER I. THE EGG 17

Chemical Composition of the Hen's Egg 20

Formation of the Egg 21

Abnormal Eggs 25

Ovogenesis 26

*

CHAPTER II. THE DEVELOPMENT PRIOR TO LAYING 32

I. Maturation 32

11. Fertilization 35

III. Cleavage of the Ovum 38

The Hen's Egg 39

The Pigeon's Egg 43

IV. Origin of the Periblastic Nuclei, Formation of the

Germ-wall 47

V. Origin of the Ectoderm and Entoderm ...... 52

CHAPTER III. OUTLINE OF DEVELOPMENT, ORIENTA-
TION, CHRONOLOGY 61

Orientation 63

Chronology {Classification of Stages) 64

Tables of the Developyyient of the Chick 68

Zn3\

vi COXTEXTS

PAGE

CHAPTER IV. FROM LAYIXG TO THE FORMATIOX OF

THE FIRST SOMITE 69

I. Structure of the Unincubated Blastoderm .... 69

II. The Primitive Streak 69

Total Views 69

Sections 74

The Head-process 80

hiterpretation of the Primitive Streak 83

III. The Mesoderm of the Opaque Area 86

IV. The Germ-wall 90

CHAPTER V. HEAD-FOLD TO TWELVE SOMITES

(From about the twenty-first to the thirty-third hour of incu-
bation) 91

I. Origin of the Head-fold 91

II. Formation of the Fore-gut 93

III. Origin of the Xeural Tube 95

The Medullary Plate 95

The Neural Groove and Folds 97

Primary Divisions of the Neural Tube 105

Origin of the Primary Divisions of the Embryonic Brain 108

IV. The Mesoblast 109

Primary Structure of the Sornites 11-4

The Nephrotome, or Intermediate Cell-mass (Middle

Plate) 114

The Lateral Plate 115

Development of the Body-cavity or Cadome 115

Mesoblast of the Head 116

Vascular System 117

Origin of the Heart 119

The Embryonic Blood-vessels 121

V. Description of an Embryo with 10 Somites .... 122

The Nervous System 124

Alimentary Canal 126

Vascular System 126

General 127

Zones of the Blastoderm 127

CHAPTER VI. FROM TWELVE TO THIRTY-SIX SO]\IITES.

THIRTY-FOUR TO SEVEXTY-TWO HOURS . 130
I. Development of the External Form, and Turning of

the Embryo 130

Separation of the Embryo from the Blastoderm . . . 130

CONTEXTS vii

PAGE

The Turning of the Embryo and the Embryonic Flexures 133

II. Origin of the Embryonic Membranes 135

Origin of the Amnion and Chorion 135

The Yolk-sac 143

Origin of the Allantois 143

Summary of Later History of the Embryonic Membranes . 145

III. The Xervous System 147

The Brain 147

The Neural Crest and the Cranial and Spinal Ganglia 156

IV. The Organs of Special Sense (Eye, Ear, X'ose) . 164

The Eye ^ . 164

The Auditory Sac 168

The Nose (Olfactory Pits) 169

V. The Alimentary Canal and its Appendages . . . 170

The StomodoEum 173

The Pharynx and Visceral Arches 173

(Esophagus and Stomach 179

The Liver 179

The Pancreas 181

The Mid-Gut 181

Ancd Plate, Hind-gut, Post-anal gut and Allantois 182

VI. History of the Mesoderm 183

Somites 183

The Intermediate Cell-mass 190

The Vascular System 197

VII. The Body-cavity and Mesenteries 205

PART II

THE FOrRTH DAY TO HATCHING, ORGANOGENY,
DEVELOPMENT OF THE ORGANS

CHAPTER VII. THE EXTERXAL FORM OF THE EM-
BRYO AXD THE EMBRYONIC :\IEMBRAXES 211

I. The External Form 211

General 211

Head 213

II. Embryonic Membranes . . . 216

General 216

The Allantois 220

The Yolk-sac 225

The Amnion 231

Hatching . . 232

viii CONTEXTS

PAGE

CHAPTER \TII. THE NERVOUS SYSTEM 233

I. The Neuroblasts 233

The Medullary Neuroblasts 233

The Ganglionic Neuroblasts 236

II. The Development of the Spinal Cord 239

Central Canal and Fissures of the Cord 242

Neuroblasts, Commissures, and Fiber Tracts of the Cord . 244

III. The Development of the Brain 244

The Telencephalon 245

The Diencephalon 249

The Meseyicephalon 251

The Metencephalon 251

The Myelencephalon 252

Commissures of the Brain 252

IV. The Peripheral Nervous System . 252

The Spinal Nerves 252

The Cranial Nerves 261

CHAPTER IX. ORGANS OF SPECIAL SENSE .... 271

I. The Eye 271

The Optic Cup 271

The Vitreous Humor 275

The Lens 276

Anterior Chamber and Cornea 278

The Choroid and Sclerotic Coats 279

The Eyelids and Conjunctival Sac 279

Choroid Fissure, Pecten and Optic Nerve 281

II. The Development of the Olfactory Organ . . . 285

III. The Development of the Ear 288

Development of the Otocyst and Associated Parts . . . 289
The Development of the Tubo-tyyn panic Cavity, External

Auditory Meatus and Tympanum 297

CHAPTER X. THE ALIMENTARY TRACT AND ITS AP-
PENDAGES 301

I. Mouth and Oral Cavity 301

Beak and Egg-tooth 302

The Tongue 305

Oral Glands 306

II. Derivatives of the Embryonic Pharynx 306

Fate of the Visceral Clefts 307

Thyroid 307

CONTENTS IX

PAGE

Visceral Pouches • • 307

The Thymus 308

Epithelial Vestiges 309

The Posthranchial Bodies 309

III. The (Esophagus, Stomach and Intestine .... 309

Oesophagus 312

Stomach 313

Large Intestine, Cloaca, and Anus 314

IV. The Development of the Liver and Pancreas , . . 319

The Liver 319

The Pancreas 323

V. The Respiratory Tract 325

Bronchi, Lungs and Air-sacs 325

The Laryngotracheal Groove 331

CHAPTER XI. THE BODY-CAVITIES, MESENTERIES AND

SEPTUM TRANSVERSUM 333

I. The Separation of the Pericardial and Pleuroperi-

TONEAL Cavities 333

Septum Transversum 334

Closure of the Dorsal Opening of the Pericardium . . . 337

Estahlishment of Independent Pericardial Walls . . . 338

Derivatives of the Septum Transversum 339

II. Separation of Pleural and Peritoneal Cavities; Or-

igin OF THE Septum Pleuro-peritoneale . . . 340

III. The Mesenteries 342

The Dorsal Mesentery 342

The Origin of the Omentum 343

Origin of the Spleen 345

CHAPTER XII. THE LATER DEVELOPMENT OF THE

VASCULAR SYSTEM 348

I. The Heart 348

The Development of the External Form of the Heart . . 348

Division of the Cavities of the Heart 350

Fate of the Bulbus .357

The Sinus Ve?iosus 357

II. The Arterial System 358

The Aortic Arches 358

The Carotid Arch 361

The Subclavian Artery 362

The Aortic System 362

X CONTENTS

PAGE

III. The Venous System ..... c .... . 363

The Anterior Vence Cavce 363

The Omphalomesenteric Veins 364

The Umbilical Veins 367

The System of the Inferior Vena Cava 368

IV. The Embryonic Circulation 372

CHAPTER XIII. THE URINOGENITAL SYSTEM ... 378

I. The Later History of the Mesonephros 378

II. The Development of the Metanephros or Permanent

Kidney 38-1:

The Metanephric Diverticulum 384

The Nephrogenous Tissue of the Metanephros . . . 387

III. The Organs of Reproduction • 390

Development of Ovary and Testis 391

Development of the Genital Ducts 401

IV. The Suprarenal Capsules 403

Origin of the Cortical Cords 405

Origin of the Medullary Cords 406

CHAPTER XIV. THE SKELETON 407

I. General 407

II. The Vertebral Column 411

The Sclerotomes and Vertebral Segmentation .... 412

Membranous Stage of the Vertebrce 414

Chondrification 418

Atlas and Axis (Epistropheus) 420

Formation of Vertebral Articulations 421

Ossification 421

III. Development of the Ribs and Sternal Apparatus. . 424

IV. Development of the Skull 427

Development of the Cartilaginous or Primordial Cranium. 428

Ossification of the Skull 431

V. Appendicular Skeleton 434

The Fore-limb 434

The Skeleton of the Hind-limb 438

APPENDIX

General Literature ^ •> .... 443

Literature — Chapter I 443

Literature — Chapter II 444

Literature — Chapter III 44o

Literature — Chapters IV and V 44o

CONTEXTS XI

PAGE

Literature — Chapter VII 447

Literature — Chapter VIII 449

Literature — Chapter IX 450

Literature — Chapter X 453

Literature — Chapter XI 4o/

Literature — Chapter XII 458

Literature — Chapter XIII 459

Literature — Chapter XIV 461

Index 465

vV

^GIC/Q

X

LIBRARY =

THE DEVELOPMENT OF THE

INTRODUCTION

I. The Cell Theory

The fundamental basis of the general conceptions of embry-
ology, as of other biological disciplines, is the cell theor3^ The
organism is composed of innumerable vital units, the cells, each
of which has its independent life. The life of the organism as a
whole is a product of the combined activity of all the cells. New
cells arise always by subdivision of pre-existing cells, and new
generations of the organism from liberated cells of the parental
body. The protozoa, however, have the grade of organization
of single cells, and the daughter-cells arising by fission constitute
at the same time new generations. In some metazoa new gen-
erations may arise asexually by a process of budding, as in Hydra,
or of fission, as in some Turbellaria; such cases constitute excep-
tions to the rule that new generations arise from liberated cells
of the parental body, but the rule holds without exception for
all cases of sexual reproduction.

The body consists of various functional parts or organs; each
of these again consists of various tissues, and the tissues are com-
posed of specific kinds of cells. The reproductive organs, or
gonads, are characterized by the production of germ-cells, ova
in the female gonad or ovary, and spermatozoa in the male gonad
or testis. However large the ovum may be, and in the hen it
is the part of the egg known as the yolk, it is, nevertheless, a
single cell at the time that it leaves the ovary in all animals.
Similarly the spermatozoon is a single cell. An ovum and sper-
matozoon unite, in the manner to be described later, and con-
stitute a single cell by fusion, the fertilized ovum or oosperm.
This cell divides and forms two; each of the daughter-cells divides,
making four, and the number of cells steadily increases by suc-
cessive divisions of all daughter-cells, so that a large number
of cells is rapidly produced. Organs are formed by successive

1

2 THE DEVELOPMENT OF THE CHICK

and orderly differentiation among groups of these cells. Among
these organs are the gonads, consisting of cells which trace a
continuous lineage by cell-division back to the fertilized ovum,
and which are capable of developing into ova or spermatozoa
according to the sex of the individual.

The lives of successive generations are thus continuous because
the series of germ-cells from which they arise shows no break in
continuity. All other kinds of cells composing the body finally
die. In view of this contrast the non-germinal cells of the body
are known collectively as somatic cells. In some way the germ-
cells of a species maintain very constant properties from gen-
eration to generation in spite of their enormous multiplication,
and this furnishes the basis for hereditary resemblance.

The establishment of the fact that in all animals the ovum is
a single cell, and that the cells of all tissues of the body are derived
from it by a continuous process of cell-division, completes the
outline of the cycle of the generations, and furnishes the basis
for a complete theory of development. The full significance
of this principle can only be appreciated by learning the condition
of embryology before the establishment of the cell-theory in the
eighteenth century. The history of our knowledge of the devel-
opment of mammals is particularly instructive in this respect:
some knowledge had been gained of the anatomy of the embryos,
mostly relatively advanced, of a few^ mammals; but the origin
of the embryo was entirely unknown; the ovum itself had not
been discovered; the process of fertilization was not understood.
In the knowledge of the cycle of generations there was a great
gap, and the embryo was as much a mystery as if it had arisen
by a direct act of creation. To be sure Harvey in 1651 had
propounded the theorem, omne vivum ex ovo, but no one had
ever seen the egg of a mammal, and there was no clear idea in
the case of other forms what the egg signified.

In 1672, de Graaf (who died in 1673 at the age of 32) published
a work, "de mulierum organis generationis inservientibus," in
which he attempted to show that the vesicles seen on the surface
of the ovaries contained the female reproductive material in
bladder-like form. But he could not reconcile this view of the
Graafian follicle with the fact that the earliest embryos discovered
by him were smaller than the follicles. For this reason his views
were opposed by Leeuwenhoek and Valisnieri; and the later re-

IXTRODUCTIOX 3

searches of Haller and his pupil Kuhlemann seemed to establish
a view which l^anished all possibility of a rational explanation
of development, viz., that, in the highest group of animals (the
mammalia) the embryo arose after fertilization out of formless
fluids.

In 1827 V. Baer discovered the mammalian ovum within the
Graafian follicle. But no correct interpretation of this discovery
w^as possible until the establishment of the cell-theory by Theo-
dore Schwann in 1839; Schwann concluded as the result of his
investigations that there was one general principle for the forma-
tion of all organisms, namely, the formation of cells; that ''the
cause of nutrition and growth resides not in the organism as a
whole, but in the separate elementary parts, the cells." He
recognized the ovum as a single cell and the germinal vesicle as
its nucleus. But on account of his erroneous conception of the
origin of cells as a kind of crystallization in a primordial sub-
stance, the cytoblastema, he was unable to form the conception
of continuity of generations which is an essential part of the
modern cell-theory.

Schwann's theory as regards the ovum was not at once ac-
cepted. Indeed, for a period of about twenty years some of
the best investigators, notably Bischoff, opposed the view that
the ovum is a single cell, and the so-called germinal vesicle its
nucleus. It was not, indeed, until 1861 that Gegenbaur deci-
sively demonstrated that the bird's ovimi is a single cell. Even
after that it was maintained for a long time by His and his fol-
lowers that all the cells were not derived from the ovum directly,
but that certain tissues, notably the blood and connective tissues,
were to be traced to maternal leucocytes that had migrated into
the ovum while it was yet in the follicle. This view was decisively
disproved in the course of time.

II. The Recapitulation Theory

Haeckel's formula, that the development of the indi\ddual
repeats briefly the evolution of the species, or that ontogeny is
a brief recapitulation of phylogeny, has been widely accepted by
embryologists. It is based on a comparison between the embry-
onic development of the individual and the comparative anatomy
of the phylum. The embryonic conditions of any set of organs
of a higher species of a phylum resemble, in many essential par-

4 THE DEVELOPMENT OF THE CHICK

ticulars, conditions that are adult in lower species of the same
phylum; and, moreover, the order of embryonic development
of organs corresponds in general to the taxonomic order of organ-
ization of the same organs. As the taxonomic order is the order
of evolution, Haeckel's generalization, which he called the funda-
mental law of biogenesis, w^ould appear to follow^ of necessity.

But it never happens that the embryo of any definite species
resembles in its entirety the adult of a lower species, nor even
the embryo of a lower species; its organization is specific at all
stages from the ovum on, so that it is possible without any diffi-
culty to recognize the order of animals to which a given embryo
belongs, and more careful examination will usually enable one
to assign its zoological position very closely.

If phylogeny be understood to be the succession of adult
forms in the line of evolution, it cannot be said in any real sense
that ontogeny is a brief recapitulation of phylogeny, for the
embryo of a higher form is never like the adult of a lower form,
though the anatomy of embryonic organs of higher species re-
sembles in many particulars the anatomy of the homologous
organs of the adult of the lower species. However, if w^e conceive
that the whole life history is necessary for the definition of a
species, we obtain a different basis for the recapitulation theory.
The comparable units are then entire ontogenies, and these re-
semble one another in proportion to the nearness of relationship,
just as the definitive structures do. The ontogeny is inherited
no less than the adult characteristics, and is subject to precisely
the same laws of modification and variation. Thus in nearly
related species the ontogenies are very similar; in more distantly
related species there is less resemblance, and in species from
different classes the ontogenies are widely divergent in many
respects.

From this it follows that inheritance of the life-history or
ontogeny is the fundamental basis of the recapitulation theory.
In the course of evolution terminal or late stages of the life
history are modified more rapidly in a visible morphological
sense, and earlier stages are more conservative in the same
sense. Hence ancestral resemblances adhere incomparably longer
to the embryo than to the adult. Ontogenies receive something
from every stage of evolution, but they retain most of the
previous ontogenetic forms, especially of the early stages, in

INTRODUCTION 5

each succeeding evolutionary stage; hence the appearance of
recapitulation of the ancestral history.

Some of these considerations may be represented graphically
as follows: let us take a species D that has an ontogeny A, B, C, D,
and suppose that this species evolves successively into species
E, F, G, H, etc. When evolution has progressed a step, to E,
the characters of the species established develop directh' from
the ovum, and are therefore, in some way, involved in the com-
position of the latter. All of the stages of the ontogeny leading
up to E are modified, and we can indicate this in the ontogeny

1. A B C D of E as in line 2; similarly, when evolu-

2. A^ B^ C^ D^ E tion has progressed to species F, seeing

3. A^ B2 C^ D2 E^ F that the characters of F now develop

4. A^ B^ C^ D^ E2 F^ G directly from the ovum, all the onto-

5. A^ B^ C^ D^ E^ F^ G^ H genetic stages leading up to F are modi-
fied, line 3. And so on for each successive advance in evolution,
lines 4 and 5. It will also be noticed that the terminal stage D of
species 1, becomes a successively earlier ontogenetic stage of species
2, 3, 4, 5, etc., and moreover it does not recur in its pure form,
but in the form D^ in species 2, D^ in species 3, etc. Now if the
last five stages of the ontogeny of species 5 be examined, viz.^
D^ E^, F^, G^ H, it will be seen that they repeat the phylogeny
of the adult stages D, E, F, G, H, but in a modified form.

This is in fact what the diagram shows; but it is an essential
defect of the diagram that it is incapable of showing the character
of the modifications of the ancestral conditions. Not only is each
stage of the ancestral ontogenies modified with each phylogenetic
advance, but the elements of organization of the ancestral stages
are also dispersed so that no ancestral stage hangs together as a
unit. The embryonic stages show as much proportional modi-
fication in the course of evolution as the adult, but this is not
so obvious owing to the simpler and more generalized character
of the embryonic stages.

The recapitulation theory as outlined above is obviousl}^ a
corollary of the theory of organic descent; it was in fact developed
in essentially its present form, soon after the publication of the
''Origin of Species," by Fritz Miiller and Ernst Haeckel. But
the data on which it was based were known to the earlier embry-
ologists; and Meckel, for instance, insisted very strongly on the
resemblance between the ontogenetic and the taxonomic series

6 THE DEVELOPMENT OF THE CHICK

(1821). V. Baer opposed Meckel's view that higher organisms
pass through the definitive stages of the lower organisms, and
formulated his conclusions on the subject in 1828 in the following

theses :

1. "The more general features of a large division of animals
arise in the embryo earlier than the more special features."

2. " From the most general features of structure arise those that
are less general, and so on until the most specific features arise."

3. "The embryo of any definite species tends away from the
specific forms of other species instead of passing through them."

4. "Fundamentally, therefore, the embryo of any higher
species is never like a lower species, but only like its embryo."

Some embryologists profess to prefer the laws of v. Baer to
the recapitulation theory as a formulation of the actual facts.
But it is obvious that the only possible explanation of the facts
is found in the theory of descent, and that therefore they must
be formulated in terms of this theory. The method of formula-
tion will depend on the conception of the nature of the factors
of organic evolution. Haeckel stated his theory in Lamarckian
terms, which renders it inacceptable in many places to those
who cannot accept the Lamarckian point of view. But as the
basis of any theory of descent is heredity, and it must be recog-
nized that ontogenies are inherited, the resemblance between the
individual history and the phylogenetic history necessarily fol-
lows. If one holds, as does the present writer, that phylogenetic
variations are germinal in their character, then one must admit
that every phase of development of every part has two aspects,
viz.: the modern, specific, or coenogenetic, and the ancestral or
palingenetic aspect. The latter aspect may be more or less com-
pletely obscured in the course of evolution, but it can never
entirely vanish because it is the original germ of the specific
form acquired. It is not correct from this point of view to classify
some features of development as coenogenetic and others as palin-
genetic, though it is obvious that some characters may exhibit
the ancestral conditions in more apparent and others in less
apparent form.

III. The Physiology of Development
To explain how a germ possessed the potency of forming an
adult, the prefor7nationists of the eighteenth century assumed

INTRODUCTION 7

that it contained a miniature adult, and that the process of
development consisted essentially in enlargement and completion
in detail of that which was already preformed. They solved the
problem of development, therefore, by denying its existence:
In the begininng the Creator had not only made all species of
animals and plants in essentially their present forms, but had
at the same time created the germs of all the generations that
were ever to come into existence. The ovum of any species,
therefore, contained encapsuled the germ of the next generation;
this, likewise encapsuled, the germ of the generation next follow-
ing, and so on to the predetermined end of the species. This
was known as the doctrine of evolution or preformation. In
opposition to this conception, those of the same period who be-
lieved in epigenesis maintained the apparent simplicity of the
germ to be real, and development to be actual. But, as there
was no conception of the continuity of generations, the adherents
of this point of view had to assume the spontaneous generation
of the embryo.

A great advance over the preformation theory of develop-
ment was made in the modern theory of determinants. This
conception, which forms the basis of Darwin's theory of pan-
genesis as well as of Weismann's germ-plasm theory of develop-
ment, is, essentially, that all the diverse components of the
organism are represented in the germ by distinct entities (pangens
of Darwin, determinants of Weismann) which are germs of the
parts that they represent, and which are so distributed in the pro-
cess of development that they produce all the parts of the embryo
in their proper sequence and relations. This is not the place
to enter into the numerous and diverse variations of the deter-
minant hypothesis. It was an advance over the preformation
theory of development in so far as it was reconcilable with the
cell and protoplasm theories of organization, but it has a real
relationship to the preformation theory inasmuch as it denies
the simplicity of the germ and avoids any real explanation of
the modus operandi of development.

Development is as truly a physiological process as secretion,
and as such is to be studied by similar methods, mainly experi-
mental. The limits of pure observation without experiment are
soon reached in the analysis of such a complex subject as the
physiology of development; experiment then becomes necessary

8 THE DEVELOPMENT OF THE CHICK

to push the analysis of the subject farther^ and to furnish the
true interpretation of the observations. In some cases experi-
ments have confirmed the physiological deductions of pure ob-
servation, and in many cases have decided between conflicting
views. Not all embryological experiments, however, are essays
in the direction of a physiologv of development; some are directed
to the solution of morphological problems, as, for instance, the
origin of the sheath cells of nerves, or the order of origin of so-
mites, or the relation of the primitive streak to the embr3'o.
Experimental embryology is, therefore, not synonymous with
physiology of development.

Physiology of development must proceed from an investiga-
tion of the composition and properties of the germ-cells. It
must investigate the role of cell-division in development, the
factors that determine the location, origin, and properties of the
primordia of organs, the laws that determine unequal growth,
the conditions that determine the direction of differentiation,
the influence of extraorganic conditions on the formation of the
embryo, and the effects of the intraorganic environment, i.e.,
of component parts of the embryo on other parts (correlative
differentiation). Each of these divisions of the subject includes
numerous problems, which have attracted many investigators,
so that the materials for a consistent exposition of the physiology
of embryonic development are being rapidly accumulated. This
direction of investigation is, however, one of the youngest of
the biological disciplines. It will be seen how far it is removed
from attempts to explain embryonic development by a single
principle.

IV. Embryonic Primordia and the Law of Genetic Re-
striction

In the course of development the most general features of
organization arise first, and those that are successively less general
in the order of their specialization. For every structure, there-
fore, there is a period of emergence from something more general.
The earliest discernible germ of any part or organ may be called
its primordium. In this sense the ovum is the primordium of
the individual, the ectoderm the primordium of all ectodermal
structures, the medullary plate the primordium of the central
and part of the peripheral nervous system, the first thickening

IXTRODUCTIOX 9

of the ectoderm over the optic cup the primordium of the lens,
etc. Primordia are, therefore, of all grades, and each arises
from a primordium of a higher grade of generality.

The emergence of a primordium involves a limitation in two
directions: (1) it is itself limited in a positive fashion by being
restricted to a definite line of differentiation more special than
the primordium from which it sprang, and (2) the latter is limited
in a negative way by losing the capacity for producing another
primordium of exactly the same sort. The advance of differen-
tiation sets a limit in all cases, in the manners indicated, to sub-
sequent differentiation, a principle that has been designated by
Minot the law of genetic restriction.

This law has not been sufficiently investigated in an experi-
mental fashion to demonstrate its universal validity, but enough
is known to establish its general applicability. A very impor-
tant property of primordia in many animals is their capacity
for subdivision, each part retaining the potencies of the whole.
Thus, for instance, in some animals two or several embrvos mav
be produced from parts of one ovum. Similarly two or more
limbs may be produced in some forms by subdividing a limb-
bud, etc.

V. General Character of Germ-cells

As already remarked the ovum and spermatozoon have the
character of single cells in all animals. They are, however,
specialized for the performance of their respective functions.
The ovum is relatively large, inert, and usually rounded in form.
Its size is due to the presence of a sufficient quantity of proto-
plasm to serve as the primordium of an embryo, and of a greater
or less amount of yolk for its nutrition. The spermatozoon,
on the other hand, is relatively minute and capable of locomotion.
It contains no food substances, and only sufficient protoplasm
to serve as transmitter of paternal qualities and for organs
of locomotion.

The Spermatozoon. The spermatozoon (Fig. 1) is an elon-
gated flagellated cell in which three main divisions are distin-
guished, viz., head (caput), neck (coUum) and tail (cauda). The
head contains the nucleus, and the neck the centrosomes of the
sperm mother-cell or spermatid. The tip of the head is often
transformed into a perforatorium. Three parts may be recog-

10

THE DEVELOPMENT OF THE CHICK

nized in the tail, viz., the connecting piece (pars conjunctionis) next
to the neck, frequently called the middle piece, the main piece (pars
principalis) and the end-piece or terminal filament (pars terminahs).
The entire tail is traversed by an axial filament; in the region

of the connecting and main pieces the axial
filament is surrounded by a protoplasmic
sheath (involucrum) which may be variously
modified in different animals. The end-piece
is made up of the axial filament alone.

The Ovum, The ova of different phyla and
classes of animals vary greatly in size, in or-
ganization, and in the nature of their enve-
lopes. In considering these variations we shall
limit ourselves to the vertebrates. Within the
ovary the ovum receives two envelopes, viz., a
primary envelope, the so-called vitelline mem-
brane, which is supposed to be secreted by the
ovum itself, and a secondary or follicular mem-
brane, which is secreted by the follicular cells.
(See Chap. I). Theoretically the distinction be-
tween vitelline membrane and follicular mem-
brane (primary and secondary egg-membranes)
is perfectly clear; but practically it is impossi-
ble in most cases to make such a distinction.
Therefore the membrane that surrounds the
ovarian ovum will be termed the vitelline mem-
brane or zona radiata without reference to its
theoretical mode of origin.

The ovum escapes from the ovary (ovula-
eon from the vas tion) by rupture of the wall of the follicle, and,
deferens, (After -^^ most vertebrates, is taken up by the oviduct

Ballowitz.) ,, 1 1 • u -x -x X 4-1

through which it passes on its way to the ex-
terior. Within the oviduct it may become surrounded by tertiary
membranes secreted by the wall of the oviduct itself. Tertiary
membranes are lacking in some vertebrates, in others they are
of great importance. Thus in birds the albumen, the shell-
membrane and the shell itself are tertiary membranes.

The principal differences to be emphasized in the ova of ver-
tebrates are, however, in the amount and arrangement of the
yolk contained within the ovum proper. All ova contain more

Fig. 1. — Sperma
tozoon of the pig

INTRODUCTION 11

or less yolk. In the case of mammals (excepting the monotre-
mata: Ornithorhynchus, Echidna, etc., which have large ova)
the yolk is scanty in amount, and quite uniformly distributed
in the form of fine granules; the ovum is, therefore, relatively
very small (mouse, 0.059 mm.; man, 0.17 mm.). Such ova are
often termed alecithal, which means literally without yolk. In
the literal sense, however, no ova are entirely alecithal, so that
it will be better to use the term of Waldeyer, isolecithal. In the
amphibia the yolk is much greater in amount and it is centered
towards one pole of the ovum; the germinal vesicle (nucleus of
the egg-cell), which occupies the center of the protoplasm of the
ovum, is therefore displaced towards the opposite pole of the
ovum. Such ova are termed telolecithal. In the ova of Selachia,
reptiles and birds, the yolk is very much greater in amount and
in consequence the protoplasm containing the germinal vesicle
appears as a small disc, the germinal disc, on the surface of the
huge yolk-mass.

But no matter how large the ovum may become by deposi-
tion of yolk, its unicellular character is not altered. The deposi-
tion of yolk is simply a provision for the nutrition of the embryo.
In the mammals the nutrition of the embryo is provided for by
the placenta; therefore yolk may be dispensed with. In the
absence of such provision the amount of yolk is a measure of the
length of the embryonic period of development. In the amphibia,
for instance, this is relatively brief, for the yolk is soon used up,
and the larva must then depend on its own activities for its nutri-
tion. Therefore the development involves a metamorphosis: the
embryo is born in a very unfinished condition, as a larva (the
tadpole in the case of amphibia), which must undergo an exten-
sive metamorphosis to reach the adult condition. In the reptiles
and birds, however, the amount of yolk is sufficient to carry the
development through to a juvenile condition, before an extrane-
ous food-supply is necessary. The metamorphosis, therefore,
which takes place in free life in amphibia, goes on within the egg
in reptiles and birds. The first form of development is known
as larval, the second as foetal.

The amount and arrangement of yolk also influences very
profoundly the form of the early stages of development. Ova
are classified in this respect as holoblastic and meroblastic. Holo-
blastic ova are those in which the process of cell division (cleav-

12 THE DEVELOPMENT OF THE CHICK

age or segmentation of the ovum), with which development
begins, involves the entire ovum. This occurs where the amount
of the yolk is relatively small and where it is completely inter-
penetrated by sufficient protoplasm to carry the planes of divi-
sion through the inert volk. But where the amount of yolk
becomes very large, or where it is not interpenetrated sufficiently
by the protoplasm, the division planes are confined to the proto-
plasmic portion of the ovum, and the yolk remains undivided.
Such ova are known as meroblastic. In these ova the cellular
part of the ovum forms a blastodisc (germinal disc) on the surface
of the yolk. The ova of Amphioxus, Petromyzontidse, Ganoi-
dea. Dipnoi, Amphibia, Marsupialia, and Placentalia are holo-
blastic; those of Myxinoidea, Teleostei, Selachia, Reptilia, Aves,
and Monotremata are meroblastic.

It is obvious that transitional conditions between holoblastic
and meroblastic ova may occur; such are in fact found among
the ganoids. In Lepidosteus, for instance, the quantity of proto-
plasm in the lower hemisphere is so slight that the division planes
form with extreme slowness. On the other hand, it should be
emphasized that the distinction between holoblastic and mero-
blastic ova is not so much due to amount of yolk as to the defi-
niteness of its separation from the protoplasm. Thus the ova
of some teleosts, particularly of the viviparous forms described
by Eigenmann, are many times smaller than the ova of Necturus
or Cryptobranchus among amphibia. Yet the teleost ovum is
meroblastic, because the protoplasm does not penetrate suffi-
ciently into the yolk, and the amphibian ovum is holoblastic.

Comparison of the Germ-cells. Although it is not within the
province of this book to enter fully into a cUscussion of this ques-
tion, yet it should be pointed out that, in spite of the extreme
differences in the structure of the germ-cells, they are exactly
equivalent in hereditary potency, as is proved by the similar
nature of reciprocal crosses. Their resemblances are in fact
fundamental and their differences must be regarded as adapta-
tions to secure their union. The comparative history of the
germ-cells, that is a comparison of ovogenesis and spermato-
genesis, brings out their fundamental similarity as germ-cells. In
both the ovogenesis and spermatogenesis three periods are clearly
distinguishable, viz. : a period of multiplication, a period of growth,
and a period of maturation. In the period of multiplication

IXTRODUCTIOX 13

the primordial germ-cells, known as ovogonia and spermatogonia
are very similar in their morphological characters; both kinds
are small, yolkless cells containing the typical or somatic number
of chromosomes; they multiply rapidly by karyokinetic division.

At the end of this period multiplication ceases and the germ-
cells increase in size (period of growth). They are now known
as ovocytes and spermatocytes of the first generation. The
growth of the ovocyte is much greater than that of the sperma-
tocyte; deposition of yolk occurs in the ovocyte during this
period, whereas in the spermatocyte no yolk is ever deposited,
though mitochondria may simulate it in appearance. Another
characteristic feature of the period of growth is the reduction of
the number of chromosomes to one half of the typical number,
w^hich takes place, according to the current conception, by union
of the chromosomes in pairs (synapsis) forming one half of the
somatic number of chromosomes, which are, however, bivalent
and are known as tetrads.

At the end of the period of growth the ovocyte of the first
generation is usually many times larger than the spermatocyte,
owing mainly to the amount of yolk formed. But the tw^o kinds
of cells are precisely alike in nuclear constitution. Then comes
the period of maturation, which is the same in both kinds of cells
with reference to the nuclear phenomena, but very different as
regards the behavior of the cell-body. The maturation consists
of two rapidly succeeding karyokinetic divisions: in the case of
the spermatocyte the first division results in the formation of
two similar cells, the spermatocytes of the second order, and the
second maturation division divides each of these equally, forming
two similar spermatids, so that four equal and similar spermatids
arise from each spermatocyte of the first order. Each spermatid
then differentiates into a single spermatozoon. In the case of
the ovocyte of the first order, the first maturation division is
exceedingly unequal; the smaller cell is known as the first polar
bodv, but both cells are ovocvtes of the second order. The second
maturation division usually involves only the large secondary
ovocyte; it is as unequal as the first division and results in the
formation of a second polar body. The division of the first polar
body, where it occurs, is equal. Thus the net result of the matu-
ration division of the ovum is the production of three cells (four
if the first polar body divides), viz., the two (or three) polar bodies

14 THE DEVELOPMENT OF THE CHICK

and the ovum. The size of the polar globules is usually so small
that their elimination makes no appreciable difference in the
size of the ovum proper, but they have, nevertheless, the same
nuclear constitution as the ovum.

The mature ovum (ootid) and the polar bodies are the precise
equivalent of the four spermatids, but whereas each of the latter
becomes a functional spermatozoon, only the ovum on the female
side is functional; the polar bodies lack the necessary protoplasm
and yolk for development, and they therefore die. The polar
bodies must be regarded as abortive ova; and a teleological ex-
planation of the form of maturation of the ovum is afforded by
the consideration that equal maturation divisions would reduce
the amount of protoplasm and yolk in the products below the
minimum desirable for perfect development.

Although the maturation divisions of the ovum and sperma-
tozoon are so dissimilar externally, yet the nuclear phenomena
are exactly alike. The net result of the maturation divisions is
to produce definitive germ-cells containing one half of the somatic
number of chromosomes owing to the reduction by pairing (syn-
apsis) that occurs in both at the beginning of the period of growth.
The somatic number is again restored when the sperm-nucleus
and the egg-nucleus unite in fertilization. Questions of funda-
mental importance for the problems of heredity arise in connec-
tion with the phenomena of maturation and fertilization, but
their consideration lies without the scope of the present book.

VI. Polarity and Organization of the Ovum
Although the ovum is morphologically a single cell, yet, as
the primordium of an individual, it has certain specific properties
that predelineate or foreshadow the main structural features of
the embryo. Polarity is the most general of these features: all
the axes of the ovum are not similar, though they may be equal;
there is one axis around which the development centers; the ends
of this axis are known as the animal and the vegetative poles of
the ovum, and the hemispheres in which they lie are named
correspondingly. In telolecithal ova the yolk is centered in the
vegetative hemisphere, the protoplasm in the animal hemisphere;
even in ova which are called isolecithal there is a tendency for
the yolk to be more abundant in the vegetative hemisphere.
The polar globules are formed at the animal pole; hence their

IXTRODUCTIOX 15

name; they often furnish the only clear indication of polarity
before cleavage begins.

With reference to the heteropolar ovic axis a series of meridia
may be defined, drawn from pole to pole over the surface; likewise
an equator and a series of horizontal zones parallel to the equator.
Thus directions on the surface of the ovum may be defined as
meridional, equatorial, or oblique.

Cleavage takes place with reference to the axis of the ovum.
Thus in holoblastic vertebrate ova the first and second cleavage
planes are meridional, and the third usually equatorial. The
mammalian ovum may form an exception to this rule, though
little is known, as a matter of fact, about the polarity of the mam-
malian ovum. The cleavage of meroblastic ova takes place
likewise with reference to the polarity (see Chap. II); and the
location of the primary germ-layers is determined by the polarity.

Not only is the ovum heteropolar, but in many bilateral
animals, and perhaps in all, it is bilaterally symmetrical before
cleavage begins; that is to say, one of the meridional planes
defines the longitudinal axis of the future embryo, and the direc-
tion of anterior and posterior ends is also predetermined in this
meridian, so that halves of the egg corresponding to future right
and left sides of the embryo may be distinguished. In the frog's
egg the plane of symmetry is marked by a gray crescent that
appears above the equator on the side of the egg that corresponds
to the hinder end of the embryo. This crescent is bisected by
the meridional plane of symmetry. In the hen's egg the plane
of symmetry of the embryo appears on the surface of the yolk
in a line at right angles to the axis of the shell, and the left side
of the embryo is turned towards the broad end, the right side
towards the narrow end of the shell. The same plane of sym-
metry must exist in the ovum prior to cleavage for reasons ex-
plained beyond, although there is no morphological differentiation
in the ovum proper, i.e., the germinal disc or yolk, that indicates it.

This predelineation of embryonic axes within the unsegmented
ovum has been interpreted physiologically as due to gradients in
rate of metabolic processes along the embryonic axes (Child),
which determine the locaUzation of the main developmental
events.

V,'

"^^[Ca}

PART I

THE EARLY DEVELOPMENT TO THE END OF

THE THIRD DAY

CHAPTER I

THE EGG

The parts of a newly laid hen's egg are the shell, shell-mem-
brane, albumen, uDd yolk. In an egg that has been undisturbed
for a short time the yolk floats in the albumen with a whitish
disc, the blastoderm about 4 mm. in diameter, on its upper sur-
face. If the yolk be rotated, it will return to its former position
in a few minutes, owing to the slightly lower specific gravity of
the hemisphere containing the blastoderm. The blastoderm is
the living part of the egg, from which the embrj^o and all its
membranes are derived. It is already in a fairly advanced stage
of development when the egg is laid. The yolk and blastoderm
are enclosed within a delicate transparent membrane (vitelline
membrane) which holds the fluid yolk-mass together. We may
now consider some details of the structure and composition of
the parts of the egg.

The shell is composed of three layers: (1) the inner or mam-
millary layer, (2) the intermediate spongy layer, and (3) the
surface cuticle. The mammillary layer consists of minute cal-
careous particles about 0.01-0.015 mm. in diameter welded to-
gether, with conical faces impinging on the shell-membrane; the
minute air-spaces between the conical inner ends of the mammillae
communicate with the meshes of the spongy layer, which is sev-
eral times as thick, and which is bounded externally by the ex-
tremely delicate shell cuticle. The spongy layer consists of
matted calcareous strands. The shell cuticle is porous, but
apparently quite structureless otherwise. The cuticular pores
communicate with the mesh-work of the spongy layer; thus the
entire shell is permeable to gases, and permits of embryonic
respiration, and evaporation of water.

17

18

THE DEVELOPMENT OF THE CHICK

The shell-membrane consists of two layers, a thick outer
layer next to the shell and a thinner one next the albumen. Both
are composed of matted organic fibers (more delicate in the inner
than in the outer layer), crossing one another in all directions.
At the blunt end of the egg the two layers are separated and
form a chamber containing air that enters after the egg is laid

(Fig. 2).

The physical characteristics of the albumen are too well
known to require description. A dense layer immediately next

3J

ML.

D y.3.

Fig. 2. — Diagram of the hen's egg in section to show relations of the parts.
A. C, Air chamber. Alb., Albumen. Bl., Blastoderm. Chal., Chalaza.
I. S. M., Inner layer of the shell membrane. L., Latebra. N. L., Neck of
Latebra. N. P., Nucleus of Pander. O. S. M., Outer shell membrane, p' v. s.,
Perivitelline space. S., Shell. V. M., Vitelline membrane. W. Y., White
yolk. Y. Y., Yellow yolk.

to the vitelline membrane is prolonged in the form of two spirally
coiled opalescent cords towards the blunt and narrow ends of
the egg respectively; these are the chalazse, so called from a
fanciful resemblance to hail stones. The two chalazse are twisted
in opposite directions. In a hard-boiled egg it is possible to strip
off the albumen in concentric spiral layers from left to right from
the broad to the small end of the egg.

THE EGG

19

The yolk and blastoderm are enclosed within the delicate
vitelline membrane; the yolk is a highly nutritious food destined
to be gradually digested and absorbed by the living cells of the
blastoderm and used for the growth of the embryo. It is not
of uniform composition throughout, but consists of two main
ingredients known as the yellow and the white
yolk. The yellow yolk makes up the greater
part of the yolk-sphere; the main part of the
white yolk is a flask-shaped mass, the bulb of
which, known as the latebra, is situated near
the center of the whole yolk, the neck rising
towards the surface and expanding in the form
of a disc (nucleus of Pander) situated imme-
diately beneath the blastoderm (Fig. 2) ; at its
margin this disc is continuous with a thin peri-
pheral layer of white yolk that surrounds the
entire mass. In addition there are several thin
layers of white yolk concentric to the inner bulb-
shaped mass.i If an egg be opened, a dehcate
hair inserted in the blastoderm to mark its po-
sition, and then boiled hard, a section through
the hair and center of the yolk will show the
above relations quite clearly. The white yolk
does not coagulate so readily as the yellow yolk,
and it may be distinguished by this property as
well as by its Hghter color.

Both kinds of yolk are made up of innumer-
able spheres which are, however, quite different
in each (Fig. 3). Those of the yellow yolk are
on the whole larger than those of the white
yolk (about 0.025-0.100 mm. in diameter) with
extremely fine granular contents. There is no ^P
fluid between the spheres. Those of the white yolk are smaller
and more variable in size, ranging from the finest granules up to

1 The assertion that the thin layers that define the concentric stratifica-
tion of the yellow yolk are of the nature of white yolk is traceable to Meckel
V. Hemsbach, Leuckart, and Allen Thomson. His was not able to satisfy
himself that the characteristic elements of the white yolk occur within these
thin concentric lamellse (Untersuchungen ueber die erste Anlage des Wir-
beltierleibes, p. 2).

Fig. 3. — Yolk-
sphere s of the
hen's egg; highly
magnified. (After
Foster and Bal-
four.)

A. Varieties of
white yolk-spheres.

B. Yellow yolk-

20 THE DEVELOPMENT OF THE CHICK

about 0.07 mm. The larger spheres of the white yolk contain
several highly refractive granules of relatively considerable size
as compared with those of the yellow spheres (Fig. 3), and such
granules may have secondary inclusions. As we shall see later,
the smaller granules of the white yolk extend into the germinal
disc (forerunner of the blastoderm) and grade into minute yolk-
granules contained within the living protoplasm.

The earlier investigators from the time of Schwann regarded the
white yolk-spheres as actual cells (Schwann, Reichert, Coste, His).
His especially laid great stress on this interpretation; he believed that
they were derived from the cells of the ovarian follicle which migrated
into the ovum in the course of ovogenesis, that they multiplied like other
cells, and took part in the formation of certain embryonic tissues. Sub-
sequently he abandoned this position as untenable. The white yolk
spheres are now universally regarded as food matters of a particular sort.

The yolk and albumen are complex mixtures of many different
substances, organic and inorganic, containing all the elements
necessary for the growth of the embryo. Very little is known
concerning the series of chemical changes that go on in them
during incubation.

Chemical Composition of the Hen's Egg. — The following data
on the chemical composition of the hen's egg are taken from
Simon's Physiological Chemistry. For details and literature the
student is referred to the standard text-books of physiological
chemistry.

GENERAL COMPOSITION OF THE YOLK

PER CENT,

Water 47.19-5L49

Solids 48.51-42.81

Fats (olein, pahiiitin, and stearin) 21.30-22.84

Vitelline and other alhumens 15.63-15.76

Lecithin 8.43-10.72

Cholesterin 0.44- 1.75

Cerebrin 0.30

Mineral salts 3.33- 0.36

Coloring matters | q r -q
Glucose J

Analysis of the Mineral Salts

Sodium (NaoO) 5.12- 6.57

Potassium (K/J) 8.05- 8.93

Calcium (CaO) 12.21-13.28

THE EGG 21

PER CENT.

Magnesium (MgO) 2.07- 2.11

Iron (Fe203) 1.19- 1.45

Phosphoric acid, free (Pi'Og) 5.72

Phosphoric acid, combined 63.81-66.70

SiHcic acid 0.55- 1.40

Chlorine Traces.

GENERAL COMPOSITION OF THE ALBUMEN

Water 80.00-86.68

SoHds 13.22-20.00

Albumens 11.50-12.27

Extractives 0.38- 0.77

Glucose 0.10- 0.50

Fats and Soaps Traces

Mineral salts 0.30- 0.66

Lecithins and Cholesterin Traces.

Analysis of the Mineral Ash

Sodium (NaaO) 23.56-32.93

Potassium (KoO) 27.66-28.45

Calcium (CaO) 1.74- 2.90

Magnesium (MgO) 1.60- 3.17

Iron (Fe.Os) 0.44- 0.55

Chlorine (CI) 23.84-28.56

Phosphoric acid (P2O5) 3.16- 4.83

Carbonic acid (CO2) 9.67-11.60

Sulphuric acid (SO3) 1.32- 2.63

Silicic acid (SiO.O 0.28- 0.49

Fluorine (Fl) Traces.

The shell consists of an organic matrix of the nature of keratin
impregnated with lime salts: calcium and magnesium carbonates
about 97 %, calcium and magnesium phosphates about 1 %,
keratin and water about 2 %, trace of iron.

The shell-membrane and the vitelline membrane are stated
to consist of keratin or a closely allied substance.

Formation of the Egg. The organs of reproduction of the
hen are the ovary and oviduct of the left side of the body. Al-
though the right ovary and oviduct are formed in the embryo
at the same time as those of the left side, they degenerate more
or less completely in the course of development (see Chap. XIII),
so that only functionless rudiments remain. This would appear
to be correlated with the large size of the egg and the delicate

22

THE DEVELOPMENT OF THE CHICK

Fig. 4. — Reproductive organs of the hen. (After Duval, based on a figure
by Coste.) The figure is diagrammatic in one respect, namely, that two

THE EGG 23

nature of the shell, as there is not room for two eggs side by side
in the lower part of the body-cavity.

The ovary lies at the anterior end of the kidney attached
by a fold of the peritoneum (mesovarium) to the dorsal wall of
the body-cavity. In a laying hen ova of all sizes are found from
microscopic up to the fully formed ovum ready to escape from
the follicle. Such an ovary is shown in Figure 4; the gradation
in size of the ova will be noticed up to the one fully formed and
ready to burst from its capsule. At 5 in this figure is shown a
ruptured follicle, and the ovum which has escaped from this
follicle is shown in the oviduct at 8. It will be seen that the part
of the definitive hen's egg produced in the ovary is the so-called
yolk. The blood-supply of the very vascular ovary is derived
from the dorsal aorta, and the veins open into the vena cava
inferior.

The oviduct is a large coiled tube (Fig. 4) which begins in a
wide mouth with fringed borders, the ostium tuhce ahdominale
(funnel or infundibulum) opening into the body-cavity near the
ovary. It is attached by a special mesentery to the dorsal wall
of the body-cavity, and opens into the cloaca. The following
divisions are usually distinguished: (1) the funnel or infun-
dibulum, (2) the albumen secreting portion, (3) the isthmus,
(4) the uterus or shell-gland, (5) the vagina (Fig. 4). The albu-
men secreting portion includes all of the coiled tube; the isthmus
is a short section next to the dilated uterus, and the vagina is
the short terminal portion opening into the cloaca (Figs. 4 and 5).

The formation of an egg takes place as follows: the yolk, or
ovum proper, escapes by rupture of the follicle along a preformed
band, the stigma (Fig. 4-4), into the infundibulum, which swallows
it, so to speak, and it is passed down by peristaltic contractions

ova are shown in the oviduct at different levels; normally but one ovum

is found in the oviduct at a time.

1, Ovary, region of young follicles. 2 and 3, Successively larger follicles.
4, Stigmata, or non-vascular areas, along which the rupture of the follicle
takes place. 5, Empty follicle. 6, Cephalic lip of ostium. 7, Funnel of
oviduct (ostium tubse ahdominale). 8, Ovum in the upper part of the ovi-
diic't. 9, Region of the oviduct in which the albumen is secreted. 10, Albu-
men surrounding an ovum. 11, Ovum. 12, Germinal disc. 13, Lower seg-
ment of albumen-secreting portion. 14, Lower part of the oviduct (''uterus,"
shell-gland). 15, Rectum. 16, Reflected wall of the abdomen. 17, Anus, or
external opening of cloaca.

24

THE DEVELOPMENT OF THE CHICK

of the oviduct. The escape of the ovum from the follicle is known
as the process of ovulation. During its passage down the ovi-
duct it becomes surrounded by layers of albumen secreted by

the oviducal glands. The shell-
membrane is secreted in the
isthmus and the shell in the
uterus (Fig. 5). The ovum is
fertilized in the uppermost part
of the oviduct and the cleavage
and early stages of formation of
the germ-layers take place be-
fore the egg is laid. The time
occupied by the o\auii in tra-
versing the various sections
of the oviduct is as follows:
Glandular portion of the ovi-
duct three hours, isthmus one
hour, uterus and laying sixteen
to seventeen hours (combined
observations of Patterson, and
Pearl and Curtis). If the hen
be disturbed eggs may be re-
tained long after they are ready
to be layed.

Some of the details of these
remarkable processes deserve
attention: the observations of
several naturalists demonstrate
that the ripe follicle is em-

FiG. 5. — Uterus (shell-gland) of the
hen cut open to show the fully
formed egg. (After Duval.)
1, Cut surface of oviduct, region of

isthmus. 2 Reflected flap of uterus. ^j,^^^^j ^ ^j^^ ^^^^^^^ of the ovi-

3, Egg ready to be laid. 4, Lower ^

extremity, or vaginal portion, of the duct before its rupture SO that

oviduct 5, Rectum. 6, Opeiiing of ^^^ ^^^^^^^ ^|^^g ^^^ ^^ ^^^^^

the oviduct into the cloaca. /, Open- , , ^

ing of the rectum into the cloaca. 8, the body-cavity, but into the

^^°^^^- oviduct itself. Coste describes

the process in the following way: ''In hens killed seventeen to
twenty hours after laying I have observed all the stages of this re-
markable process. In some the follicle, still intact and enclosing
its egg, had already been swallowed, and the mouth of the oviduct,
contracted around the stalk of the capsule, seemed to exert some
pressure on it, in other cases the ruptured capsule still partly

THE EGG 25

enclosed the egg which projected from the opening; in others
finally the empty capsule had just deposited the egg in the en-
trance of the oviduct." According to Patterson the funnel of
the oviduct becomes inactive as soon as an egg is received, but
about the time of laying it becomes highly active and again clasps
an egg follicle.

The existence of double-yolked eggs renders it probable that
the oviduct can pick up eggs that have escaped into the body-
cavity. But in some cases ova that escape into the body-cavity
undergo resorption there.

Immediately after the ovum is received by the oviduct a
special layer of albumen is secreted which adheres closely to the
vitelline membrane and is prolonged in two strands, one ex-
tending up and the other down the oviduct ; these strands become
the chalazse; the layer to which they are attached may, therefore,
be called the chalaziferous layer (Coste) of the albumen. The
Une joining the attachments of the chalazse is at right angles to
the main axis of the ovum (that passing through the germinal
disc) ; it is obvious, therefore, that there must be some antecedent
condition that determines the position of the ovum in the oviduct;
this is probably the position of the ovum in the folhcle, i.e., the
relation of the germinal disc to the stigma, for the follicular
orientation is apparently preserved in the oviduct. The question
is of considerable importance because, as we shall see, the axis of
the embryo is later bisected by a plane passing through the
chalazse, and is therefore certainly determined at the time that
the chalazffi are formed, and Bartelmez even traces it back to the
earliest stages of the ovocyte.

After formation of the chalazse the ovum passes down the ovi-
duct, rotating on the chalazal axis, and thus describing a spiral
path; the albumen which is secreted abundantly in advance of
the ovum is therefore wrapped around the chalaziferous layer
and chalazse in successive spiral layers and the chalazse are re-
volved in spiral turns.

Only about 50 % of the white of the egg is formed by the albu-
men secreting portion of the oviduct; this is in the form of a
dense layer formed of matted fibers; the shell membrane is de-
posited directly on this; and the more fluid portion of the albumen
constituting 50% or more of its entire bulk enters through the
shell membrane while the egg is in the isthmus and uterus (Pearl
and Curtis, 1912).

26 THE DEVELOPMENT OF THE CHICK

Abnormal eggs are of two main kinds: those with more than
one 3^olk, and enclosed eggs (ovum in ovo). Double-yolked eggs
are obviously due to the simultaneous, or almost simultaneous,
liberation of two yolks, and their incorporation in a single set of
egg-membranes. The two yolks are usually separate in such
cases and are derived, presumably, from separate follicles. But
two yolks within a single vitelline membrane have been observed;
such are in all probability products of a single follicle. Cases of
three yolks within a single shell are extremely rare. The class
of enclosed eggs includes those in which there are two shells,
one within the other. In some cases the contents of the enclosed
and the enclosing eggs are substantially normal, though of course
the enclosing shell is abnormally large; in others the enclosed
egg may be abnormal as to size (small yolk), or contents (no
yolk). In all cases described, the enclosing egg possesses a yolk
(Parker). Abnormal eggs of these three classes are of either
ovarian or oviducal origin; doubled-yolked eggs and eggs with
abnormal yolks are due to abnormal ovarian conditions; enclosed
eggs to abnormal oviducal conditions, or to both ovarian and
oviducal abnormalities. Assuming the normal peristalsis of the
oviduct to be reversed when a fully formed egg is present, the
egg would be carried up the oviduct a greater or less distance and
might there meet a second yolk. If the peristalsis became normal
again, both would be carried to the uterus and enclosed in a
common shell. (For a fuller discussion of double eggs see G. H.

Parker.)

Ovogenesis. The ovogenesis, or development of ova, may
be divided into three very distinct stages. The first stage, or
period of multiplication, is embryonic and ends about the time
of hatching (in the chick) ; it is characterized by the small size of
the ova and their rapid multiplication by division. The multi-
ph'ing primitive ova are known as ovogonia. At the end of this
period multiplication ceases and the period of growth begins.
The ova, known as ovocytes of the first order, become enclosed
in follicles; the size of the ovum constantly increases and the
yolk is formed. The third period, known as the period of matura-
tion, is characterized by two successive exceedingly unequal
divisions of the egg-cell, producing two minute cells, the polar
globules, that take no part in the formation of the embryo, but
die and degenerate. The process of maturation begins in the

THE EGG

27

fully ripe follicle and is completed after ovulation in the oviduct,
while the ovum is being fertilized.

The origin of the primitive ova, their multiplication and
the formation of the primordial follicles is described in Chapter
XIII. In the young chick all the cell cords and cell nests (de-
scribed in Chapter XIII) become converted into primordial
follicles. During the egg-laying period there is a continuous
process of growth and ripening of the primordial follicles, which
takes place successively; the immense majority at any given
period remain latent, but all stages of growth of egg follicles may
be found in a laying hen.

A primordial follicle consists of the ovum surrounded by a
single layer of cubical epithelial cells (granulosa or follicle cells);
the fibers of the adjacent stroma have a concentric arrangement
around the follicle forming the theca folhculi (Fig. 6 Str.). The
ovum itself is a rounded cell with
a large nucleus placed excentri-
cally so as to define a primary
axis of the ovum. In the pro-
toplasm on one side of the
nucleus is a concentrated mass
of protoplasm, the yolk-nucleus,
from w^hich rays extend, and
minute fatty granules.

HoU derives the follicular cells
in birds from the stroma, but on
insufficient grounds. According to
D'Hollander, they are derived, like
the primitive ova, from the germi-
nal epithelium, in which he agrees
with the majority of his predeces-
sors. He states that the period of
multiplication of the ovogonia ends about the time of hatching; that the
period of growth of the ovocytes begins at about the fourteenth da}- of in-
cubation (seven days before hatching), and before the formation of the
primordial follicle, which begins on the fourth day after hatching. Thus
the periods of multipHcation and gro\\i^h overlap.

Although the nucleus (germinal vesicle of authors) is strongly
excentric in position in the youngest ovocytes, it occupies a more
nearly central position in those slightly older. When the ovum is
about 0.66 mm. in diameter, it moves to the surface along the
shortest radius and comes to lie almost in contact with the vitel-

FiG. 6. — Primordial follicle from the
ovary of the hen. (After Holl.)

Gr., Granulosa. N., Nucleus. Str.,
Stroma. Y. N., Yolk nucleus.

28

THE DEVELOPMENT OF THE CHICK

line membrane (Fig. 7). It becomes elliptical, and later the outer
surface is flattened against the vitelline membrane, the inner
surface remaining convex (Fig. 8). The point on the surface to
which the germinal vesicle migrates is situated away from the
surface of the ovary, and thus in the position of the pedicle of

/:S.-

, V Jtr^r '.J*- -*^, V ft Ou/'

Fig. 7. — Section of an ovarian ovum of the pigeon; drawn from a prepara-
tion of Mr. J. T. Patterson. The actual dimensions of the ovum are 1.44
X 1.25 mm.

f. s., Stalk of follicle. G. V., Germinal vesicle. Gr., Granulosa. L.,
Latebra. p. P., Peripheral protoplasm, pr. f., Primordial folhcles. Th. ex.,
Theca externa. Th. int., Theca interna. Y. Y., Yellow yolk. Z. r., Zona
radiata.

the follicle, when the latter projects from the surface of the ovary
(Fig. 7). This determines the position of the future germ disc.
The nucleus increases in size with the growth of the ovum; in the
youngest ovocytes its diameter is about 9 /x; in the ripe ovum it is
flattened and may measure 455 ju in diameter by 72 ^ in thickness.

THE EGG 29

While the nucleus is still near the center of the egg a very
dense deposit of extremely fine granules is formed around it, and
gradually extends out towards the periphery of the cell, but
does not involve the peripheral layer of protoplasm. This central
aggregation of yolk-granules represents the primordium of the
latebra or central mass of the white yolk.

The ovum grows very slowly up to a diameter of about 6
millimeters, and all of the yolk found during this period belongs
to the category of white yolk. Certain of these ova, but only a
few at any one time, then suddenly begin to grow at an enor-
mously increased rate, adding about 4 mm. to their diameter
every twenty-four hours until the full size of al)out 40 mm. in
diameter is attained. It is during this period that the concentric
layers of yellow and white yolk are laid down in the periphery.

Riddle has studied this period by the ingenious method of
feeding the stain Sudan III, which has an especial affinity for fat,
to laying hens at definite time intervals. The stain attaches itself
to fatty acids of the food which are taken up unchanged by the
egg. The consequence is that during any period of Sudan III
feeding a red stained layer of yolk is formed; so that it is possible
by regulating the dose and interrupting the feedings to obtain
ova with alternate bands of stained and unstained yolk. In this
way he was able to show that a layer of yellow and of white yolk
about 2 mm. in combined thickness on the average is laid down
each twenty-four hours.

In a previous study the same author had shown that there is
a daily rhythm of nutrition, associated with high and low blood
pressure, which is responsible for the formation of the alternate
fault-bars and fundamental bars of birds' feathers. It is this same
claih^ rhythm that determines the concentric stratification of the
yolk, yellow yolk being formed during the longer period of high
blood pressure, and white yolk during the briefer nocturnal period
of low pressure.

"The layer of white yolk of the hen's egg is then a growth-
mark left at the ever changing boundary of the ovum ; it represents
the result of yolk formation under sub-optimal conditions."
(Riddle.)

The germinal vesicle lies in a thickening of the peripheral
layer of protoplasm known as the germinal disc, which is con-
tinuous, like the remainder of the peripheral protoplasm, in early

30 THE DEVELOPMENT OF THE CHICK

stages with the protoplasmic reticulum that forms the walls of
the yolk- vacuoles. The germinal disc increases in extent and
thickness, and the peripheral protoplasm disappears over most of
the yolk. An inflow of the peripheral protoplasm into the disc
appears very probable by analogy with the bony fishes where
this process can be studied with great ease.

The method of formation of the neck of the latebra and the
so-called nucleus of Pander, or peripheral expansion of the neck,
follows more or less directly from the preceding account: As the
circumference of the ovum enlarges, the germinal disc is carried
out and leaves behind it a trail in which yellow yolk is not formed.
When the ovum is fully grown, the exact boundaries between the
protoplasmic germinal disc and the yolk are not determinable.
The disc itself is charged with small yolk-granules which grade
off very gradually into the white yolk lying around and beneath

the disc.

The mode of nutrition of the ovum and the formation of the
vitelhne membrane remain to be considered. The nutrition is
conveyed from the highly vascular theca follicuh by way of the
follicular cells, or membrana granulosa, to the ovum. The nutri-
ment enters by diffusion; at no stage is there any evidence of
immigration of sohd food particles, let alone entire cells, into
the growing ovum. At an early stage a definite membrane is
formed between the ovum and the folhcular cells, the zona radiata
or primordium of the vitelhne membrane (Fig. 7). This is
pierced by innumerable extremely minute pores which become
narrow canals as the zona radiata increases in thickness. The
•follicular cells and the peripheral layer of protoplasm of the ovum
are connected by extremely dehcate strands of protoplasm that
pass through the pores (Holl). In some way the nutriment of
the ovum is conveyed through these strands.

The discussion as to whether the zona radiata is a product of
the ovum itself or of the follicular cells seems to me to be largely
academic and wih not be summarized here. There seems to be
sufficient evidence of a primary true vitelline membrane secreted
by the ovum itself, though this may not represent the entire
zona radiata of older ova.

The third phase of ovogenesis, maturation or formation of
the polar globules, is transferred to the next chapter, because it
is overlapped by the process of fertihzation. It is not definitely

THE EGG 31

known if maturation in birds may be completed without fertiliza-
tion, but it seems probable that, as in many other animals, the
completion of maturation is dependent on the stimulus of fertihza-
tion. It is, however, essentially a process absolutely distinct
from fertilization, and in some animals {e.g., echinids) is com-
pleted without fertilization.

CHAPTER II
THE DEVELOPMENT PRIOR TO LAYING

I. Maturation

During the growth period the germinal vesicle has increased
to an enormous size (455 x 72 ju in an ovmn 37 mm. in diameter,
Fig. 8). It lies in contact with the vitelline membrane. The
margins of the lenticular nucleus are folded into the interior in
such a way that sections give an effect of rod-shaped bodies spring-
ing from the membrane which were doubtfully interpreted as

^'-^

Fig. 8. — Vertical section of germinal vesicle of hen's egg after Sonnenbrodt.
Size of egg 37 mm. in diameter; size of nucleus 455Mx72/i.

chromosomes by Holl. The real chromosomes are however in
the center in the form of double rods (Fig. 8). The maturation
divisions of the hen's egg have not been described, but we have
fortunately a very good account of the maturation and fertiliza-
tion of the pigeon's egg by E. H. Harper, which furnishes the
basis of the following description:

The wall of the germinal vesicle begins to break down in
ovarian eggs of about 18.75 mm. diameter, the full size of the egg
of the pigeon being about 25 mm. Part of the fluid contents of
the germinal vesicle flows out and forms a layer outside the disinte-

32

DEVELOPMENT PRIOR TO LAYING

33

grating wall (Fig. 9). The chromosomes and nucleoli form a
group near the center of the upper plane surface of the germinal

Chr

<5£)-^

;.'

G.Tr

-^.<S^' .^ A,.; ^ <^ ,.<^

A

^. r^

ki

-.7?.SjO./'.

'Tetr.

Fig. 9. — Vertical section of the germinal vesicle and part of the germinal
disc of an ovarian ovum | inch in diameter; pigeon, x 385. (After
Harper.)
Chr., Chromosomes. Gr., Granulosa. G. V., Wall of germinal vesicle.

vesicle. The first maturation spindle is formed before ovulation,
containing eight quadruple chromosomes (tetrads). The spindle
is still in the equatorial plate
stage when the ovum is
grasped by the mouth of the
oviduct (Fig. 10). The bulk
of the substance of the ger-
minal vesicle soon forms a
yolk-free cone extending
from the maturation spin-
dle deep into the superficial i _^

yolk. The outer end of the Fig. 10. — Vertical section of the germinal
spindle is in almost imme- ^li^c of the pigeon's egg showing the
diate contact with the SUr- ^""^ maturation spindle. The egg was
c e .. T.I clasped hy the funnel of the oviduct.

lace 01 the ovum. In the o -^ oaaa .vr* u x

8.oO P.M. X 2000. (After Harper.)

later stages of formation of m. Sp. 1, First maturation spindle. Tetr.,
the first polar body each Tetrad.

tetrad, or quadruple chromosome, separates into two dyads or
double chromosomes, and the members of each pair of dyads
separate and approach opposite ends of the spindle (anaphase).

34

THE DEVELOPMENT OF THE CHICK

Thus at each end of the spindle there are eight dyads. Those at
the outer end then enter a Httle bud of jorotoplasm projecting
above the surface of the germinal disc, and this bud with the
dyads is cut off as the first polar body, which lies in a depression
of the germinal disc beneath the vitelline membrane (Fig. 11).
Eight dyads, therefore, remain within the germinal disc.

A second maturation spindle is then formed almost imme-
diately, apparently without the intervention of a resting stage
of the nucleus, and takes a radial position similar to that occupied
by the first, with the dyads forming an equatorial plate (Fig. 11).

■7/.3p.2.

Fig. 11. — Second maturation spindle and first polar body of the pigeon's
egg; a combination of two sections. 8.15 p.m. x 2000. (After Harper.)
m. Sp. 2, Second maturation spindle, p. b. 1, First polar body. v. M.,
Vitelline membrane.

Each dyad then divides along the preformed plane of division,
and the daughter-chromosomes diverge towards opposite poles
of the spindle. The outer end of the second maturation spindle
then enters a superficial bud of the protoplasm of the germinal
disc similar to that of the first maturation spindle; and this bud
together with the contained chromosomes becomes cut off as the
second polar body.

The result of these processes of maturation is the formation
of three cells, viz., the two polar bodies and the mature egg.
The polar bodies are relatively very minute and soon degenerate
completely.

After the formation of the second polar body there remain
in the egg eight chromosomes, each of which represents one
quarter of an original tetrad. These form a small resting nucleus
known as the egg-nucleus or female pronucleus. It is many
times smaller than the original germinal vesicle (Fig. 12), and

DEVELOPMENT PRIOR TO LAYING

35

it rapidly withdraws from the surface of the egg to a deeper
position near the center of the germinal disc. (Concerning the

p.d.I.

p.b.a.

~v.M.

-py.^.

Fig. 12. — Egg nucleus (female pronucleus) and polar bodies

of the pigeon's egg. (After Harper.) 8.30 p.m. x 2000.

E. N., Egg nucleus, p. b. 1, First polar body. p. b. 2,
Second polar body. p'v. S., Perivitelline space, v. M., Vi-
telline membrane.

general theory of the maturation process see E. B. Wilson, "The
Cell in Development and Inheritance/' the Macmillan Company,
New York.)

11. Fertilization

The spermatozoa traverse the entire length of the oviduct
and are found in the uppermost portion in a fertile hen. The
period of life of the spermatozoa w^ithin the oviduct is considerable,
as proved by the fact that hens may continue to lay fertile eggs
for a period of at least three weeks after isolation from the cock.
After the end of the third week the vitality of the spermatozoa
is apparently reduced, as eggs laid during the fourth and fifth
weeks may exhibit, at the most, abnormal cleavage, which soon
ceases. Eggs laid forty days after isolation are certainly unfer-
tilized, and do not develop (Lau and Barfurth). The so-called
parthenogenetic cleavage of such eggs is merely a phenomenon
of fragmentation of the protoplasm; there is no true cell-division.

The ovum is surrounded immediately after ovulation, that is
in the infundibulum, by a fluid containing spermatozoa in suspen-
sion. In the egg of the pigeon from twelve to twenty-five sperm-

36

THE DEVELOPMENT OF THE CHICK

atozoa immediately bore through the egg-membrane and enter the
germinal disc, within which the heads, which represent the nuclei
of the spermatozoa, enlarge and become transformed into sperm -
nuclei (Fig. 13). In the hen's egg five or six usually enter. The
fate of the middle piece and tail of the spermatozoa is not known in

birds, but it is improbable that they furnish
any definitive morphological element of the
fertilized egg. At the time of entrance of
the spermatozoa the first maturation spindle
is in process of formation ; it lies in the center
of a group of granules at the surface of the
egg, which is bounded by a non-granular
zone of protoplasm, called by Harper the
polar ring, in which the sperm-nuclei ac-
cumulate. External to the polar ring the
protoplasm is granular again (Fig. 14).

The sperm-nuclei remain quiescent while
the polar bodies are being formed, and,
when the egg nucleus is reconstituted, one
of them, which may be called the male pro-
nucleus or primary sperm nucleus, moves
inwards and comes into contact with the
egg nucleus (Fig. 15). The opposed faces
of the conjugating nuclei become flattened
together, until the contours form a single
sphere, the first segmentation nucleus, in which a partition sep-
arates the original components, viz., the sperm and egg nucleus.
The partition apparently disappears. However, it is very un-
likely that a complete intermingling of the contents of the two
germ-nuclei takes place, because in other groups of animals where
the processes have been more fully studied, it has been determined
that each germ-nucieus forms an independent group of chromo-
somes of the same number in each.

Shortly after its formation, the first segmentation nucleus
prepares for division in the usual karyokinetic way. The first
segmentation (or cleavage) spindle thus formed lies near the
center of the germinal disc a short distance beneath the surface
and its axis is tangential to the surface, or, in other words, at
right angles to the axis of the egg. The fertilization may be
considered to be completed at this stage.

Fig. 13. — Stages in
the transformation of
sperm heads into the
sperm nuclei from the
ovum of the pigeon.
x2000. (After Har-
per.) The order of
stages is indicated by
the letters a — g.

DEVELOPMENT PRIOR TO LAYING

37

The entrance of several spermatozoa appears to be character-
istic of vertebrates with large ova; thus for instance, it has been
described in selachii, some amphibia, reptiles, and birds. Such
a condition is known as polyspermy; it is normal in the forms
mentioned, but occurs only under abnormal conditions in the

m

i'^1'--.'-.

WM^S-y--]':-^^^^^^^^^^^

'^^■'

'-.-.■.■■

Fig. 14. — Horizontal section of the germinal disc of a pig-
eon's ovum immediately after ovulation, x 125. (After
Harper.)
N., Nucleus, probably first maturation spindle, p. r.,

Polar ring. Sp. N., Sperm nuclei.

V^

/■'itft AV^,

W

.--o

"1

.J

Fig. 15. — Vertical section of the pigeon's egg showing germ nuclei
(pronuclei) in the center of the disc, x 2000. 10.40 p.m. (After
Harper.)

38 THE DEVELOPMENT OF THE CHICK

great majority of animals. Harper observed that the number
of sperm-nuclei formed in the pigeon varied from, twelve to twenty-
five in different cases. Only one of these serves as a functional
sperm-nucleus; the remainder or supernumerary sperm-nuclei
migrate, as though repelled, from the center towards the margins
and deeper portions of the germinal disc, where they become
temporarily active, dividing and furnishing a secondar}- area of
small cells (accessory cleavage) surrounding the true cleavage-
cells produced by division of the central portion of the disc around
the descendants of the segmentation nucleus. It has been sup-
posed by some authors who studied the selachii that the de-
scendants of the supernumerary sperm-nuclei form functional
nuclei of the so-called periblast, but this view has been disproved
for the pigeon (Blount), in which it can be demonstrated that
the supernumerary sperm-nuclei have but a brief period of
activity, and then degenerate.

III. Cleavage of the Ovum

The fertilized ovum is morphologically a single cell, with a
single nucleus, the first segmentation nucleus. The living proto-
plasm is aggregated in the germinal disc, and the remainder of
the ovum is an inert mass of food material destined to be assimi-
lated by the embryo which arises from the germinal disc. The
first step in the development is a series of cell-divisions of the
usual karyokinetic type, restricted to the germinal disc, which
rapidly becomes multicellular. As the early divisions take place
nearly synchronously in all the cells, there is a tendency for the
number of the cells to increase in geometrical progression, fur-
nishing 2-, 4-, 8-, and 16- etc., celled stages; but sooner or later
the divisions cease to be synchronous. All of the cells of the
body are derived from the germinal disc, and the nuclei of all
cells trace their lineage back to the first segmentation nucleus.
The supernumerary sperm-nuclei do not take part in the forma-
tion of the embryo.

Cell-division is the most conspicuous part of the early de-
velopment; hence this period is known as the cleavage, or
segmentation, period. But it should be remembered first, that
cell-division is as constant a process in later embryonic stages as
in the cleavage period, and second, that it is probable, though
little is known yet about this subject in the bird's egg, that

DEVELOPMENT PRIOR TO LAYING 39

other important phenomena are going on during the cleavage
period.

The type of cleavage exhibited by the bird's egg is known
as meroblastic, for the reason that only a part of the ovum is
concerned, viz., the germinal disc. This is obviously due to the
great amount of yolk (see Introduction, pp. 11 and 12).

To understand the form and significance of the cleavage of
the bird's egg, it is necessary first of all to gain a clear idea of the
structure of the germinal disc and its relations to the yolk. At
the time of the first cleavage the germinal disc is round in surface
view and about 3 mm. in diameter; the center is white and is
surrounded by a darker margin about 0.5 mm. wide. These
two zones have been compared to the pellucid and opaque areas
of later stages. We shall call the outer zone the periblastic zone,
or simply periblast. In section, the germinal disc is biconvex,
but the outer surface which conforms to the contour of the entire
egg is much less arched than the inner surface. The disc is every-
where separated from the yellow yolk by a layer of white yolk
(Fig. 2) ; on the other hand, there is no sharp separation between
the disc and the white yolk. The granules of the latter are largest
in the deeper layers and there is a gradual transition from them
to the smaller yolk-granules with which the disc is thickly charged
(Fig. 19). It is practically impossible in a section to say where
the protoplasm of the disc ceases; it is indeed probable that it
extends some distance into the white yolk both beneath and
around the margins of the disc. Thus in Figure 21 a cone, ap-
parently of protoplasm, extends into the neck of the latebra a
considerable distance. In other cases it does not extend so far.

The Hen's Egg. The form of cleavage of the hen's egg is
illustrated in Fig. 16, A-E. The first cleavage appears in surface
view as a narrow furrow extending part way across the germinal
disc (Fig. 16 A). According to Patterson it occurs just as the egg
is entering the isthmus about three hours after the estimated time
of fertilization. While the ends of the first cleavage furrow are
still extending towards the periblast, the second division begins.
It is a vertical division in each cell like the first, and the two fur-
rows meet the first cleavage furrow at right angles. They may
meet the first furrow at approximately the same point, in which
case they form an approximately straight hne (Fig. 16 B), or they

40

THE Df:VELOPMENT OF THE CHICK

B

D

Fig. 16. — Five stages of the cleavage of the hen's egg. (A, B,
D and E after KolUker; C after Patterson.)

A. First cleavage furrow (x 14). The egg came from the
lower end of the oviduct. . , .

B. Four-celled stage (xl7); from the uterus.

C. Eight-celled stage (x 18). u ^ ^a^

D. Nine central and sixteen margmal cells (x about iOj.

E. Late cleavage stage (x about 22).

DEVELOPMENT PRIOR TO LAYING 41

may meet the first cleavage furrow at separate points, in which
case the intervening part of the first furrow becomes bent at an
angle, forming a cross furrow. The third set of cleavage planes
are vertical like the preceding planes, but they tend to be variable
otherwise. In Fig. 16 C there is shown an eight-celled stage in
which three of the new furrows are approximately at right
angles to the second cleavage plane, but other arrangements are
found.

Before describing the later cleavage stages, we should note
certain important relations of the first four or eight cells: First,
these are not complete cells in the sense that they are separate
from one another. They are, indeed, areas with separate nuclei
marked out by cleavage furrows in a continuous mass of proto-
plasm. The furrows do not cut through the entire depth of
the germinal disc, and the cells are therefore connected below
by the deeper layer of the protoplasm; nor do the furrows extend
into the peril^last, and all the cells are therefore united at their
margins by the unsegmented ring of periblast. Second, accord-
ing to several observers, the center of the cleavage, i.e., the place
where the first two cleavage furrows cross, is sometimes excentric.
It was believed by those who emphasized this point, that the
displacement is towards the posterior end of the blastoderm; but
Coste, for instance, failed to note any excentricity, and Patterson
noticed both conditions, and showed that the displacement might
even be towards the anterior end of the blastoderm. In the
pigeon, according to Miss Blount's observations recorded below,
excentricity appears to be exceptional; moreover, the excentric
area may bear any relation whatever to the future hind end of
the embryo, so that in the pigeon it will not bear the interpreta-
tion that has been placed on it in the hen's egg.

The following cleavages (after the eight-celled stage) in the
hen's egg are very irregular, but two classes of furrows may be
distinguished in surface view: (1) those that cut off the inner
ends of the cells, and (2) those that run in a radial direction.
The furrows of the first class produce a group of cells that are
bounded on all sides in surface view, l)ut these are, at first, still
connected below l)y the deeper protoplasm. They may be called
the central cells. These are bounded by cells that are united
in the marginal periblast, and thus lack marginal boundaries as

42

THE DEVELOPMENT OF THE CHICK

well as deep boundaries; they may be called the marginal cells
(Fig. 16 D). The distinction between central and marginal
cells is one of great importance which should be clearly
grasped.

In the surface views of later cleavages the following points
should be noted: (1) the group of central cells increases by the
addition of cells cut off from the inner ends of the marginal cells,
and by the multiplication of the central cells themselves; (2) the
marginal cells increase by the formation of new radial furrows.
The increase of the central cells is much more rapid than that of

Fig. 16 A. IMedian section of a blastoderm of the hen's egg which showed
about 64 cells in surface view (after Patterson). S.c, segmentation
cavity.

the marginal cells, and the cells themselves are much smaller than
the marginal cells, both because of their mode of origin and also
because of their more rapid multiplication. The area of the
central cells is also constantly increasing, with consequent re-
duction of the marginal zone (Fig. 16 E). Emphasis has been
laid by several authors on the excentric position of the smallest
cells, and the inference has been drawn that these represent the
hinder end of the glastodisc. Similar excentricity in the pigeon's
egg is without reference to the future embryonic axis (see
Fig. 18).

But the surface views do not show what is going on in the
deeper parts of the germinal disc. At the eight-celled stage a
narrow space appears in the depth of the central portion of the
blastoderm approximately between protoplasm and yolk; this is

DEVELOPMENT PRIOR TO LAYING 43

the segmentation cavity which furnishes a lower boundary to the
central cells. In later stages it extends peripherally to the inner
margin of the periblast, and thus all of the central cells become
completely bounded. A new class of cleavage planes then forms
in these cells after the thirty-two-celled stage, horizontal or parallel
to the surface; in this way the central part of the blastoderm
becomes two cell-layers deep, and later several layers deep. The'
segmentation cavity never cuts under the marginal cells, which
remain united below and at their margins by the periblast (Fig.
16 A).

In the older accounts of the horizontal cleavages by Kolliker, Duval
and others these are represented as forming before the segmentation
cavity, thus leaving the deeper cell in continuity ^\ith the yolk. Such
cells are then supposed to continue budding off cells from their upper
surfaces. But this view has been shown to be incorrect by the observa-
tions of ^Miss Blount on the pigeon described below and by Patterson on
the hen included above.

The Pigeon*s Egg. The cleavage of the pigeon's egg has
been worked out in detail by Miss Blount; as it must be made the
basis of the description of the formation of the germinal wall and
the germ-layers in the absence of anj^ consistent account for the
hen's egg, it will next be described. The fundamental features of
the cleavage are the same as in the hen's egg, so that the descrip-
tion need not be repeated.

The feature to be particularly emphasized in the cleavage
of the pigeon's egg is the occurrence of a secondary or accessory
cleavage in the marginal zone or periblast (Figs. 17 and 18 A).
When the origin of these cells is traced it is found that they arise
around the supernumerary sperm-nuclei, which accumulate and
multiply in the periblast. The complete history of these nuclei
has been worked out ])y Harper and Blount, so that there
can be no doubt as to their derivation. Another interesting
point illustrated by the figures is that the marginal cells have
a peripheral wall wherever the accessory cleavage occurs, but
between the groups of accessory cleavage cells the marginal cells
are continuous with the periblast (Figs. 17 and 18 A,) as they are

44

THE DEVELOPMENT OF THE CHICK

every\vhere in the hen's egg. In a section of a germinal disc,
showing the accessory cleavage (Fig. 20), it is seen that the
peripheral boundary of the marginal cells cuts under the margin
for a considerable distance.

The accessory cleavage becomes manifest at the time of
api^earance of the first cleavage plane, and increases in amount

Fig. 17. — Photograph of an eight-celled pigeon ovum
(after Mary Blount). 2.45 a.m. Accessory cleavage
(ac. el.) in the marginal zone bounding the segmented
area. Vesicles, appearing black in the photograph,
are seen on the surface of the yolk beyond the mar-
ginal zone of the germinal disc. Orientation as in
Fig. 18.

up to about the 32-celled stage, and thereafter gradually decreases
until it completely disappears (Figs. 18 B, C, and D). The
peripheral boundaries of the marginal cells disappear "pari passu,
and, when the accessory cleavage is finally wiped out, the mar-
ginal cells are everywhere continuous with the periblast, as in
the hen's egg (Figs. 18 B and C). In some eggs the accessory
cleavage is much more extensive than in others; indeed, in some
it appears to be entirely absent, but this is relatively rare. In
the stage shown in Fig. 18 B. for instance, there is usually con-
siderable accessory cleavage; but in this egg there is none. The
variation is obviously due to variations in the number of super-
numerary spermatozoa, such as mav readilv occur.

DEVELOPMENT PRIOR TO LAYING

45

The question arises whether the disappearance of the cell-
walls around the sperm-nuclei is caused by degeneration of the
latter, or is simply a later syncytial condition in the periblast in

B

C

D

Fig. 18. — Photographs of the cleavage of the pigeon's ovum (after Mary
Blount). The figures are so arranged that the axis of the shell is across
the page with the large end to the left. The future axis of the embryo
is therefore inclined 45° to the margin of the page with the anterior end
to the right above.

A. A very regular sixteen-celled stage; accessory cleavage well shown;
thouffh not well focused on the lower margin. 3.45 a.m.

B. Approximate thirty-two celled stage. There is no accessory cleavage
in this case. The formation of the central from the marginal cells may be
readily observed in this figure. 5.15 a.m.

C. Later stage of cleavage. 7.10 a.m.

D. CleavaQ:e at 9.30 a.m. The marginal cells are now becoming separated
peripherally from the periblast which has received its nuclei from them.

which the sperm-nuclei are embedded. There can be little doubt
that the former alternative is correct. While in the stages of
the accessory cleavage, sperm-nuclei are readily found ]:)oth in

46

THE DEVELOPMENT OF THE CHICK

the accessory cleavage-cells and also in the unsegmented periblast
(Figs. 19 and 20), they decrease in number as the accessory
cleavage planes disappear, and when the latter are entirely lost

■ « 4» V a* '^

■'M

Fig. 19. — Transverse section of the blastoderm of a pigeon's egg about
8| hours after fertilization (4.45 a.m.). (After Blount.)
1, Accessory cleavage. 2, Migrating sperm-nuclei, a, b, c, d, Cells of
primary cleavage.

the periblast is absolutely devoid of nuclei. Fragmentation of the
sperm-nuclei is a frequent accompaniment of their disappearance.
Thus the accessory cleavage is a secondary and transient
feature of the cleavage of the pigeon's egg due to polyspermy.
After it has passed, the ovum is in precisely the same condition

• .'•• * • •■•*■.■."•.••;•■.■■.■■'•■.•.' .• ■ ••• • ' ••
■. • ••.•.:.••••.;.•••*.■•■.'. • ••

» •■ ••». •.••■".••;
• •. . •. • • • • • • •

Fig. 20. — Transverse section of the blastoderm of a pigeon's egg at the end
of the period of multiplication of sperm-nuclei, about 10 hours after fertil-
ization (6.30 A.M.). (After Blount.)

1, Accessory cleavage around the sperm-nuclei. 2, Marginal cells; sharply
separated from the sperm-nuclei. 3, Central cells. 4, Sperm-nuclei.

as the hen's ovum of the same stage of development. In the hen's
egg Patterson has shown that there is a very limited and incon-
spicuous accessory cleavage (see Fig. 16 C) around the fewer
supernumerary sperm-nuclei that occur. But most of these nuclei
in the hen tend to pass into deeper portions of the disc and there
undergo complete fragmentation without producing superficial
furrows.

Another feature brought out by these photographs requires
emphasis. The periblast ring shows no definite outer margin.

DEVELOPMENT PRIOR TO LAYING 47

but beyond the zone of the accessory cleavage there may occur
two or three concentric circles variously indicated (Fig. 17).
Vacuoles, appearing black in the photographs, are very common
in the outer zones. These appearances indicate that the peii-
blastic protoplasm extends farther out in the superficial white
yolk than is usually believed to be the case; and this suggests an
interesting comparison with the teleost ovum, where the peri-
blastic protoplasm surrounds the entire yolk as a ver}- thin layer.
Sections confirm the idea that the periblastic protoplasm has an
extension beyond the so-called margin of the blastodisc. Some
eggs show a more definite margin than others; it may be that
there is a periodic heaping of the periblast at the margins, for
which again an analogy may be found in teleosts.

Although the smallest cells may be more or less excentric in
the segmented germinal disc of the pigeon, their position bears
no constant relation to the future embryonic axis. They may
lie in this axis in front of or behind the middle, or to the right or
left of it (cf. Fig. 18 A-D).

At the eight-celled stage a horizontal fissure begins to ap-
pear beneath the central cells (Fig. 19). This marks the full
depth of the blastoderm at all stages, and the several-layered
condition arises by horizontal cleavages between this and the
surface. Comparison of Figs. 19, 20, and 22, drawn at the same
magnification, will show that the depth does not increase by addi-
tion of cells cut off from below, as was once supposed to be the
case in the bird's ovum. The horizontal fissure not only marks
the full depth of the blastoderm, but it also indicates the site
of the segmentation cavity which arises gradually by accumula-
tion of fluid between the cells and the underlying unsegmented
protoplasm and yolk. The segmentation cavity gradually ex-
tends towards the margin of the blastoderm, but it is bounded
peripherally by the zone of junction between the marginal cells
and the periblast.

IV. Origin of the Periblastic Nuclei, Formation of the

Germ- WALL

Our knowledge of this part of the subject in the hen's egg is
very incomplete, and the various accounts are contradictory.
The reason for this is the great difficulty of securing a complete
series of stages, and of arranging them in proper sequence. There

48 THE DEVELOPMENT OF THE CHICK

is no way of timing the development, so that one has to judge
the sequence of the stages, all of which come from the utertis, by
the degree of formation of the shell, by the size of the cells and
by the appearance of the sections. This can be at best only
approximate; and, as the securing of any given stage is largely
a matter of chance, no one has, as a matter of fact, secured a
complete series. In the pigeon, on the other hand, the time
since laying the first egg is a fairly exact criterion of the stage
of development of the second egg. It has, therefore, been pos-
sible to secure a complete series, and the subject has been worked
out by Miss Blount, whose publications furnish the basis of the
following account.

The periblast ring is entirely devoid of nuclei after the super-
numerary sperm-nuclei have degenerated. The marginal cells
become greatly reduced in size owing to multiplication and
continuous production of central cells, and their nuclei thus
approach more and more closely to the periblastic ring. The
scene then changes; the marginal cells cease to produce central
cells; when their nuclei divide the peripheral daughter-nuclei
move out into the periblast, which is thus converted into a nu-
cleated syncytium. The periblastic nuclei multiply rapidly and
invade all portions of the periblastic ring, which maintains its
original connection with the white yolk. Not only do the peri-
blastic nuclei invade the periblastic ring, but some of them also
migrate centrally into the protoplasm forming the floor of the
segmentation cavity. They do not, however, reach the center,
but leave a non-nucleated sub-germinal area, corresponding
approximately to the nucleus of Pander, free from nuclei. The
subgerminal syncytium may be known as the central periblast
to distinguish it from the marginal periblast. They are, of
course, continuous. In sections one has the appearance of nuclei
in the yolk, for there is no sharp boundary between peril)last
and yolk (Fig. 22). The syncytium, which has received its nuclei
from the marginal cells, is the primordium of the germ-wall (Figs.
21, 22, 23, 24).

There is a snarp contrast between the segmented blastoderm
and the syncytial periblast not only in structure but also as
regards fate. The marginal cells constitute a zone of junction be-
tween blastoderm and periblast. Thus in Fig. 22 it will be ob-

DEVELOPMEXT PRIOR TO LAYIXG

49

served that the large marginal cells on each side are continuous
with the periblast, and nuclei are found in the periblast both
central and peripheral to the zone of junction. The latter forms

,u.^=,^^

j00^^^t^^ik^

• ■

Z

• •

• ■

•:•.•.•.•■. ♦•**/« •-*«
•■■•••• -I-i**'-'

: • •••••♦

re ^

5

*.

* '

• • • .

• • ■

•
•

'-': •. ':•# •^^

■:•• .♦#» « i; o

■.; . « %

* *

•

•

^, ^

Km

■> ■■

•

• •

•
•

•

• '■■'■

» ,s.

I

Fig. 21. — Longitudinal section of the blastoderm of a pigeon's egg at the
time of disappearance of the sperm-nuclei. On the left (anterior) margin,
the marginal cells have become open, that is, continuous with the peri-
blast, as contrasted with Fig. 20. About 11 hours after fertilization (7.00
A.M.). (After Blount.)

1, Marginal cells. 2, Cone of protoplasm. 3, Marginal periblast. 4, Neck
of latebra. 5, Yellow yolk.

Fig. 22. — Transverse section through the center of the blastoderm of a

pigeon's egg, 14^ hours after fertilization (10.30 a.m.). (After Blount.)

1, Marginal cells. 2, Marginal periblast. 3, Nuclei of the subgerminal
periblast.

50 THE DEVELOPMENT OF THE CHICK

a ring around the blastoderm. It persists during the expansion
of the blastoderm over the surface of the yolk.

The blastoderm now begins to expand, owing largely, at first,
to additions of cells to its margin cut off from the periblast. The
central as well as the marginal periblast contributes to the blas-
toderm, but the former appears to be rapidly used up. The mar-
ginal periblast, which is commonly called the germ-wall from
this stage, on the other hand grows at its periphery while it adds
cells to the blastoderm centrally, and thus it moves out in the
white yolk, building up the margin of the blastoderm at the same
time. The original group of central cells appears to correspond
approximately to the pehucid area; the additions from the germ-
wall would thus constitute the opaque area.

eanization into cells. 4, Vacuoles

fe

Some phases of these processes are illustrated in Figs. 23 and
24. In the vertical section. Fig. 23, the surface of the germ-
wall next the blastoderm is indented as though for the formation
of superficial cells. Along the steep central margin of the germ-
wall groups of cells are apparently being cut off and added to
the cellular blastoderm. In the horizontal section, Fig. 24, the
process of cellularization at the central margin of the germ-wall
is apparently proceeding rapidly.

The superficial cells thus added to the margin of the cellular
blastoderm become continuous with the ectoderm, and the
deeper layers later form the yolk-sac entoderm which becomes
continuous with the embryonic entoderm secondarily. We can

DEVELOPMENT PRIOR TO LAYING

51

thus distinguish a syncytial, more peripheral, and a cellular, more
central, portion of the germ-wall.

Fig. 24. — Part of the margin of a horizontal section

through the blastoderm of a pigeon's egg about 25 hours

after fertiHzation (8.50 p.m.). (After Blount.)

1, Periblast nuclei. 2, 3, Cells organized in the periblast.
4, A cell apparently added to the blastoderm from the
periblast. 5, Vacuoles.

In later stages the central margin of the syncytial part of the
germ-wall becomes much less steep, owing apparently to active
proHferation of cells. This is illustrated in Fig. 25. Later yet

B o

Fig. 25. — Outlines of the margins of transverse sections
of the blastoderm of pigeon's eggs; 26 (A), 28 (B), and
32 (C) hours after fertilization. (After Blount.)

52 THE DEVELOPMENT OF THE CHICK

the external margin extends out peripherally and forms a short
projecting shelf, appearing wedge-shaped in section (Figs. 28 A,
etc.). This we shall call the margin of overgrowth.

Thus we may distinguish the following zones: (1) margin of
overgrowth; (2) zone of junction with the yolk (syncytial germ-
wall); (3) the inner zone of the germ-wall, and (4) the original
cellular blastoderm (pellucid area) Fig. 29.

V. Origin of the Ectoderm and Entoderm

The ectoderm and entoderm are the primary germ-layers,
out of which all organs of the embryo differentiate; hence great
importance attaches to the mode of their origin. But until recently
it was not possible, in the case of the chick, to decide between
three conflicting views. These are: (1) The theory of delamina-
tion, viz., that the superficial cells of the segmented blastoderm
form the ectoderm and the deeper cells the entoderm; in other
words, that the blastoderm splits into the two primary germ-
layers. This is the oldest view, but it has not lacked support in
recent times, e.g., by Duval. (2) The theory of invagination, viz.,
that the primary entoderm arises as an ingrowth from the
margin of the blastoderm. This view, which was supported
by Haeckel, Goette, Rauber, and some others, brings the mode
of gastrulation in the bird into line with lower vertebrates. (3) A
third and relatively recent point of view is that the primary
entoderm arises as an ingrowth of cells from the germ-wall,
more particularly from the posterior portion. This view, put
forward by Nowack, has been adopted in substance by 0.
Hertwig (Handbuch der vergl. u. exp. Entwickelungslehre der
Wirbeltiere).

The conflict of opinion was due to the fact that the critical
stages occur prior to laying, and no one had investigated a com-
plete series of stages until recently. The investigations of J. T.
Patterson on the pigeon have, however, cleared the matter up.
A very complete series of stages of the pigeon's ovum was studied,
with results that are consistent in themselves and that agree with
the principles of formation of the primary germ-layers in the
lower vertebrates.

The first step in the process of gastrulation, or formation of

DEVELOPMENT PRIOR TO LAYING 53

the primary entoderm, is a thinning of the blastoderm, wliich
begins sHghtly posterior to the center and rapidly involves a
sector of the posterior third of the blastoderm. This process
occurs between twenty and thirty-one hours after fertilization.
It is due apparently to the gradual rearrangement of the cells
in a single layer. A late stage of this process is shown in Figure
26, which represents a complete longitudinal section through the
Ijlastoderm thirty-one hours after fertilization. It will be ob-
served that the anterior portion of the blastoderm is several cells
thick (26 A), but as one passes towards the posterior end the
number of layers becomes less, and is reduced to a single
layer at the extreme posterior end. Here and there, e.g., at X,
the arrangement of the cells indicates that cells of the lower
layer are entering the upper layer. It is obvious that such a
process must result in increase of the diameter of the blas-
toderm, and Patterson states that the average diameter twenty-
one hours after fertilization is 1.915 mm. and 2.573 mm. ten
hours later. The thinning also involves enlargement of the
segmentation cavity, which may now be known as the subgerminal
cavity.

Hand in hand with the thinning out there takes place an
interruption of the germ-wall at the posterior end, so that in this
region the margin no longer enters a syncytium but rests directly
on the yolk (cf. anterior and posterior ends of Fig. 26).

Figure 27 is a reconstruction of the stage in question. The
germ-wall, represented by the parallel lines, is absent at the
posterior end. Here the cells of the blastoderm rest directly
on the yolk. The sector bounded by this free margin and the
broken line represents the area of the blastoderm that is
approximately one cell thick. The figures 2 to 7 indicate
regions approximately two to seven cells thick.

Gastrulation begins by an involution or rolling under of the
free margin, as though the free edge were tucked in beneath the
blastoderm. The involuted edge then begins to grow forward
towards the center of the blastoderm, and thus establishes a lower
layer of cells, the primary entoderm. As soon as this process
is started the margin of the blastoderm begins to thicken, and
thus the inner layer of cells (entoderm) and the outer layer of
cells (ectoderm) are continuous with one another in a marginal
thickening (Fig. 28).

^®

©si;-

ks/S;

Sf?)-^

•••i

.a.

er;

./.••

:r;'^r

^;f^'

:•.•: ^

03.

'•;•

^••*

'^ m

• w
••••

^^

o

o ■»

^ o

o

^-^ o

Ph

ci P-t
1—1

c" *>

O =3

S3 O

-1^ c3

^ to

CO i:^

- ^ 5r

P ^ ^

U
tt.

o o 2

fcJD '^M

A O <D

c
o

e3

0)

1=1
o

o

o

is o
^ '-^ •

fc£ GJ ^

^1 S o

a

n "=^

•^ .2 -*^

S -5 So
2<< -

o

OQ

DEVELOPMENT PRIOR TO LAYING

55

The margin of invagination is known as the Up of the blasto-
pore or primitive mouth; the space between this margin and
the yolk is the blastopore, and the space between the entoderm
and yolk, derived from part of the subgerminal cavity, is the
archenteron or primitive intestine.

Fig. 27. — Diagrammatic reconstruction of the blasto-
derm of which a longitudinal section is shown in
Fig. 26.

C-D., Plane of Fig. 26.

G. W., Germ-wall. 1, 2, 3, 4, 5, 6, and 7 indicate
regions of the blastoderm which are approximately from
1 to 7 cells deep respectively. The broken line around
1 indicates the region where the blastoderm is approxi-
mately one cell deep, x 27.2. (After Patterson.)

The first stage in the formation of the entoderm is interpreted
as involution of the free margin, and this view is supported by
the fact, determined by Patterson, that the antero-posterior
diameter of the blastoderm is shorter than the transverse diameter
during this process, whereas previously the blastoderm was
approximately circular. An even stronger support of this view
is furnished by experiments which demonstrate that injuries to
the margin made just prior to gastrulation appear later in an

«;^^ •-

•SI;.*! f:-;X-'"» I

vs^ ».; •) "5 -^•- - -1 - -^

'■» ■ .".••.:•• i ,
.•:.-;•..••..■.••• <

• ■ C^

o

ft

O

o

CO

o
;-!

CO

5

I a

IE

^ ^-^ '-^

o: ^ ^

L^ ^ -^

►^ '"o ' £c

^ c = .
o !h c -:;

s ;::

GJ >^ C

s;

CS-, VS* • • • • O »

■ r

9 •

:••

o

*^ O ^-i ""^

o ^ - —

S "::: r S
?-< ^ '\- _

<^ o <^
^ O =£-=£

^ >-< t B
jh o ;^ ,,

n-i '^ =*- "";

O =i i-

_: J- i,

c S - -2

•_^ c <; i.

• S -^^ C -^
> -= b

G .S S ->'

o ^j ?■ r; w rr
b£. ^ O E it -

• -^ "^ -^ r ^J ^-^

^ " c "S ^ -^

jH o -^ W ^ ^

•-•^ a --7- r
C2 o Qj , -; ^ -
O o X W c -

-^ t_ '-^ Jt =t
c2^ O .^ O

o

c
.2

CD

m

bJj

C
O

1 O _

GO C O •

6
1—1

DEVELOPMENT PRIOR TO LAYING

57

anterior position in the entoderm (Patterson). But after the
margin has thickened the farther extension of the entoderm is
due, largely at least, to ingrowth from the marginal thickening.

Patterson also believes that the thickening of the margin is
due not so much to multiplication of cells in situ as to immigration
of cells from the sides. This view is also supported by experi-
ments.

C E

D F H

Fig. 29. — Diagrammatic reconstruction of the blastoderm of a
pigeon's egg, 36 hours after fertilization; from the same series as
Fig. 28. X 27.2. (After Patterson.)

E., Invaginated or gut entoderm. O., Margin of overgrowth.
PA., Outer margin of pellucid area. R., Margin of invagination
(dorsal lip of blastopore). S., Beginning of yolk-sac entoderm.
Y., Yolk zone. Z., Zone of junction.

The arrows at the posterior margin indicate the direction of
movement of the halves of the margin. The circles in the pellucid
area indicate yolk masses in the segmentation cavity.

Figure 29 is a reconstruction of a blastoderm in the stage of
Fig. 28, that is at the height of gastrulation. The margin of
overgrowth (cf. Fig. 28 O) is represented by the area O; the
zone of junction by the ruled area Z; the inner portion of the

ii-r^

^1

O

O

<11

O

;->

c5

o

o
03

O

00

CO

bO
be
<D

jc

"c
o

bJD

03

S

o

o
o

0)

o

H

o
;-<
O

o

u

02

o

0^ O
03 O

■^ o

o .2
o .S

02

CI

o

c3 Qj
_C CO

c o

C
O ^

CO pq

o

X

'^ fcX)

<D

r o

^^

u, o3
.0 g

bJD

o3

>

< <

DEVELOPMENT PRIOR TO LAYING

59

germ-wall by the area with large granules Y. These zones con-
stitute the opaque area. The circles in the pellucid area represent
megaspheres, that is yolk-masses cut off from the floor of the
subgerminal cavity and lying in the latter (cf. Fig. 28 M). The
invaginated entoderm is represented by the crossed area E;
the lip of the Vjlastopore, where ectoderm and entoderm are
continuous, by the region R.

Fig. 3L — A diagrammatic reconstruction of the blastoderm repre-
sented in Fig. 30. (After Patterson.)

R., Mass of cells left after closure of blastopore. S.G., Anterior
portion of subgerminal cavity not yet crossed by the entoderm. Other
abbreviations as in Fig. 29.

The last three or four hours prior to laying witness the closure
of the blastopore. A comparison of Figs. 27 and 29 will show
that the blastopore has become considerably narrower in the
later stage. It will be observed that the posterior ends of the
germ-wall are approaching. Finally they come into contact, and
the blastopore is closed. During this process the lip of the
blastopore is not cut off externally, but on the contrary comes

60 THE DEVELOPMENT OF THE CHICK

to lie within the germ-wall at the posterior margin of the pellucid

area.

This is illustrated by Figs. 30 and 31, representing a longi-
tudinal section and a reconstruction of a blastoderm three hours
before laying. Considering the reconstruction first, it will be
noted that the lip of the blastopore, R, now lies within the blasto-
derm at the posterior margin of the pellucid area. The greater
portion of the pellucid area is now two-layered owing to the
continued expansion of the entoderm E, which has met and
united with the germ-wall at the sides. The section (Fig. 30)
passes longitudinally through the center of the blastoderm. The
mass of cells at D represents the original lip of the blastopore.
It is continuous with the germ-wall behind and with the ento-
derm in front. The latter is not a continuous layer (Fig. 30 A),
and the cells are not coherent. It is probable that the extension
of the entoderm is due largely to independent migration of the
cells. Subsequently the entoderm cells unite to form a coherent
layer of flattened cells. (See Chap. IV.)

In some cases the closure of the blastopore takes place in
such a way as to produce' a marginal notch, which is referred
to again in connection with the primitive streak (Chap. IV).

CHAPTER III

OUTLINE OF DEVELOPMENT, ORIENTATION, CHRO-
NOLOGY

The preceding chapters have traced the development up to
the time of laying. The formation of the germ-layers has begun;
and the stage of development is fairly definite, though not abso-
lutely constant. When the egg cools, after laying, the develop-
ment ceases, but is renewed when the temperature is raised to
the required degree by incubation.

On the surface of the volk is a whitish disc about 4 mm. in
diameter, known as the blastoderm. Edwards gives the average
diameter of the unincubated blastoderm (59 eggs) as 4.41 mm.,
of the area pellucida (50 eggs) as 2.51 mm. The central part
of the blastoderm is more transparent and is hence known as
the area pellucida; beneath it is the subgerminal cavity. The
less transparent periphery is known as the area opaca. In the
course of development the embryo, and the embryonic mem-
branes which serve for the protection, respiration, and nutrition
of the embryo, arise from the blastoderm.

The embryo proper arises within the area pellucida, which
becomes pear-shaped as the embryo forms; the remainder of the
blastoderm beyond the embryo is extra-embryonic. From it
arise the embryonic membranes known as the amnion, chorion,
and yolk-sac. The allantois (Fig. 33 B) arises as an outgrowth
from the hind-gut of the embryo, and spreads within the extra-
embryonic body-cavity; it thus becomes an extra-embryonic
membrane secondarily. The growth of the embryo and of the
extra-embryonic blastoderm are distinct, though interdependent,
processes going on at the same time.

During the first four days of development the blastoderm
spreads very rapidly (Figs. 32 and 33). 'Thus on the fourth day
(Fig. 33 A) the greater portion of the yolk is already covered.
Thereafter the overgrowth of the yolk proceeds much more slowly
(cf. Fig. 33 B). In the opaque area there arise, as concentric zones,
the area vasculosa distinguished by its blood-vessels and the area

61

62

THE DEVELOPxAIEXT OF THE CHICK

vitellina, which may be divided into inner and outer zones
(Figs. 32 and 33). The development of the embryo during the
same period is indicated in the same figures.

Fig. 32. — A. Hen's egg at about the twenty-sixth hour of incubation, to
show the zones of the blastoderm and the orientation of the embryo with
reference to the axis of the shell. (After Duval.)
B. Yolk of hen's egg incubated about 50 hours to show the extent of
overgrowth of the blastoderm. (After Duval.)

A. C, Air chamber, a. p., Area pellucida. a. v., Area vasculosa. a. v. e.,
Area vitellina externa, a. v. i., Area vitellina interna. Y., Uncovered
portion of yolk.

The blastoderm early becomes divided in two layers as far
as the margin of the vascular area. The outer layer, known
as the somatopleure, is continuous with the body-wall, which is
open ventrally in the young embryo. The inner one, known as
the splanchnopleure, is continuous with the wall of the intestine
which is likewise open ventrally. The space between these two
membranes, the extra-embryonic body-cavity, is continuous
with the body-cavity of the embryo. Ultimately, the splitting
of the blastoderm is carried around the entire yolk, so that
the latter is enclosed in a separate sac of the splanchnopleure,
the yolk-sac, which is connected by a stalk, the yolk-stalk, to the
intestine of the embryo. This stalk runs through an opening
in the ventral body-wall, the umbilicus, where the amnion, which
has developed from the extra-embryonic somatopleure, joins the
body-wall (Fig. 33 B).

About the nineteenth day of incubation the yolk-sac is drawn

OUTLINE OF DEVELOPMENT, CHRONOLOGY

63

into the body-cavity through the umbiUcus, which thereupon
closes. The young chick usually hatches on the twenty-first day.
Orientation. It is an interesting and important fact that
the embryo appears in a definite relation to the line drawn through
the axis of the entire egg, or to the line joining the bases of the
two chalazse, which is usually the same thing. If the egg be
placed as in Fig. 32 A, with the blunt end to the left, the head
of the embryo will be found directed away from the observer
when the blastoderm is above; the left side of the embryo is
therefore towards the broad end, and the right side towards the
narrow end of the egg. According to Duval this orientation is

Fig. 33. — A. Yolk of hen's egg incubated 84 hours. (After Duval.)
B. Embryo and membranes of the hen's egg on the seventh day of incu-
bation. (After Duval.)

AL, AUantois. Am., Amnion, a. v., (in B) Area vitellina. E., Embryo.
S. t., Sinus terminalis. Other Abbreviations as in Fig. 32.

found in about 98.5% of eggs: of 166 eggs observed, in which
the embryo was formed, Duval found 124 oriented exactly in
this manner, 39 in which the axis of the embryo was slightly
oblique, 2 in which the head was towards the broad end, and 1
in which the usual position was completely inverted. In the
pigeon's egg the orientation of the embryo is equally definite, but
slightly different. The axis of the embryo cuts the axis of the
entire egg at an angle of about 45°, the head of the embryo being

64 THE DEVELOPMENT OF THE CHICK

directed away from the observer to the right, when the broad
end of the egg is to the observer's left as in Fig. 32 A.

The definiteness of orientation of the embryo with reference
to the axis of the egg enables one to distinguish anterior and
posterior ends of the blastoderm before there is any trace of an
embryo; and while there is no possibility of orientation by
examination of the blastoderm itself, or when such orientation is
otherwise extremely difficult. By the method of orienting the
blastoderm w^ith reference to the axis of the shell, observers have
been able to discover important features of the early development
which would otherwise, no doubt, have escaped observation
The relation is of interest in other respects discussed in their
appropriate places. (See p. 15.)

Chronology (Classification of Stages). The development of
an animal is an absolutely continuous process, but for purposes
of description it is necessary to fix certain stages for comparison
with those that precede and those that follow. Each stage has
a certain position in the continuous process, and the correct ar-
rangement of stages is therefore a sine qua non for their correct
interpretation. This may seem a very simple matter seeing that
development is in general from the more simple to the more
complex. And it would be so if it were not for the fact that
embryonic stages, like the adult individuals of a species, vary
more or less, so that no one embryo is ever exactly like another.
These embryonic variations involve (1) the rate of development
of the whole embryo, so that at a given time in the process no
two embryos are in exactly the same stage; (2) the relative rates
of development of different organs; (3) the size of the embryo,
for embryos of the same stage of development may vary some-
what in size.

Although the total period of incubation is fairly constant in
the hen's egg, about twenty-one days, yet there is great variation
in the grade of development of embryos of the same age, especially
during the first week. This is due to two main factors: first,
variation in the latent period, that is the time necessar}^ to start
the development of the cooled blastoderm after the egg is put
into the incubator, and second, to variation in the temperature
of incubation. Individual eggs may vary in rate of develop-
ment when these two factors are constant, but this difference is
relatively slight. Other things being equal, the latent period

OUTLINE OF DEVELOPMEXT, CHROXOLOGY 65

varies with the freshness of the egg; it is relatively short in eggs
that are newly laid, and long in eggs that have remained qui-
escent some time after laying. It is obvious that the latent
period will form a more considerable portion of the entire time
of incubation in early than in late stages. Hence the difficulty
of classifying embryos, particularly in the first four or five
days of incubation, by period of incubation. Eggs procured from
dealers usually show such great variations in degree of develop-
ment, at the same time of incubation, that it is quite impossible
to grade them with any high degree of accuracy by time of incu-
bation. It is statf'd also that the rate of development varies
considerably at different seasons, other factors being constant.
But this has not been found to be a serious matter in my own
experience.

Variations in temperature, either above or below the normal,
also seriously affect the rate of development, and produce abnor-
malities when extreme. If the temperature be too low, the rate
is slower than normal; if too high, the rate increases up to a
certain point, beyond which the egg is killed.

The physiological zero, that is the temperature below which
the blastoderm undergoes no development whatever, has been
estimated differently by different authors. Some place it at
about 28° C, others at about 25°; Edwards places it as low as
20-21° C. At the last temperature, apparently, a small percent-
age of eggs will develop in the course of several days to an early
stage of the primitive streak, but most eggs show no perceptible
development. In very warm weather, therefore, the atmos-
pheric temperature m.ay be sufficient to start eggs. The follow-
ing table is given by Davenport based on Fere's work:

Temperature .34° 35° 36° 37° 38° 39° 40° 41°

Index of Development 0.65 0.80 0.72 1.00 1.06 1.25 1.51

The index of development represents the proportion that the
average development at a given temperature in a given time
bears to the normal development {i.e., development at the normal
temperature for the same time). There is an increase in the rate
up to 41°; a maximum temperature, which cannot be much
above 41°, causes the condition of heat-rigor and death.

There would seem to be no better way to determine the normal
temperature for incubation than by measuring the temperature

66 THE DEVELOPMENT OF THE CHICK

of eggs incubated by the hen throughout the entire period of
incubation. This has been done very carefully by Eyclesh3mier,
who finds the internal temperature of such eggs to be as follows:

Day of incubation

1

2

3

4

5

Temperature of hen

102.2

103.0

103.5

104.0

103.8

Temperature of egg

98.0

100.2

100.5

100.5

100.4

Day of incubation

6

7

8

9

10

Temperature of hen

105.0

104.6

104.5

105.0

105.0

Temperature of egg

101.0

101.8

102.5

101.6

102.0

Day of incubation

11

12

13

14

15

Temperature of hen

104.8

105.2

104.5

105.0

105.2

Temperature of egg

101.8

102.2

102.0

102.5

102.0

Day of incubation

16

17

18

19

20

Temperature of hen

105.0

104.6

104.8

104.5

104.5

Temperature of egg 103.0 102.4 103.0 103.0 103.0

The temperature of the hen is seen to be somewhat higher
than that of the eggs. In an artificial incubator where 85 % of
the fertile eggs hatched on the twentieth and twenty-first da3^s,
the temperatures were as follows:

Day of incubation
Temperature of incubator
Temperature of egg

Day of incubation
Temperature of incubator
Temperature of egg

Day of incubation
Temperature of incubator
Temperature of egg

Day of incubation
Temperature of incubator
Temperature of egg

It would be possible then to establish a normal rate of develop-
ment, by using perfectly fresh eggs incubated at a normal tem-
perature. In practice I have found that the times given in Duval's
atlas are approximately normal, and these are, therefore, adopted
so far as given. But even under the best conditions the varia-
tions are sufficient to prevent close grading of stages by time of
incubation in the first three days. This may be due to differences
in the grade of development at the time of laying, owing to varia-

1

2

3

4

5

102.0

102.0

103.0

102.0

102.5

99.5

100.0

101.0

100.5

100.5

6

7

8

9

10

103.0

102. 5

102.0

103.0

103.5

101.0

100.0

100.0

101.0

101.5

11

12

13

14

15

103.0

103.5

104.0

103.5

104.0

101.5

101.8

102.0

102.5

103.0

16

17

18

19

20

104.5

104.0

103.5

104.0

104.5

103.0

103.0

102.5

102.5

103.5

OUTLINE OF DEVELOPMENT, CHRONOLOGY 67

tioRS in the time of development in the oviduct and uterus, or
to slow development before incubation in warm weather, or to
individual variation. It becomes necessary, therefore, to find
some other system. The method followed by a considerable
number of investigators, namely to classify by the number of
somites, has been found to be best between about the twentieth
and ninetv-sixth hours of incubation. In the table which follows,
therefore, this method of classification is used. For the sake
of brevity throughout the book a stage reckoned by the number
of somites will be w^ritten 1 s, 2 s, 3 s, etc. It is true that the rela-
tive rate of the development of organs varies slightly. Never-
theless, classification by number of somites is unquestionably
the most exact method up to the end of the fourth day at least.
Beyond this stage the method is difficult to apply, and after
about the sixth day the number of somites becomes constant.
After the fourth day the time of incubation is usually a suffi-
ciently exact criterion for most purposes: the latent period has
become a relatively inconsiderable fraction of the whole time
of incubation, and the embryos that survive, assuming fresh eggs
and normal temperature of incubation, are in about the same
stage of development.

Classification of embryos by length is a favorite method
particularly in Germany, and it offers many advantages in the
case of some animals; under many conditions it is the only avail-
able method. But it offers considerable difficulties, the most seri-
ous of which come from the varying degrees of curvature of the
embryo. In early stages of the chick, for instance, up to about
12 s, the total length of the embryonic axis may be measured,
for the embryo is approximately straight. The cranial flexure
then begins to appear, and slowly increases to a right angle;
during this period there may be an actual reduction in length
of the embryo (cf. table, 14-16 s). Conditions are also compli-
cated by the fact that the head of the embryo is turning on its
left side at the same time. The cervical flexure then appears
and causes a second reduction of the total length (cf. table 29-
32 s). Later still the curvature of the trunk and particularly
of the tail develops in somewhat varying degrees and makes
bad matters worse. After these flexures are formed, let us say
at about eighty hours in the chick, it is customary to take the
so-called neck-tail measurement, that is, from the cervical flexure

68 THE DEVELOPMENT OF THE CHICK

to the apex of the tail flexure. But even then it is questionable
if this measurement is as accurate a means of classification as
the age of normally incubated embryos; particularly as the cer-
vical flexure is secondarily eliminated by raising of the head.
It is probable that the measurement from the tip of the head to
the apex of the cranial flexure (head-length) would be best for
classification of chick-embryos by measurement. This dimen-
sion may be readily taken, after the cranial flexure begins,
throughout the entire period of incubation. However, it has
been relatively little used up to the present time.

The following tables give the chronology of development up
to the end of the fourth day, the period usually covered in labo-
ratory courses. For the later chronology the student is referred
to Keibel and Abraham's Normaltafeln zur Entwickelungsge-
schichte des Huhnes (Gallus domesticus), Jena, Gustav Fischer,
1900. In the various chapters of Part II, the later chronology
of the various organs is given here and there throughout the text.
It is believed that these references will be sufficient on the Avhole
to enable the student to determine what embryos to select for
the desired stage of most organs. The tables have been made
practically continuous from 1 s up to 41s, because these cover
the period of development in which the primordia of most organs
are formed. They have been constructed mostly from entire
mounts. The corresponding tables in Keibel and Abraham's
work are noted by number in the right-hand column.

Chronological Tables of the Development of the Chick

I. Before Laying:

1. Maturation and fertilization; found in the oviduct above the

isthmus.

2. Early cleavage up to about the thirty-two celled stage found in

the isthmus of the oviduct during the formation of the shell-
membrane (Patterson) .

3. Later cleavage, formation of periblast and entoderm, etc., found

in the uterus up to time of laying.
Data for the pigeon given in Chapter II; see legends to figures.

II. Incubation to Formation of the First Somite:

The period may be divided in three parts: (1) before the appearance
of the primitive streak; (2) primitive streak formed but no head process;
(3) after the appearance of the head-process. These stages may be sub-
divided by time or by length of the primitive streak.

m. FROM t TO 41 SOUITES

Dcdf-

uiion

„™....,

A«e

FIOUIB

Primiii™
SmalL

Nmroui Syiitm

E^

Ear

Note

Epiphyiii

Photyiu and Derinllnt

Urinogenilal
Syiiem

^■(KuLu Syilrm

».,„,...

Amnion

Allinlou

Olher Stiucltua

Tablea*

CoU.

iS

,Anuo.lK.No,<)

,,,mm.

lorn

Me>d fold diuinctly

jandi

'

jS

,™™.

"(Du«IJ

„.,mm.

JTHulLinr fold, mcclinic
in ncioD ul mld-briin

Fnrc-iuiaboulo.iy mm.
lung

He^.fold dxpcr

6.nd,

'»

»s

.,,<om.

■■,a

I^mm.

MRlulbrirloUiuloiS
Mcdulbry fold) cloud

Fatr-tvi aboui .16 mm.
long

Fore-gut aboul 0.4 mm.

aiood bUndi Ubldd cm.
U^o^a^opp^te ,».

DlwdUlanda noil formed

II and 11

long

up to fore gut

i^BUB.

<M).mn..

il.f. «iirel,own

mj-jul a

Same

t.s

jjinni.

•i./sr-

D Jl mm.

M(du1kiTrukl.tu.cmrI

"Sd-'^S-

Fon-tul dMbl aboul

Lateral honu ol bind
germ «teod lo le«l <A

"

«n

ilxKil J mm.

^UT"

tip uf head

Sam-"'

,s

.,,<™.

9-j.mni.

Mfdullary folda t1««l

voide

Pure irut (luKd aboul

b.il>a of bean begun

"

'"

es

LIS mm.

' lDu.Bl

o*j mm.

Mtdullary r<ild> clOKd

[>rimaTT
oplic

'Dre-uul doKd about

Fuilon of Ul. haira of
bean incomplete

Bel-een .
ind 18

SJfi

Mflullary lolds ilowd

Primarr

FDre.4tul [la»d about

Septum between halyo

tej

«s

oa,i mm.

ol heart rupturing

,.,

lit nun.

houn
iDunI)

J boun

^mlndlcatiaBolcnnlil
OdUrt

litht cnniil Oeiun

o.i» mm.

da dculy iadicainl

|.liD[ of dOSDg

Opi. to. nol
conjuiclfd
.1) ba»

Slighi ton-

> "b^ ol
opl in

Foregul do«d aboul

Henri bent lUghlly lo
right

He.in bent lo right

and™

-

14 s

*»»■

ighi maitl IttiuK

Aboul oj6

Iic»ll» Jospdr^N'nuo-

Constrlttian
al biMol

Shjlloff pli

Fir« rtKeroJ cicfl In.
metU enlodetm

Heart beat lo right

U

'"

.TratllT°'m^ """"

bX'nd &
Iran

>(S

counuav™

ad b((ln> to lure on

Atau. 0,

Primaiy va.

D«p, bul

urc-gul doMd 1.4 mm.

Uott allgblly 5-ibapcd

leadfold coven nlremc

jj

iJI

Ihclcllilde

«5l'USt

inde opcu

tip ol head

iDdicJled

Hibcd

pit

16 s

mn, M „t„un.

a boun

Jk. .jS

LAaisS

UktisS

UluiiS

Fort-gut clc»] 1.1 mm.

Like IS S

lead-fold co.m (niirr

•J

0>4

lakcn of Ociura

(Du«l)

focebnmrwuo

.,s

.„...

?^^K-?J33'""

LikruS, RoolofhJnd
linlD becoming Ihln

"IS

UkcisS

Second vistenil deli

-■h.ipe of heart (lightly

-Jead-fold coven lo olic
region tunujuaily long)

180 10 go

,6

■ss

9 mm. pealBI Imgih

Dlin hod mure Ikui
hill luiMd DO Wl side

^-^r^ts

"QiLUriction appon bc-
l.c^n di- and leleo-

■^sa

Like II S

Lenmb ol loregul 1 1
mm. Two iiKenJ (ut-
nin. .liU closed

-ihape of bean my
Indlcuied

lead fold conn anlerior

put of hind brain

Mandibular archa begto
loprojta

"

5.P

,r,.s

-S mm. urialcU length

4 houn
IUuvbI)

udrullyluniBllaltli.
Cnnlul and iin-icol
ncnira rouodri ob-

'"Sa

Sllfhl nar-

= s

deep pit

Na indioillDa ol hyp-
opbi-ai

.luough

\unculo i-enlricubir
Ditunnndicaiedbyoon.

Like 18 S

'*

OS

..s

1„7.ES.»

.elLlumrdloBlhlDmllt
Cr.ni.1 (tuure-riibi
anilt.itf.neiujmr)-

Only In lail

^j^!J!^bJr

"sill'

olpi.

Hypophi-iii barely InHi-

ihrouKh

jd Yi*. pouch Kcn

I'tnliiculai loop noir
vcnlnl ID »ur.-«n.

™"""""

Sudden venlrally lumed
neiure ol trunk .boui
8th wmiie (due 10

»*-3J

»»

...

""-

.ifllurncdloi-flinmlle.
Cr.oljinau«al"UI*
r. anilc. Mr., (tuui.

vm .fi»hi

S'U

«IM«»S

»^™j,
sr

Ukt 11 S

like 11 S

Lenglh ol lore-gut t-J
mm.olhcmiKJikeiiS

Uke >i S

tleadlold CTOHO id ni
ani pouch nod id «

*'a

J6»

fjS

J, T mm, gntUM fcnph

jrviol nciun >nitc nl

D uil bud

Uk. a.S

Moulholpil

vi^naliaa In ftoDI Dl

Lenglh ol lore-gut 1 ij

«S'riy"pertaraie4"m

Like 31 S,

■Jead-fnld covem lo lolh

Tail. fold barely indlcaled

iS-.i»

J6j

iraoj-

oral plate

upper angle

■iiuuled

<i.i mm, (TtaloJ kniib

.crriol nenire lite ijS.

n tail bud

Iduiniai

Rebii«ly

nalioninNo.jSi(liSl

"^^^pllTfl^,"^^

Lenilh nl lute-gul about

Apei of i-Hilriclc vcnlnl

^"t!^"™""**

NolaU-fold

*'

M-»» S

iitlan> n[ tnin mnrc

U^n™. n«hl "^k

iliUopcn

oponingol
SUml"'^

lion in (funl ol oral
pbU

Two complete aoftlc
arches

.. s

6*«™.p«i«.i«.rh

a houn

di^.l',"™cl ""

■> tall bud

llkc«-.jS

louth. ol

yke.4-.1S

\o epiphnii

Same ai 14-aJ S

»mc a. 14-1; S

Sam.aa«-.^S. ^^^^
archB-^fl^d?*"""

rtndlold cover. 10 171b

Tall-fold indicaled

-

049

,™n.,g™,«nr«„h

9 houn

epiuilk fluura •llihlly
ICB Ihan ixHCcUni

nun bud

toulh ol

No cpipbtiii

"E?^ '-'"■!

d ri«*ral pouch ndl
deielo[cd. Thyroid
and lung divauoili

Two complelE aortic
arehu- Third nearly

lead-fold coven to >otl>
lomite

Tail bud projecu behind
Hlnd-gul lorma n bay

**

Ji8

"So"-

Hcll muked

H^^o-

icf-

a , mm palru Imilh

"crvlcal Ituurt man

Mouih ol

OHe KBcIe

rUckenlns

Epiph,Ti. , iMTTU >liRht

Same as ,7 S

'.aztir.sii--

rhicT complete aortic

FalJ-fold formed . con-

Form. <maU side o|in

4j

4'

'p^cillSf,

•Imuil

0( MIO-

dem. No

uilhn

11°^ fX'" "u^

pouch

diaed

tn"^""

»mite"""

-., mm. nW" """

UVe i« S

Like iB S

Like » S

UkcittS

No cplpb^Ul

Same M ay

JkeiH. Oml membrane

Thn» complele aortic
arcbci

Bud3olhlnd
limba In-
dialed by
thickening

Head-fold coven 10 »lh
«.miie. Small lailfold

UkcaSS

pleure

...

6*ni(i).«tol«llo«0h

Dcrcu ..1 nctvtal lid

UK nulin onRlc d
hind Inln unci iruok

CouiriHInii of Islhtnui
bMQinint proiwuncnl

byit ol

oprajni

Oik mide^

UkciSS

SmiU epiphyu.

dljtilly

Founb rim. pouch iodi.
caled. Cloaiog mem.

Ma """ "■" "^

Three camplete avttic
plele

Dudi ol fore
and hind

lirea'Sd'l-^

Hcod-fold coven lo iSIb
lomlie. Small lall-lold

Alianti^ eiltnding into

jiS

wmm.nttkun

Ccr.l(.L ntiurt a full
rlHhi >i>i|lc

MannnMrtcUnDottub.

RdlnilUtet

"'SJS"-

X,';.""

Small cpipbiid.

iRd« ai di«n1 tnd.

]/s"

Oval opening inlo»ti.nl'
otic ^-ily enendmii

Sameaaja

46

loH

oI oUic-

Sliiiht deprwlon «I la.

from iflih lo lu»t be-

^"*

10., 1-.

lundlbulutwiun

hind nU totnile

»»s

I.Tmm.Hd>,uU

fleiure

'=iia'--^'"

Sime u }i

""• " '■

''"t'.iors

ollaciory
IhanjiS)

Small eplpbiilt

Same a> }i

Same asp

Sime ai yi

Limb bud.
i-etun^"

Amniotic umbilicu. •!■
mwi cDiicely do«d

Me»b1a>lolallanu^be.
lint U> olend Into
Cody cavity

Curving ot 1*11 *nd In-
CRUC Of cervical Ilea-

)l«

us

aurora, BRk'Ull

^■""'

Shallow [it

Stmeujr

Sameu]>

Simeaijs

Limb budi

io«idtbolK>"i™H'

Kidt cavlly

Vo nicnni of tall

'"

MS

tj mm. eidi-Ull. t^
mm. (orrmld Inln

doofl? bdialcd

"rjs-r

"ua

like»S

utS^Seprniinn deuly

"i-.r^'sii'-c:

SamcMjaS

Uke ). S

Curving ol lall begun

4S&4&>

'"

limb budl

nid dlvenlculum doi.
Ing

umiics

t» mm Htkiill. >^
mm. l(R-m)d Inln

ckarl) todioiB)

"15"°'

Lalenl

boundUT

VeiT ilijhl dittal W

aunjoiringjojuplure

Oral membrane lunbet

•rluculum "Xed?
Tounh i-Uc, pDUcb

aiiiS

Amnion completely
cloaed

.*elllaa

Curving ol tall

»a>->i

16 S

' (!« "nnin'*"""'

AWH^n

tm«)j todiuiol

Par.<hac<d

Lalenl

Enginatiun lUchtlr eo-

Ruplure ol oral mnn.
P«i.tt ipre-oral (ul)

Fourth pouch dearly Ken

"acr

,nlar»cmeoi Into body
cavity

"

«s

mm. Ivc-mid tnlo '

cl-tlrlndtaSST'"'

sr

ni U hem
Uphoinl

Eniinilion b turon
lucknM.diU»lly and
jjyb^ .marked ..d»

Sh.Klenin« ol IniiLfina.

lioo ol hvp. oMfii 10
rtifjptn'""' «^ nnil

Oral membrane gone
Fourth i-iKcnl puuch

Fouitb aortic arch
termed

Cloaed

UUal eolargemeol nol
l^iun

Tip of tall begin. 1" U
dlrecicd fun>a/da

»s

lA mm. »«k-ull, >«
mm. lonmld Inln

•in*** lodkaiBj

Endol. dun
iphniml

like 31

Hemijphcrlcal englna
tion

marked

ykejft

Cloaad

gun

Jl*

41 S

M mm. n«kmll, ,,,

Ahoal «6

Same a> 34: Unl hill cf

ESTtS

Deep

Inlundibulam aroadf

Fourth Tbonl poudi

Ailiolbudi

■ holt ilLinlail flaik
thaped

01

mm, Ior»nM bnin

bodr lamin* 00 al'lt

f«m>dc&

podTct.
tbipcd in

m.arted

fully tBimEil

equal lo

■llDUl i

breidih

68 T

to the apex ol
if this measui
the age of no]
vical flexure ;
It is probable
the apex of tl
classification (
sion may be
throughout th
been relativel}
The follow
to the end of
ratory courses,
to Keibel anc
schichte des I
1900. In the
of the various
It is believed t
to enable the
the desired sU
practically cor
the period of d
are formed. '
mounts. The
work are no tec

Chronoloc

I. Before Layii

1. Maturatic

isthmu;

2. Early cle

the istb
membn

3. Later cle^

in the
Data for

II. Incubation 1
The period n

of the primitive
(3) after the app
divided by time

CHAPTER IV

FROM LAYING TO THE FORMATION OF THE FIRST

SOMITE

I. Structure of the Uxixcubated Blastoderm

There is more or less variation in the stage of development
of iminciibated blastoderms; in exceptional cases these variations
may be extreme. However, the usual condition may be described
very briefly as follows (see Fig. 34): Beneath the pellucid area
is the subgerminal cavity bounded marginally by the germ-wall.
The posterior part only of the pellucid area is two-layered. The
lower layer or gut-entoderm terminates posteriorly at the germ-
wall, with which, however, it is not united. It is composed of
spindle-shaped cells which form a coherent layer, perforated by
numerous small openings that appear as breaks in the layer
in section. In front of the gut-entoderm a few scattered cells
appear in the subgerminal cavity. The gut entoderm does not
reach the germ-wall either laterally or anteriorly, but in the
course of a few hours' incubation it spreads so as to unite with
the germ-wall around the entire margin of the pellucid area.

The germ-wall is slightly thicker at the posterior than at the
anterior end, that is to say, that the nuclei extend deeper into
the yolk (Fig. 34). There is a broad zone of junction and beyond
this the margin of the blastoderm overlaps the yolk a short dis-
tance. The germ-wall has not yet become organized as a layer
separate from the yolk.

The ectoderm is thicker in the region of the area pellucida
than in the area opaca; and slightly thicker in the center than
at the margin of the area pellucida.

XL The Primitive Streak

Total Views. The primitive streak is the first sign of forma-
tion of the embryo proper; it appears early on the first day of
incubation as an elongated slightly opaque band occupying

69

70

THE DEVELOPMENT OF THE CHICK

:•.■■' (fl

Q

m<-:--'

';••■•*.*"

;!■•'. •••'>*

V.

,'-■*■».' '^ 6-

*i

If-.' •..-►

N

!?•■' ;'-iv

■'

i:i^^^l''

<^

M:,-^

1 #.:;■:.

^ ;^:;:

ii^

I

^k

-^t^:'^

s r-

, '^

Qi

b£

o

o

-^

-f^

o3

M

1

*'"'

73

C

0)

Oi

O

^

^

^

0)

-^J

•

o

o

^— ^

^^H

a;

r-t

^

s

H

^f

^^

- J^

5

^ 3

*M

• ^^

o

• ^^

'^

^

_>

^=^

-*^

G o

-_^_,

"3

Pl^ 0)

o

Lh

r1

0~^

o

^

o

rH

-S

^^

tn -

s^

q;

ii^

o

-3

^
-^j

^

o .

,~

• r— (

H

03

-1-3
(4-1

o 03

CD

H3.

-O

f— ♦

F^

-^J

OJ

o

>.>

• ^

-M

-t^ +-J

^

11

r-4

S

o s

-^f^

^

^

o3

^-t— 1

_o

S "^

o

'i^

^ '7^

a;

G (^

r^

-fj

Lh

_o

(^

¥ c

'-^J

s

^^

a;

0)

3

cc

■^

"^^ c

r o

bX}'C

03

oT

• s

;-!

JO <D

'bJD

O

•— *

O

03 -

M

<^t-(

o

o3

o

^f^

c

_o

-5

o
« p— (

2

0)

r Kn

'^

^ E^

CO

o

C OJ

,

S<1 >

o

3

o

HH

(4-1

^

o

FROM LAYING TO FORMATION OF FIRST SOMITE 71

the posterior half or two fifths of the circular pellucid area (Fig.
35 B). It is relatively narrow in front and widens posteriorly,
where it is at the same time less dense. Its anterior end usually
does not quite reach the center of the pellucid area. It rapidly
increases in length; the anterior end appears to be practically a
fixed point, and growth takes place posteriorly probably not by
addition, but between the two ends. The posterior half of the
pellucid area elongates simultaneously, keeping pace with the

Fig. 35. — Surface views of two stages of the blastoderm of the egg of
the sparrow. (After Schauinsland.)

A. Before the appearance of the primitive streak.

B. The first appearance of the primitive streak.

a. o., Area opaca. a. p., Area pellucida. Ent. Th., Thickening of en-
toderm, pr. str., Primitive streak.

primitive streak which lies entirely within it in the chick and
most other birds. Thus the area pellucida becomes oval, then
pear-shaped, and the primitive streak bisects the greater part of
its length (Figs. 35, 36, 44, etc.).

According to Koller the primitive streak takes its origin from a
crescentic area at the posterior margin of the pellucid area, which he
terms the sickle. The primitive streak appears as a process extending
forward from the center of the sickle, and, as it grows forward, the
lateral horns of the sickle are gradually taken into its posterior end.
Koller's observations and interpretations have not, however, been con-
firmed by subsequent investigators and they would appear to rest on
rather exceptional and inessential conditions.

72

THE DEVELOPMENT OF THE CHICK

Fig. 36. — A. Intermediate stage of the formation
of the primitive streak of the sparrow. (After
Schauinsland.)

B. Fully formed primitive streak of the spar-
row. (After Schauinsland.)

a. o., Area opaea. a. p., Area pellucida. Ent.
Th., Thickening of entoderm. Mes., Mesoderm,
pr. f., Primitive fold. pr. gr., Primitive groove.
pr. p., Primitive pit. pr. str., Primitive streak,
s. gr., Sickle groove.

At first the surface of the primitive streak is even, but, as
it elongates, a groove appears down its center. This groove is
known as the primitive groove; it is bounded by the primitive
folds and terminates abruptly in front in a pit, the primitive
pit. which corresponds to the neurenteric canal of other verte-

FROM LAYING TO FORMATION OF FIRST SOMITE 73

brates (Figs. 35, 36, 44, etc.). The primitive groove does not
involve the extreme anterior end of the primitive streak, which
forms a Uttle knot in front of it, the primitive knot {" Hen-
sen's knot"). The posterior end of the primitive streak termi-
nates in an expansion which is not very obvious in surface view,
and hence is not usually described; it may be called the primitive
plate (Figs. 36, 44 A, 44 B, etc). In some cases the primitive
streak and groove are bifurcated at the posterior end (Fig. 44 B).
The primitive streak is the first clear indication of the axis of the
embryo.

The neurenteric canal is a canal that connects the posterior end of
the central canal of the neural tube with the intestine. It arises from
the anterior end of the primitive mouth, and is typically developed in
Selachia, Amphibia, reptiles, some birds {e.g., duck, goose. Sterna, etc.).
It begins in the primitive pit and extends forward into the head-process
(p. 80). Subsequently the primitive pit becomes surrounded by the
medullary folds, and thus opens into the neural canal. An opening is
later formed through the entoderm so that the definitive canal connects
neural tube and hind-gut. In the chick the neurenteric canal is never
typically developed. Usually it is represented only by the primitive pit.
In exceptional cases I have found traces of it in the head-process.

The so-called head-process appears in front of the primitive
knot (Figs. 36 B and 44 B). In surface view it appears not unlike
the primitive streak itself, but is fainter and less clearly defined.
It is continuous with the primitive streak at the primitive knot,
but its axis is usually a little out of line with the axis of the primi-
tive streak.

Figs. 35 and 36 exhibit four stages of the development of
the primitive streak of the sparrow (after Schauinsland). The
darker area in the anterior part of the area pellucida is caused
by a thicker region of the entoderm which in the course of time
becomes of uniform thickness with the remainder. It will be ob-
served that the primitive streak arises entirely within the area
pellucida (Fig. 35 B). In later stages its posterior end is bifurcated
(Figs. 36 A and B), and we have the appearance of a sickle some-
what similar to Roller's description for the chick. The primitive
groove begins near the anterior end of the primitive streak in an
especially deep pit just behind the primitive knot, and extends
back the entire length of the primitive streak into the horns of
the sickle. The head-process is barely indicated in Fig. 36 B.

74 THE DEVELOPMENT OF THE CHICK

The later history of the primitive streak is illustrated in Figs.
44, ol, 61, 65, etc.: the embryo arises in front of it around the
head-process as a center; the anterior end of the primitive streak
marks the hind end of the differentiated portion of the embryo.
As the embryo grows in length the primitive streak decreases (cf.
measurements in table), until finally, when the completion of the
embryo is indicated by the formation of the tail-fold, the primi-
tive streak disappears. The primitive knot and primitive pit
occupy its anterior end at all stages, and, as the embr3"o differen-
tiates from the anterior end of the primitive streak, the primitive
pit must be regarded as moving back along the line of the primi-
tive groove, always representing its anterior end.

Sections. The preceding sketch of the superficial appearance
of the primitive streak must now be followed by a careful exami-
nation of its structure and role in the development.

c

Fig. 37. — Three sections through the primitive streak of a sparrow at a
stage intermediate between Figs. 35 and 36. x 230. (After Schauinsland.)

A. In front of the primitive streak.

B. Through the anterior end of the primitive streak (primitive knot).

C. About through the center of the primitive streak.

All recent authors are agreed that the primitive streak owes
its origin to a linear thickening of the ectoderm, from Avhich cells
are proliferated between the ectoderm and the entoderm, forming
a third layer, the mesoderm. Figs. 37 A, B, C show three trans-
verse sections through a blastoderm of the sparrow slightly more
advanced than the stage shown in Fig. 35 B. The first section
is just in front of the primitive streak. The ectoderm is thick
in the center and thins gradually toward the margin of the area
pellucida, becoming decidedly thin in the region of the area opaca.
The thin entoderm of the area pellucida unites peripherally with
the thick yolk-sac entoderm of the area opaca. The second

FROM LAYING TO FORMATION OF FIRST SOMITE 75

section passes through the anterior end of the primitive streak;
the ectoderm is greatly thickened (primitive knot); the base-
ment membrane is interrupted below, and the lowermost cells
are becoming loose. The third section is through a more pos-
terior portion of the primitive streak. The proliferation from
the ectoderm is more extensive, the cells are looser and are begin-

Ent --^'-^^"' ""^^^

.¥es.

Fig. 38. — Transverse sections through a very short primitive streak of the
chick. Incubated 17^ hours; no head-process.

A. Through the anterior end of the primitive streak (primitive knot).
Mesodermal cells are being proliferated from the ectodermal thickening;
some are scattered between the two primary germ layers. The entoderm
shows no proliferation, though some mesoderm cells are adhering to it.

B. Fourteen sections posterior to A. (Entire length of the primitive
streak is 80 sections.) The mesoblast wings are forming; the primitive
groove and primitive folds are indicated. The entoderm is free from the
mesoderm.

Ect. Ectoderm. Ent., Entoderm. Mes., Mesoderm, pr. f., Primitive
fold, pr.gr. Primitive groove, pr. kn., Primitive knot.

ning to spread out laterally. The entoderm is a continuous
membrane without any connection with the primitive streak,
and there are no cells between ectoderm and entoderm save those
derived from the primitive streak.

Figs. 38 A and B show the structure of the primitive streak

76 THE DEVELOPMENT OF THE CHICK

of the chick at a more advanced stage, but before the formation
of the head-process. Sections in front of the primitive streak
show no cells between ectoderm and entoderm. In the region
of the primitive knot (A) the ectoderm is greatly thickened,
forming a projection above and below. Cells become detached
from the lower surface of the ectoderm, and are converted into
migratory cells between the two primary layers. Immediately
behind the primitive knot the primitive groove begins abruptly;
it is the seat of active proliferation from the lower layer of the
ectoderm, and the cells migrate out laterally forming wings of
cells, which do not, however, reach the area opaca (Fig. 38 B).
Conditions are very similar along the entire length of the primitive
streak at this time; but near the posterior end a few cells of the
mesoderm reach the area opaca and begin to insinuate themselves
between the ectoderm and the germ-wall. There is no evidence
at any place that any of the mesoderm cells are derived from the
entoderm. The axial thickening of the primitive groove comes in
contact with the entoderm and appears in places fused to it.

Figures 39 A-E represent five sections through the head-process
and primitive streak of a chick embryo at a time when the head-
process is still very short. The first section through the head-
process is described beyond. B is through the primitive knot;
the ingrowth of cells is more extensive than in the preceding
stage and it will be observed that they are now fused with the
entoderm, so that the latter no longer appears as a distinct layer.
C is through the primitive groove near its anterior end. D is a
little behind the center of the primitive groove, and E is through
the primitive plate. Behind the center of the primitive streak
the entoderm is again free (D). It will be observed that the
area of proliferation in the primitive plate is very wide.

YiG. 39. — Five sections through the head-process and primitive streak of a
chick embryo. The head-process is very short.

A. Through the head-process, now fused to the entoderm.

B. Through the primitive knot.

C. Through the anterior end of the primitive groove.

D. A little behind the center of the primitive streak.

E. Through the primitive plate.

The total number of sections through the head-process and primitive
streak of this series is 102. B. is 4 sections behind A. C. is 12 sections behind
A. D. is 59 sections behind A. E. is 87 sections behind A.

Ect., Ectoderm. Ent., Entoderm. G. W., Germ-wall. H. Pr., Head-
process, med. pi., Medullary plate. Mes. Mesoblast. pr. f. Primitive fold,
pr. gr., Primitive groove, pr. kn., Primitive knot. pr. pi., Primitive plate.

/nedcL

"=M

^-3

.^t^STx-^

-.,«®

■*i^iSS2^""

j^'J'^^St^^f'VA^^'

• • •

i.«r>'

'^Sij&Trr^r^

fi^^

^.--

>^

B

'nt.

■ ''?j'

VV^ /!5^f^

*-♦,

»5*

c^ ::■

D

- y°^fi/.

••»•■••■■■'■"'" ■ ^ ^

78 THE DEVELOPMENT OF THE CHICK

The mode of origin of the mesoderm of birds has been a very puzzling
question as is proved by the numerous views that have been in vogue
from time to time. One of the earhest views was that the mesoderm
arose by spHtting of the primary entoderm (Remak). This view sur-
vives in part even at the present time (mesoblast of the opaque area).
Balfour believed that the mesoblast in the region of the embryo "ori-
ginates as two lateral plates split off from the primitive hypoblast," and
that the primitive streak mesoblast is extra-embryonic, or at most enters
into the formation of mesoblast of the extreme hind end of the embryo
(allantois mesoblast in part). This view is found in the "Elements of
Embryology" of Foster and Balfour. A third view% now of historical
interest only, was that the mesoblast cells arose peripherally and mi-
grated between the two primary germ-layers (Peremeschko, Goette).
The latter author even attempted to derive the primitive streak from
an aggregation of such inwandering cells. The view that the primitive
streak arises as a thickening of the ectoderm and that it is the source
of all the mesoderm was first stated by Kolliker, and has been accepted
by Hertwdg, Rabl, and many others. It may, indeed, be regarded as
definitely established for the embryonic mesoblast. Others, however,
believe with His that the mesoblast of the opaque area arises by delam-
ination from the germ-wall; this question is discussed beyond. It should
also be noted that it is probable that the primitive embryonic mesoblast
is supplemented in certain regions at later stages by cells proliferated
from both entoderm and ectoderm, particularly in the region of the
head, (gee pp. 116, 117.)

In early stages of the primitive streak the mesoblast cells
are relatively sparse and bear every appearance of migrating
separately. But as the ingrowth progresses and the cells become
more numerous, the mesoderm becomes converted into coherent
plates. These are wedge-shaped, the central broad ends fused
wdth the primitive streak and the narrow margins extending
laterally (Figs. 40 A, B, C). They soon overlap the margin of
the opaque area and thus is produced a three-layered portion of

Fig. 40. — Three transverse sections of a late stage (corresponding to about
Fio-. 44 B), through the head-process and primitive streak of a chick embryo.

A. Near the hind end of the head-process.

B. Through the primitive pit.

C. A short distance behind the center of the primitive streak. The region
between the lines A-A and B-B is represented under a high magnification
in Fig. 41.

Bl. I., Blood island, coel. Mes., Coelomic mesoblast. Ect., Ectoderm.
Ent., Entoderm. G. W., Germ-wall. med. pi., Medullary plate. Mes., Meso-
derm. N'ch., Notoehord. pr. f., Primitive fold. pr. gr., Primitive groove,
pr. p.. Primitive pit.

FROM LAYIXG TO FORMATION OF FIRST SOMITE

79

Si'.'''.

£sv.",

',?;<

tpJ??V a « .:

^

^

x'

pi .

■5?

m

ei

•3B"" J'

^

80

THE DEVELOPMENT OF THE CHICK

the latter which corresponds to the future vascular area. The
mesoblast grows out, not only from the sides of the head-process
and primitive streak, but also from the hind end of the latter,
that is from the primitive plate. The mesoblast thus extends into
the opaque area behind the embryo at a very early stage (Figs.
42 and 44).

The primitive groove must be regarded as an expression of
the forces of invagination of the mesoblast, and the primitive
folds as the lips of this invagination.

Mas

.0«*^:

•|

G.lV

Fig. 41. — The part of the section shown in Fig. 40 C, between A-A and
B-B more highly magnified.
Abbreviations same as Fig. 40.

The Head-process. Two stages of the head-process are shown
in tranverse section a short distance in front of the primitive
knot in Figs. 39 A and 40 A. It consists of a thicker central
mass of cells with lateral wings; the central part, or primordium
of the notochord, is continuous posteriorly with the axis of the
primitive streak. These two portions of the mesoblast are often
termed gastral and prostomial, connected with the head-process
and primitive streak respectively. The head-process becomes
inseparably fused with the entoderm in the middle line imme-
diately after its formation; and this fusion is continued back
along the axis of the primitive streak (Figs. 39 and 40). The
fusion is particularly intimate and persistent at the extreme
anterior end of the head-process; behind this point the notochord
and entoderm soon separate again in the course of development.
But the anierior end of the notochord remains attached to the

FROM LAYING TO FORMATIOX OF FIRST SOMITE 81

0^

O

!:£!

O

O

o
o

73

o
>

5:

>

o

—^ r-<

J!:-:*^

o

■ ;h

r fcX)

ffi o

bO

^

'^ tvi

^

^^ o

w >

r-"

• ^H

*— 1

-^

o

-♦.s

s'S

j:^ -^^

^^

2 '- eS

-*

-►^=*;-S

^

- . ^

•^

^^o

w^

r >

-tJ

*^ "^

fcJC

-3 5 s

o

M • «-H

-SdrT

• ~ 1— I

rH

s o

r*

~ M *-

«^

^, O —

^-^
O

-^S -

*-H

o ^ .•

^

. -»^ _. -H

^i ^ ^ .^

1— I _;i .>

82

THE DEVELOPMENT OF THE CHICK

entoderm for a considerable period after the formation of the head-
fold. A longitudinal section shows the head-process as an append-
age to the anterior end of the primitive streak, or the primitive
knot (Fig. 42).

m.n.

Fig. 43. — Diagrams to illustrate the theory of concrescence as applied to
the primitive streak of the bird. The central area bounded by the broken
line represents the pellucid area ; external to this is the area opaca, showing
as concentric zones the germ-wall (G. W.), the zone of junction (Z. J.),
and the margin of overgrowth (M. O.). m. n., Marginal notch. For de-
scription see text.

The most obvious interpretation of the head-process is as
an outgrowth from the primitive knot. But another, and more
probable interpretation in view of all the facts, is that the head-
process is a later stage of the anterior end of the primitive streak;

FROM LAYING TO FORMATION OF FIRST SOMITE 83

that a gradual separation of the ectoderm takes place in the
axis of the primitive streak beginning at the anterior end, and
progresses posteriorly. That part in which the ectoderm is
separated represents the head-process; it has therefore the same
composition as the primitive streak, except that the ectoderm
has become independent.

Interpretation of the Primitive Streak. The discussion of the
significance of the primitive streak involves two parts: (1) its
morphological significance, and (2) its role in the formation of the
embryo. The first question involves knowledge of comparative
embryology, which is not assumed for the purposes of this book,
and it will therefore be considered very briefly. The fundamental
relations of the primitive streak must define its morphological
interpretation; the first thing to be noted is that the germ-layers,
more especially the ectoderm and mesoderm, are fused in the
primitive streak; second, the differentiated part of the embryo
is formed in front of it; third, the neurenteric canal occupies the
anterior end of the primitive streak; fourth, the anus forms at its
posterior end. Now these characters are exactly those of the
blastopore or primitive mouth of lower vertebrates, that is of the
aperture of invagination of the archenteron. For these reasons,
and because in all other essential respects the primitive streak
corresponds to the blastopore, it must be interpreted as the homo-
logue of the latter. It is to be regarded, therefore, as an elongated
blastopore, and the primitive groove as a rudimentary archenteric
invagination.

This interpretation raises the question as to its relation to
the original marginal area of invagination of the entoderm. Can
these two things be really different stages of the same thing?
The concrescence theory gives a theoretical basis for their iden-
tification. It will be remembered that the margin of invagina-
tion represents a small section of the margin of the primitive
blastoderm in the pigeon, and, by inference, in the chick also.
The remainder of the margin where the zone of junction persists
is the margin of overgrowth. Now we assume that the closure
of the original marginal area of invagination proceeds by con-
crescence or coalescence of its lips, beginning in the middle line
behind, thus producing a suture which is the beginning of the
primitive streak. Let the above circles (Fig. 43) represent the
blastoderm in four stages of closure of the original area of invag-

84 THE DEVELOPMENT OF THE CHICK

illation. The shaded margin represents the zone of junction, the
unshaded portion of the margin represents the area of invagina-
tion of the entoderm. The dotted contour represents the margin
of the pellucid area. In A the middle of the area of invagination
is marked 1, and corresponding points to the right and left 2, 3,
and 4. In diagram B it is supposed that the margin of invagina-
tion is turned forward at 1, and that the lateral portions are
brought together as far as 2, thus producing a suture in the middle
line 1-2 continuous with the margin 3-4. The zone of invagina-
tion is correspondingly reduced in extent and the zone of junction
increased. In diagram C the lateral lips of the zone of invagina-
tion are represented as completely concresced, thus producing a
median suture 1, 2, 3, 4, extending through the posterior half
of the area pellucida to the margin. The zone of junction is
on the point of closing behind the line of concrescence which is
the primordium of the primitive streak. In diagram D, finally,
the opaque area has closed in behind the line of concrescence
which occupies the hinder half of the pellucid area.

To apply this theory to the actual data of the development,
it is only necessary to assume that the entoderm separates from
the ectoderm along the line of concrescence, and that the primi-
tive streak arises subsequently along the same line. The actual
demonstration of the truth of this conception cannot be furnished
bv observation alone, however detailed. It is, however, possilDle
to test it by experiment, though difficult because the concrescence
must take place, if at all, prior to laying. The strong support
of the theory lies at present in the data of comparative embry-
ology; in the lower vertebrates the mesoderm and entoderm
are both formed from the margin of invagination.

Summarizing the matter, we may say that in the chick gastru-
lation is divided into two separate processes: the first is the in-
vagination of the entoderm from the margin, and the second is
the ingrowth (or invagination) of mesoblast and notochord from
the primitive streak, which represents the coalesced lips of the
margin of invagination; the primitive groove is therefore the
expression of a second phase of invagination.

The genetic relation of the primitive streak to the margin of
the blastoderm is well illustrated by an abnormal blastoderm
described bv Whitman in which the primitive groove was con-
tinned across the area opaca to a marginal notch at the posterior

FROM LAYING TO FORMATION OF FIRST SOMITE 85

end. A similar marginal notch at the hinder end of the blasto-
derm in the line of prolongation of the primitive streak has been
described also by His and Raiiber, but in the cases observed
by them there was no connection with the primitive groove.
It suggested to them, however, the idea of genetic connection
between the two, and was used as argument for the derivation
of the primitive streak from the margin by concrescence.

The second question concerning the primitive streak, its role
in the formation of the embryo, may be answered very briefly
by saying that it is itself the primordium of the greater portion
of the axis of the embryo; some indeed maintain that it represents
the entire embryonic axis excepting the short pre-chordal part
(Kopsch). The view of Balfour and Dursy that it takes no essen-
tial part in the formation of the embryo, but atrophies as the
embryo forms, is now of historical interest only. The question
is how much of the embryo is represented by the primitive streak.
But this question is by no means easy to answer, and there is
no complete agreement in regard to it. The one point that is
definitely settled is that the anus arises at the hinder end of the
primitive streak; but what point in the embryo corresponds to
the anterior end of the primitive streak, or, in other words, how
much of the embryo is laid down in the blastoderm in front of
the primitive streak, is a disputed question. The attempt has
been made to solve the problem by destroying the anterior end
of the primitive streak by a hot needle, or by electrolysis, then
sealing up the egg and permitting it to develop farther and finally
locating the resultant injury in the embryo. But, while one
worker finds the injury at the anterior end of the notochord
(Kopsch), that is in the region of the fore-brain, another finds it
in the region of the heart, that is in the hind-brain (Peebles).
The reasons for this discrepancy in results are two: (1) the methods
employed are not sufficiently exact, and (2) it is difficult in the
living egg to determine the exact location of the anterior end of
the primitive streak, and sometimes even to distinguish it from
the head-process. Owing to the extremely rapid growth of all
parts of the embryonic axis, a minute division of the primitive
streak becomes a relatively long part of the embryonic axis in a
very short time. It is obvious, therefore, that the slightest
deviation of the injury from the point aimed at may lead to

86 THE DEVELOPMENT OF THE CHICK

considerable error in the results. The result of Kopsch, however,
is more consistent with our knowledge of other forms.

III. The Mesoderm of the Opaque Area

We have seen that the mesoderm arises from the sides of the
head-process and the primitive streak, and grows out between
the ectoderm and the entoderm to the margin of the pellucid
area; it then begins to overlap the opaque area at first behind,
later at the sides, appearing between the ectoderm and the germ-
wall. Figs. 44 A, B, C, and 45 illustrate its peripheral extension;
at first it spreads most rapidly behind the embryo, but soon ex-
tends with equal speed opposite the primitive streak, and thus
a considerable portion of the area opaca becomes three-laj^ered,
consisting of ectoderm, mesoderm, and germ-wall (Figs. 40 C
and 41). The contour of the anterior margin of the mesoderm
it as first rounded, convex anteriorly (Figs. 44 A and B). Then
the antero-lateral angles of the mesoblast begin to extend forward
so that the anterior boundary becomes concave (Fig. 44 C) ; the
lateral horns thus established continue to grow forward and
ultimately meet in front of the head (Fig. 45) ; they thus bound a
mesoblast-free area in front of and beneath the head, known
as the proamnion, into which the mesoderm does not penetrate
until a relatively late stage of development.

Blood-islands (Figs. 44 C and 45) develop early in the three-
layered part of the opaque area; appearing first behind the em-
bryo, they rapidly differentiate forward opposite the sides of
the embryo and follow the expansion of the mesoblast. This
three-layered portion of the opaque area is known as the vascular
area (area vasculosa) after the appearance of the blood-islands.
It soon acquires a very definite peripheral boundary by the forma-
tion of the vena (sinus) terminalis at its margin (Fig. 45). The
two-layered peripheral portion of the opaque area is known as
the vitelline area (area vitellina), and here again we distinguish
two zones, an outer including the zone of junction, and an inner
one (Figs. 32, 33).

The first blood-islands are masses of cells lying on the germ-
wall behind the embryo; the first blood-cells (erythrocytes) and
blood-vessels arise from them, hence their name. Soon after
their origin the blood-islands appear red owing to the formation
of haemoglobin. Between the blood-islands and the ectoderm

FROM LAYING TO FORMATION OF FIRST SOMITE 87

■f.

X

o

tt.

c

.

c

2

*

^^

■*-i

^ •

c2^

7*

>'

a

p • •

r^

ci

^ '

£

ri

^

^

•/5

-J:

—^^

^

1^

^

("-V

^^

r*

^H

—1

o

^

bJL

Xl

cc

**

r^

c3
>

3,

>

-h^

,f

^

-*^

A

^

^*

f-H

r^

^

»— 4

r^

<

f^

V.

^

^

P.

>

xii

c

O

bi

O

>

1

Cl.

-*->

<i3

,

'S

>

a

^

;_

1— (

'""

c

CI.

02

^

'+3

•

J—

^

ce

»— N

•^

Ih

c

^

c

•— 1

^

&.

■^H

y:
^

<

*^

C

CO

/-*

'^

:

_c3

o

-(J

.

1

"Hh

o

!»

^

'^^

' ,

o

;-<

^

.^

O

i^^

j^

■ >

0.

c
(—

"■^

/-H

^

-t—

c;

'

c

r^

.^H

(4—

^

'c

/^

n:

,1—

P-(

X ^ *- "T O l-»H

ry: r* cS << . fc< .

?^ =^ ^ ."^C- fH

o ^ j; r ;- d.

c rz

Si • c

t- X

c3
. 0)

X --H

o •—

r- X ^^ ""^ ?

X
^ X

t- ' — '

<PQ

in

O g CJ

X C !-

"x "^ ci ■
^ r.S
^_ 1^ -r I

0^

5 ^I^

>

^1

8S

THE DEVELOPMENT OF THE CHICK

is a layer of the mesoderm (Fig. 41). If the blood-islands be
reckoned as mesoderm we must distinguish two layers of the
latter, viz., a deep or vascular layer (angioblast) lying next the
germ-wall, and an upper layer next the ectoderm, which may
be called the ccelomic mesoderm, inasmuch as the body-cavity
(coelome) develops within it later.

r

jorg

n F

prstr

\\ -

\ I* • -\, • /I '5 *. ■ ,

\-:^-tIf^^'^'^-u

.V.'

lit.

4 — -3. p.

3"^ ^"^-1

• d vase.

Fig. 45. — Blastoderm and embryo at the stage of four-
teen somites. The horns of mesoblast are on the point
of meeting in front of the head.

a. p., Area pelkicida. a. vase, Area vaseulosa. a. v. i..
Area viteUina interna. Ht., Heart, n. F., Neural folds,
pr'a., Proamnion, pr. str., Primitive streak. S. t., Sinus
terminalis.

There are two sharply contrasted views concerning the origin
of the mesoblast in the area opaca. According to the one point
of view it is simply a peripheral extension of the primitive streak
mesoblast with which as a matter of fact it is continuous (Hert-
wig, Rabl, and others). According to the other point of view

FROM LAYING TO FORMATIOX OF FIRST SOMITE 89

it is split off from the germ-wall (His and others). One thing
is perfectly clear, viz., that the mesoderm of the opaque area
arises in continuity with the primitive streak mesoderm; the
second view would therefore be better expressed, as Riickert
states it, that the primitive streak mesoderm grows in the region
of the area opaca at the expense of elements of the germinal wall.

If the cells of the primitive streak mesoblast be compared
with the cells of the forming blood-islands a sharp contrast is
observed; the mesoblast cells of the area pellucida are devoid of
yolk-granules; young blood-islands on the other hand contain
yolk-granules of precisely the same character as those of the
germ-wall (Fig. 41), which must have been derived from the latter.
If the origin of the blood-islands be carefully traced, they are
found to be rooted in the protoplasm of the germ-wall; and prior
to the appearance of the blood-islands proper, protoplasm and
nuclei of the germ-wall aggregate superficially in a manner that
appears to foreshadow the blood-islands. Therefore, either the
blood-islands are derived from the cells of the germ-wall, or
cells of the mesoderm growing over the germ-wall burrow into
the latter, engulf yolk-spheres, and reappear in masses as blood-
islands. Patterson (1909) has shown by an experimental study
that in any region in which primitive streak mesoblast is pre-
vented from reaching the germ- wall, blood-islands fail to develop.
The second alternative is therefore probably right in principle.

Another question concerns the origin of the layer of coelomic
mesoblast that overlies the blood-islands: is it derived from the
primitive streak mesoblast, or is it split off from the blood-islands?
When the latter first appear, in the periphery of the vascular area
at least, there is no coelomic mesoblast above them. It appears
later, at first not as a coherent layer, but as scattered cells that
rapidly unite to form a layer. In many places the microscopical ap-
pearances indicate strongly that the cells are split off from the sur-
face of the blood-islands; but, as they are usually not far from the
edge of the advancing coelomic mesoblast, it may be that they are
derived from the latter. Riickert states, however, that, in the case
of some isolated blood-islands behind the embryo, a layer of meso-
blast is formed over them while they are still isolated. This would
render the derivation from the blood-islands probable in such cases.
It is possible, therefore, that the coelomic mesoblast grows partly,
at least, at the expense of the superficial cells of blood-islands.

90 THE DEVELOPMENT OF THE CHICK

As rapidly as they are formed the various blood-islands con-
nect and anastomose with one another, forming a vascular net-
work Ivino; between the coelomic mesoblast and the remains of
the germ-wall. This network spreads throughout the vascular
area, and appears later in the pellucid area, and communicates
with the blood-vessels of the embryo (Figs. 44 and 45). In the
next chapter we shall consider the manner in which the extension
takes place, and the origin of the blood-vessels and blood-cells.

IV. The Germ-wall

The germ-wall arises, as we have seen, through infiltration
of the superficial white yolk by the periblast. These cells mul-
tiply and anastomose and form a multinucleated syncytium with
the yolk-granules in its meshes. By degrees the protoplasm itself
takes up the j^olk-granules, which are gradually digested, and the
germ-wall thus becomes organized as a coherent layer. It then
separates from the underlying yolk. The next period in the
history of the germ-wall is its differentiation, which takes place
in the vascular area concomitantly Avith the formation of the blood-
islands: a considerable proportion of the protoplasm and nuclei
of the germ-wall accumulates at the surface and forms the vascu-
lar mesoderm in the manner already described. The part of the
germ-wall that remains after the separation of the mesoderm then
differentiates into the characteristic entodermal epithelium of the
opaque area, which is known as the yolk-sac epithelium (ento-
derm) because it is destined to form the lining of the yolk-sac.

After the formation of the vascular area the term germ-wall
must be restricted to the lower layer of the vitelline area, because
within the vascular area it has already differentiated into the
mesoderm and yolk-sac entoderm. The development of the
germ-wall takes place in a centripetal direction; at any period
during the overgrowth of the yolk the three stages of the germ-
wall may be found in the concentric zones. The first stage,
that of periblast, is found in the zone of junction (area vitellina
externa); the second stage, that of organization of the germ-
wall, is found in the area vitellina interna; and the third stage,
that of differentiation, is found at the margin of the area vascu-
losa. Within the latter area the differentiation is completed.

CHAPTER V
HEAD-FOLD TO TWELVE SOMITES

(From about the twenty-first to the thirty-third hour of incubation)

I. Origin of the Head-fold

At the end of the period described in Chapter IV, the embryo
is represented by a central differentiated area of the blastoderm,
lying within the area pellucida, distinguished anteriorly by the
medullary plate and head-process, and posteriorly by the primitive
streak. The layers of the embryonic area are everywhere continu-
ous with the corresponding layers of the extra-embryonic blasto-
derm, with no clear line of division between the two. In the course
of the second and third days the embryo becomes clearly defined
by its own growth, and by the formation of bounding folds.

The delimitation of the embryo from the blastoderm begins
immediately after the formation of the head-process by the for-
mation of a fold at the anterior end of medullary plate known as
the head-fold (Fig. 42). Seen from the surface, this fold has a
semicircular outline, the concavity of which is directed posteriorly
(Fig. 44). It involves both the ectoderm and entoderm. A later
stage is shown in sagittal section in Figs. 46 and 47: the ecto-
derm and entoderm immediately in front of the medullary plate
make a sharp bend downwards and backwards, and then turn
forward again. The head-fold thus produces an internal bay in
the entoderm, the beginning of the fore-gut. There is similarly an
external bay, the posterior angle of which is the head-fold proper,
lying beneath the projecting head. These bays are of course
turned in opposite directions, the internal one opening into the
subgerminal cavity posteriorly, and the external one opening
anteriorly on the surface of the blastoderm.

The transition from the ectoderm of the medullary plate into
that of the under surface of the head and the proamnion is a grad-
ual one. The difference is, however, very strongly marked (Fig.
47). The formation of the head-fold is due to the more rapid

91

92

THE DEVELOPMENT OF THE CHICK

b£

-^ >

S ^-^

■fTlii'f'S?

r '^

5 e^ffi

C o

'^ ^ £

A rt

C C ,<* i-

b£0 «

is 2

^ ^ ^

Q w CC

^ ^^

: ->^

X

im

growth of the medullary plate,
which causes the latter to extend
forward above the thinner and more
pliable membrane in front. The
entoderm is attached to the inner
surface of the anterior end of the
medullary plate (Fig. 47), and is
apparently carried forw^ard with the
latter to form the anterior portion
of the fore-gut. The actual form of
the fold depends upon the mechani-
cal properties of the membranes
concerned, especially the unequal
thickness of their parts produced
by unequal growth.

Although the head-fold thus ap-
pears to be a single fold involving
the two primary layers, it is con-
venient, for purposes of description,
to consider it as two separate folds,
ectodermal and entodermal. The
deepening of these folds takes place
at the same rate up to the time
when four somites are formed (Fig.
49). At about this time the paired
primordia of the parietal cavity
(amnio-cardiac vesicles), which ap-
pear in the mesoblast in the lateral
extensions of the head-fold (Fig.
50), push in towards the mid-
dle line so as to separate the ecto-
dermal and entodermal limbs (Figs.
52 and 58). When six somites
are formed, these cavities fuse in
the middle line, thus effecting a
complete separation of the two
limbs. The further progression of
the head-fold, after this union,
takes place separately in the two
limbs.

HEAD-FOLD TO TWEL\'E SOMITES

93

11. Formation of the Fore-gut
The extension of the amnio-cardiac vesicles between the
ectodermal and entodermal layers of the head-fold introduces a
section of the body-cavity (pericardium) between these layers
and at the same time converts the ectodermal liml) into a portion
of the somatopleure, and the entodermal limb into a portion of
the splanchnopleure. (See p. 115.) The splanchnopleuric
head-fold extends posteriorly very rapidly after the invasion
of the body-cavity, while the somatopleuric fold apparently
remains fixed for some time, though the head-fold appears to

Fig. 47. — Head-fold region of Fig. 46 highly
magnified.
For abbreviations see Fig. 46.

become deeper, owing to the forward extension of the head
above the blastoderm. The posterior extension of the splanch-
nopleuric head-fold lengthens the floor of the fore-gut; it is
caused by the median growth and concrescence of folds of the
splanchnopleure (Fig. 53). Along with this process is involved
the development of the heart described farther on. The growth
in length of the fore-gut may be realized by a comparison of
Figs. 50, 52, 62, etc.

Thus by the 12 s stage a considerable section of the fore-gut
is already established (Fig. 63); this is the pharyngeal division;
from the first it is extremely broad, and lunate in cross-section
(Fig. 54), the floor being composed of columnar cells, and the roof

94

THE DEVELOPMENT OF THE CHICK

of very flat cells. The lateral extensions may be regarded as
diverticula; subsequently these grow more rapidly at four places
along their length, and come in contact with the ectoderm. Thus
four pouches are established on each side as described in detail

fi.gr

&o.

Fig. 48. — Stage of first intersomitic groove
drawn from an entire mount in balsam by
transmitted light,
a. c. v., Amnio-cardiac vesicle, a. o., In-
ner margin of Area opaca. Ect., Ectoderm.
Ent., Entoderm H. F., Head -fold. i. s.f.l.,
First intersomitic furrow, med. pi., Medullary
plate. Mes., Mesoderm, n. gr., Neural groove,
pr. gr., Primitive groove. Pr'a, proamnion.

in the next chapter. At the 12 s stage one such place of contact
is already formed, lying a short distance in front of the thickened
ectoderm destined to form the auditory pit.

HEAD-FOLD TO TWELVE SOMITES

95

Another place of fusion between the fore-gut and the ecto-
derm is the so-called oral plate (pharyngeal membrane), which
occupies a mid-ventral position at the extreme anterior end.
The parietal cavities meet posterior to the oral plate (Figs. 67
and 75). Transverse sections show the oral plate to be depressed
beneath the level of the ventral surface of the head at the stage of
10 somites (Fig. 55), a condition that increases, as development

/f./r

e.ijO.

Fig. 49. — Median sagittal section of the head at the stage of 4 s.

a. i. p., Anterior intestinal portal. F. G., Fore-gut. Ect., Ectoderm.
Ent., Entoderm. H. F., head-fold. Mes., Mesoblast. n. F., Neural fold,
or. pi., Oral plate.

proceeds, by the formation of the cranial fiexture, and by the up-
growth of the tissues behind and at its sides; thus will be estab-
lished a deep depression lined by ectoderm, the floor of which is
formed by the oral plate, and which is destined to form a large
part of the mouth. The depression is known as the stomodseum.

IIL Origin of the Neural Tube
The Medullary Plate. The medullary plate is the primordium
of the central nervous system. At the time of formation of the
head-fold it is broad in front and narrower posteriorly, ending
opposite the posterior end of the primitive streak. Its central
portion is not a separate plate of cells in the region of the primi-

96

THE DEVELOPMENT OF THE CHICK

tive streak, but this part becomes distinct as the i^rimitive streak
splits into its derivatives. It is therefore only when the latter
is entirely used up that the entire length of the medullary plate
is established. However, long before this time the greater por-
tion has become converted by folding into the neural tube, a
process that proceeds in general from in front backwards. Thus

a.o.

re.

n.F.

— SJ.

-s.z.

-^.3.

-pr.gr.

Fig. 50. — Embryo of 3 s from above, drawn in bal-
sam with transmitted light.

a. c. v., Amnio-cardiac vesicle, a. o., inner margin
of Area opaca. F. G., Fore-gut. N'ch., Notochord.
n. F., Neural fold. pr. gr., Primitive groove, s. l,s. 2,
s. 3, First, second and third somites.

successive stages may be studied in serial sections of the same
embryo; an anterior section, for instance, showing the completed
tube, one farther back, the folded medullary plate, and yet more
posteriorly the central part of the medullary plate disappears in

HEAD-FOLD TO TWELVE SOMITES

97

the undifferentiated mass of the primitive streak. These condi-
tions must be born in mind in the following description.

The Neural Groove and Folds. Shortly after the formation of
the head-fold the center of the medullary plate becomes sunk in
the form of a deep groove beginning a short distance behind the

Fig. 5L — Embryo of 4 s from above, drawn in alcohol by reflected light.

a. c. v., Amnio-cardiac vesicle, a. p., Area pellucida. a. v. i., Inter-
nal vitelline area. med. pi., Medullary plate, n. F., Neural fold. Pr'a.,
Proamnion, pr. str., Primitive streak, s. 1, s. 3, First and third
somites.

98 THE DEVELOPMENT OF THE CHICK

anterior end of the plate (Fig. 48) (the neural groove) ; the mar-
gins of the anterior portion of the medullary plate then become
elevated somewhat above the surrounding blastoderm, forming

eip

• ji --■>-♦ f

%

-'.-/*

Fig. 52. — The same embryo from beneath,
a. c. v., Amnio-cardiac vesicle, a. i. p., Anterior intestinal portal.
H. F., Head-fold. Pr'a., Proamnion.

the neural folds (Figs. 51 and 56). The latter rise very rapidly,,
thus deepening the neural groove, and bend in towards the middle
line (Figs. 53, 54, etc.,) meeting, by the time four or five somites are

HEAD-FOLD TO TWELVE SOMITES

99

formed, a short distance back of the anterior end of the medullary
plate (Figs. 50 and 51). The posterior ends of the neural folds
do not, at this time, reach the region of the first somite. The
region where the neural folds first come in contact corresponds
approximately with the region of the future mid-brain, or ante-
rior part of the hind-brain.

Fig. 52 A. — Median longitudinal section of the head, stage of 4 s. The sec-
tion passes through the length of one of the neural folds just behind the
anterior end. (Cf. Fig. 5L)
a. i. p., Anterior intestinal portal. Ect., Ectoderm. Ent., Entoderm.
F. G., Fore-gut. H. F., Head-fold. Mes., Mesoderm. Mes. H. C, Meso-
blastic head cavity, n. F., Neural fold. or. pi., Oral plate.

The process of closure itself is essentially the same in all
regions of the neural tube. Each neural fold has two limbs: an
inner thick limb, belonging to the medullar}' plate, and an outer,
thin limb, continuous with the general ectoderm (cf. Fig. 68 B).
When the folds of opposite sides come in contact, the inner limbs
of the two sides become continuous with one another, and also
the outer limbs, the ectoderm then passing continuously over a
closed neural tube.

Certain cells in the suture and in the walls of the tube next

100

THE DEVELOPMENT OF THE CHICK

* r- (

-4-^

c ^

bJO

o

I— -^

If^

r-^

'— J,

i~ G

ZJ

,

c

S

T3

^

^

a

3^ p^

r^

c3

o3 ^
s^ O

• 1— <

-t-S

t^-^

•i-H

Ho
r o

O

^

f^£:

o

Ifl

r^^

(-^

o

H

X

>

o

'c3

6

~I-J

^

oT

t^

1

tCH

c

O '^

O

-M

-^ '^

c3

o

-1^

r^

Oi

o

H ^

>l 1

• ^H

•

-l-i

c

> ^^

+J

^^

c3

>5

l5

^

^

O

c5

•^^ '^

;>^

O

C s-i

r-i

C =3

Is

©

2§

_G

-C

H^^SS

'-+3

-♦^

cc

•— ' r^ ;-(

o

o

^ O

-(^

?J^ ^'^

^H

r-i

^ o o

in

o
• 1— (
-^

S

i5

o

=-1-1
o

«3 S K>

o

^

S A'o

■+-J

^

,xz '-^

re

T3

OJ

o

«r^ r

,

^ ."Xi

02

S3

^0^

^

<a

■ >^

•I— »

-^

X

^^

s

C3 ri

^-«

r^

o

«+-!

5 >.

t3

o

o

i^ 03

a;

o

^ -

a;

o

•^ d^.

>

CO

>H-g

c

fl

o3 ^ o3

03

o
o

^

r.^Q

X!

cu

03 a

CO

g

> •

LO

p

. >5 .

,

o

03 .t^

o

«+H

>^

l-H

03 :3

h^

-f^

HEAD-FOLD TO TWELVE SOMITES

101

the ectoderm are destined to form the neural crest, a structure
of great significance, inasmuch as the series of cranial and spinal
ganglia is derived from it. (See following chapter.)

J'Som'f/.

] -3 pi' pi.

«ri>-*c*?*^*c^

Fig. 54. — Transverse section through the same embryo a short distance
in front of the anterior intestinal portal. For explanation of letters see
preceding figure; in addition: Ph., Pharynx. Som'pl., Somatopleure.
Spl'pl., Splanchnopleure. v. M., Ventral Mesentery.

Fig. 54 a. — Transverse section through the head of a 10 s embryo. The

region of the section is near the center of the hind brain.

Ao., Aorta. End'c, Endocardium. End'c. S., Endocardial septum.
H. B., Hind brain. My'c, Myocardium, p. C, Parietal cavity. Ph., pharynx.
So'pl., Somatopleure. Spl'pl., Splanchnopleure. v. M., Ventral mesentery.

The Neuropore. From the place where the neural folds first
meet, the elevation and fusion proceed both forwards and back-
wards in a continuous fashion (cf. Figs. 59, 61, 65, etc.). Although
the open anterior stretch of the neural tube is very short in com-
parison to the posterior open part, it is not until about the 12 s

102

THE DEVELOPMENT OF THE CHICK

stage that the former closes completely (cf. Fig. 64). The final
point of closure at the anterior end, known as the neuropore, is
supposed by some to be a point of great morphological signifi-
cance, and to mark the extreme anterior end of the original neural

ax: Mes.

Fig. 55. — Transverse section through the head immediately behind the

optic vesicles; stage, 10 s.

Ao., Aorta, ax. Mes., Axial mesoblast. Ect., Ectoderm. Ent., Entoderm.
]\I. A., Mandibular arch. M. B., Mid-biain. ]Mes., Mesoderm, or. pi., Oral
plate, p'a. c, Periaxial cord. p. C, Parietal cavity. Pr'a., Proamnion. Ph.,
Pharynx, v. Ao., Ventral aorta.

axis. It is identified by these writers with the permanent neuro-
pore of Amphioxus. However, this is open to question. Poste-
riorly the closure of the neural tube proceeds much more rapidly,
though, of course, it is not fully completed untd after the disap-
pearance of the primitive streak.

-,_ medpl.

^■F

"^^Ec^.

m^^^mmi^^^^smis^-

Fig. 56. — Early stage of the neural folds. Transverse section through a

4-5 s embryo between the last somite and the anterior end of the primitive

streak.

Ect., Ectoderm. Ent., Entoderm, n. F., Neural fold. N'ch., Noto-
chord. med. pi., Medullary plate. Mes., Mesoderm.

The question as to the position of the anterior end of the
original neural axis is one of great morphological significance.
Accompanying the closure of the neural tube in this region the

HEAD-FOLD TO TWELVE SOMITES

103

yjf.

//.A

/?.C/

r

J7 Cr.

TtTaiv'

dC.

medpi

/^..

«3Bi^

^•■?/^;tv

^C^/

— >*-<?.

Fig. 57. — Later stage of the neural folds. Section through the head of an

embryo of 2-3 s; corresponding to about the future mid-brain region.

Coel., Coelome. g. C, Germinal cells, med. pi., Medullary plate. Mes.,

Mesoblast. n. F., Neural fold. n. Cr., Neural crest. N'ch., Notochord. som.

Mes., Somatic layer of mesoblast. spl. Mes., Splanchnic layer of mesoblast.

anterior end rapidly grows forward beyond the anterior end of
the fore-gut. The floor of the neural tube does not, however,
take part in this extension, the consequence being that the sum-
mits of the neural folds form
arching knees extending in front
of the original anterior end of
the medullary plate (Figs. 51
and 52). The extreme anterior
end of the neural tube formed
in this way has a ventral as well
as a dorsal defect, and when it
closes there is a ventral as well
as a dorsal suture. The end
of the ventral suture marks the
original anterior end of the me-
dullary plate, and this lies at
the stage of 10 somites a short
distance in front of the ante-
rior end of the oral plate in
the region of the future re-
cessus opticus (Fig. 62). (Go-
ronowitsch calls the anterior
fissure, sutura cerehralis ante-
rior; His divided it into two

Afy'C.

^C/).

Fig. 58. — Ventral view of the head

region of an embryo of 5 somites,

drawn in balsam with transmitted

light. X 30.

a. c. v., Amnio-cardiac vesicle,
a. i. p.. Anterior intestinal portal.
F. G., Fore-gut. My'c, Myocardium.
N'ch., Notochord. n. F., Neural fold.
s 2, s 4, Second and fourth somites^

104

THE DEVELOPMENT OF THE CHICK

a.c.s.

op. Ves.
cep/i. Mes

EG.

V.o.m.

3. a

/}.T.

3.Z

//eh.

pr. str.

Fig. 59. — Embryo of 7 s from above drawn

in balsam with transmitted light, x 30.

a. c. s., Anterior cerebral suture, ceph.
Mes., Cephalic Mesoblast. F. G., Fore-gut.
N'ch., Notochord. n. T., Neural tube. op.
Ves., Optic vesicle. Pr'a., Proamnion. i)r.
str., Primitive streak, s 2, s 7, Second and
seventh somites. V. o. m., Omphalo-mes-
enteric vein.

HEAD-FOLD TO TWELVE SOIMITES

105

parts, sutura neurochordalis sen ventralis and sutura termi7ialis
anterior.)

The neuropore question resolves itself into this: What part
of the sutura cerebralis anterior is to be called neuropore? As
the suture extends from near the infundibulum to the pineal
region at least, there is a wide range of choice. However, there
is a point in the suture near its dorsal end where the separation
of the ectoderm from the neural tube takes place later than
elsewhere. This may be regarded as the equivalent of the
neuropore. The suture is the site of formation of the lamina
terminalis (Chap. VIII).

op- Ves ■

a.i.p.

Fig. 60. — The head of the same embryo from

below X 30.

a. i. p., Anterior intestinal portal. End'c. s.,
Endocardial septum. F. G., Fore-f:;ut. Ht., Heart.
N'ch. T., Termination of Notochord. op. Ves.,
Optic vesicle, p. C, Parietal cavity. Pr'a., Pro-
amnion. V. o. m., Omphalo-mesenteric vein.

It will l^e seen that according to this account most of the
primary fore-brain includes no part of the original floor of the
neural tube.

Primary Divisions of the Neural Tube. The neural tube is the
primordium of the brain and spinal cord. Its cavity becomes the
ventricles of the brain and the central canal of the cord. There

106

THE DEVELOPMENT OF THE CHICK

. ■:: -:^>;rt\vJa:i:S-;;|■

jor.str.

•^

■ •■; ##.;

.//

Fig. 61. — Embryo of 9 s from above drawn

as a transparent object with transmitted

light. X 30.

Abbreviations same as before; in addi-
tion: H. B., Hind brain. M. B., Mid brain.
n. S.j Neural suture.

HEAD-FOLD TO T\YELVE SOLUTES

107

o/)Ves.
ceph. Mes. -^

^v?s^#^'

S^'

^^^

/'-

• //?/.

jVch.T.
or.pl.

MA.

N.r.
p.C.

Ht.

\

V.o./n

d.l.p.

*

" N

End'c.5.

S.B.

-M L ^ V

Fig. 62. — The head of the same embryo from beneath more
highly magnified. In this drawing an attempt is made to
show different levels of the embryo superposed: thus the
heart is uppermost in the figure, beneath this the fore-gut
(F. G.), beneath this the notochord, and at the lowest level,
the neural tube,
a. c. s., Anterior cerebral suture. Inf., Infundibulum.

M. A., Mandibular arch. p. C, represents the anterior

boundary of the parietal cavity, or. pi., Oral plate. Other

abbreviations as before.

is no clear distinction between l)rain and cord at first, the one
passing without any anatomical landmark into the other. Now
the brain is the central nervous system of the head, so it is not
until one can determine the posterior boundary of the embryonic
head that it becomes possible to determine the hind end of the

108 THE DEVELOPMENT OF THE CHICK

brain. The first clear landmark is given by the mesoblastic so-
mites, because it is known that the four anterior somites are
cephalic. All of the neural tube in front of the fifth somite is
therefore cranial. What a large proportion of the neural tube
this is in early stages may be seen by comparison of figures of
embryos in the period covered by the chapter (cf. Fig. 61). Be-
fore the appearance of the first somite the entire medullary plate
in front of the primitive streak is in fact cranial.

Origin of the Primary Divisions of the Embryonic Brain. The
embryonic brain is divided into three divisions of unequal length,
viz., the fore-brain (prosencephalon), mid-brain {mesencephalon),
and hind-brain (rhombencephalon). The first division is character-
ized in the period we are considering by its very considerable
lateral expansions, the rudiments of the optic vesicles (Figs. 59,
61, 63, etc.), and also by the fact that there is a suture in the
anterior portion of its floor owing to the mode of its origin (Fig.
62). A definite constriction between it and the following division
first appears in embryos Avith six or seven somites (Fig. 59). At
the stage of 9-10 somites the next division (mid-brain) becomes
clearly marked off by a constriction from the hind-brain (Fig.
61). The latter is relatively very long, and its anterior half is
characterized in the 12-somite stage by the existence of five divi-
sions (neuromeres) separated by constrictions (Fig. 63).

It will be noted that the first neuromere of the hind-brain appears
about twice as large as the succeeding ones ; it really includes two neuro-
meres according to some authors. Similarly, it is maintained that the
mid -brain includes two neuromeres and the fore-brain three.

According to Hill's account the entire brain of the embrj^o chick
is composed of eleven neuromeres or neural segments, which are formed
even in the 1 s stage. The first three enter into the composition of the
fore-brain; the next two, viz., 4 and 5, form the mid-brain, and the last
six the hind-brain.

The three that enter into the composition of the primary fore-brain
have the following fate according to Hill: the first forms the telen-
cephalon, the second the anterior division (parencephalon) and the third
the posterior division (synencephalon) of the diencephalon. The cere-
bellum arises from the first neuromere of the hind-brain, sixth of the
series. This question is more fully discussed in Chapter VI. (See
Fig. 83.)

HEAD-FOLD TO TWELVE SOMITES

109

N.B

op. Ves.

■M.B.
FG.

Hi.

j 0;;-.o:-^-.'.-.Cr

Ao.

-3. IS.

■■^

-pr str.

Fig. 63. — Embryo of 12 s, from above, drawn
as a transparent object with transmitted
light. X 30. Abbreviations as before.

IV. The Mesoblast

The changes in the mesoblast during this period are of great
importance. At the time of appearance of the liead-fold it con-
sists of two great sheets of cells between ectoderm and entoderm

no

THE DEVELOPMENT OF THE CHICK

beginning on each side of the head-process and primitive streak,
and extending laterally and posteriorly to the margin of the
vascular area. The lateral margins at this time extend anterior to
the embryonic axis, so that the anterior margin of the mesoblast
forms a curve with the concavity directed forward.

Fig. 64. — Head of the same embryo from
below. X 30. Abbreviations as before.

The mesoblast in the region in front of the primitive streak
is known as gastral mesoblast, and in the region of the primitive
streak as prostomial mesoblast; the latter is fused with the primi-
tive streak. However, the distinction between the gastral and
prostomial mesoblast is not of permanent significance, because
the latter is being continually converted into the former as the
primitive streak undergoes separation into ectoderm, notochord,
and mesoderm.

Confining our account now to the gastral mesoblast: a trans-
verse section across an embryo in which the head-fold is forming
shows a sheet of cells lying on each side of the notochord between
the ectoderm and entoderm. It is several cells deep near the
notochord, and thins gradually peripheralh' (cf. Fig. 56). The
thicker portion next the notochord is distinguished as the paraxial
mesoblast (vertebral plate) from the more peripheral portion or
lateral plate. The mesoblast is sparser, the cells more scattered,

HEAD-FOLD TO TWELVE SOMITES 111

and the whole tissue of much looser texture in the more anterior
portions of the embryo.

The paraxial mesoblast increases rapidly in thickness and
thus becomes clearly distinguishable from the lateral plate.
Shortly after the formation of the head-fold a transverse cleft
appears in the paraxial mesoblast a short distance in front of the
anterior end of the primitive streak (Fig. 48). This is soon fol-
lowed by a second cleft, a very short distance behind the first,
and thus a complete mesohlastic somite is established. The division
is accomplished rather by segregation of the cells than by an
actual folding. The mesoblast cells immediately in front of the
first cleft aggregate so as to form a somite continuous anteriorly
with the mesoblast of the head, thus lacking an anterior
boundary; this is the first somite, and the one formed between
the first two clefts in the mesoblast is the second.

The first somite established is first, not only in point of time,
but also in position, all the remainder forming in succession behind
this (cf. Figs. 48, 50, 51, 59, 61, etc.). As this is a point of con-
siderable importance for understanding the topography of the
embryo, and as previous text-books have a different account of
it, it is worth while to give the evidence for this position in some
detail. It has been believed up to a very recent time that from
two to four somites were formed in front of the first one. This
belief was due very largely to a misconception of the nature of
the primitive streak, which was believed by some to be extra-
eml^ryonic, that is to lie behind the embryo and not to be a part
of the embryo itself. The first somite lies so near to the anterior
end of the primitive streak that it was difficult to believe that
room could be made by growth between it and the primitive
streak with sufficient rapidity to accommodate the rapidly form-
ing somites. In the entire absence of differentiated organs it was
impossible to find landmarks by which to distinguish the first
somite among the first five or six; hence it was natural to suppose
that a certain number of somites arose in front of the first, espe-
cially as it Avas not known how much of the anterior portion of
the embryonic axis represented the head. However, in the
absence of natural landmarks identifying the first somite formed,
it is quite possible to create artificial ones, and in this way to
identify it in later stages. This has been done by Miss Marion
Hubbard and by Patterson in the following manner: The posi-

112 THE DEVELOPMENT OF THE CHICK

tion of the first somite was marked immediately after the
appearance of the first cleft with a delicate electrolytic needle
which left a permanent scar. The eggs thus operated on were
closed up and permitted to develop to a stage of from 10

MB.

//.£.

F.B.

3u. ep.

3.^

S.I2.

pr.str.

Fig. 65. — Embryo of 12 s, from above, drawn in alcohol with re-
flected Hght.
au. ep.. Auditory epitheUum. Other abbreviations as before.

to 25 somites; and then the mark was found to coincide
with the first somite of the series. In the next place it was
possible by similar means to mark out the topography of the
embryonic head in the stage of one or two somites. Thus it
was determined that a mark made immediately in front of the
first somite formed appeared later in the region of the otocyst;

HEAD-FOLD TO TWELVE SOMITES

113

but this arises normally at the stage of 12-14 somites, a very
short distance in front of the first somite of the series, which is
thus shown to have the same position as the first somite formed.
On the other hand, if one assumed that the first somite formed

/f.F

HL

yV'cA ^

A.c.y.

Vo.m.

3. 1. p.

Fig. 66. — The same embryo from beneath, drawn in alcohol with

Abbreviations as before.

reflected light.

became the third or fourth of the series, it is clear that one would
have to make a mark some distance in front of the first somite
formed, to strike the place of origin of the otocyst. Marks made
on this theory were always found a considerable distance in
front of the otocyst. Altogether a large number of experiments

114 THE DEVELOPMENT OF THE CHICK

was made, the concurrent testimony of which was perfectly
conclusive.

The somite formed in front of the first cleft is thus the first
in position of the definitive series and the remainder arise in suc-
cession behind it. The formation of the somites therefore follows
the usual law of antero-posterior differentiation.

There is always a stretch of unsegmented paraxial mesoblast
between the last somite and the anterior end of the primitive
streak.

The first four somites belong to the head, and enter into the
composition of the occipital region. The more anterior part of
the mesoblast of the head never becomes segmented in the chick.
In the anamniote vertebrates, segmentation of the mesoblast
extends farther forward, and there is a greater number of cephalic
somites. This may be taken as evidence that a large part, at
least, of the head was primitively segmented like the trunk.
As we shall see later, the primitive metamerism of the head is
also expressed in other ways: neuromeres, branchiomeres, etc.

The segmentation of the mesoblast finally extends to the
hind end of the tail, new segments being continually cut off
from the anterior end of the paraxial mesoblast until it is all used
up. This is not complete until the fifth day. The number of
somites thus formed is perfectly constant, as is also the fate of
the individual somites.

Primary Structure of the Somites. Each somite is primarily
a block of cells arranged in the form of an epithelium around a
small central lumen, towards which the inner ends of all the cells
converge (Fig. 68 B). The central cavity (myocoele) is, however,
filled with an irregularly arranged group of cells, and, though
the cavity must be regarded as part of the primitive body-cavity,
or ccelome, it has no open communication with it. After the
somites are formed they rapidly become thicker so that their
lateral boundary becomes very sharply marked; this is not due
to a longitudinal constriction external to the paraxial mesoblast,
as usually stated. Each somite has six sides, of which five are
free, viz., dorsal, ventral, anterior, posterior, and median. The
sixth or lateral side is continuous with the nephrotome.

The Nephrotome, or Intermediate Cell- mass (Middle Plate).

HEAD-FOLD TO TWELVE SOMITES 115

The somites and the lateral plate are not in immediate contact
but are separated by a short stretch of cells continuous with
both, known as the nephrotome or intermediate cell-mass or
middle plate. The intersegmental furrows do not extend into
the intermediate cell-mass, and the latter therefore remains
unsegmented like the lateral plate. It consists fundamentally
of two layers of cells, dorsal and ventral, of which the former
is continuous with the dorsal wall of the somite and the somatic
layer of the lateral plate, and the latter with the ventral wall
of the somite and the splanchnic layer of the lateral plate (Fig.
68 B). Thus if the two layers of the intermediate cell-mass
were separated the space between them would be continuous
with the coelome that arises secondarily in the lateral j^late. This
condition actually exists in some of the Anamnia (Selachii, for
instance) in which the intermediate cell-mass is also segmented.

The Lateral Plate. This name is given to the lateral meso-
blast within which the body-cavity arises. It is separated from
the somite by the nephrotome and its lateral extension coincides
with the margin of the vascular area.

Development of the Body-cavity or Coelome. The coelome
or body-cavity arises within the lateral plate as a series of sep-
arated small cavities, distributed throughout its whole extent,
which appear first in the anterior portion (1-3 s stage). By
successive fusion of these cavities and their extension centrally
and laterally, there arises a continuous cavity, the coelome,
which extends from the nephrotome to the margin of the vascular
area (Fig. 68), and which becomes the pleuro peritoneal and per-
icardial cavities in the embryo, and the extra-embryonic body-
cavity beyond the boundaries of the embryo.

Of the two lavers of the lateral mesoblast thus established,
the external is known as the somatic and the internal as the
spla7icknic layer. In the course of development the somatic
laver becomes closelv bound to the ectoderm, thus constituting
the somatopleure, and the splanchnic layer becomes similarly
united to the entoderm, thus establishing the splanchnopleure.
The somatopleure is destined to form the body-wall and the
extra-embryonic membranes known as the amnion and chorion;
from the splanchnopleure is derived the alimentary canal with
all its appendages, and the yolk-sac. As described in detail in the
next chapter, this splitting of the mesoblast progresses with

116 THE DEVELOPMENT OF THE CHICK

the overgrowth of the yolk until it extends completely around
the latter

Returning now to the first stages in the formation of the coe-
lome. In the 3 s stage it undergoes a precocious expansion in
the region lateral to the head of the embryo (Figs. 51, 52, etc.),
forming a pair of large cavities known as the amnio-cardiac
vesicles, because they participate in the formation of the amnion
and pericardium. These cavities extend in rapidly towards the
middle line, and enter the head-fold in the 4-5 s stage (Figs. 52,
58). At the stage of 6-7 s they meet in the floor of the fore-gut
immediately behind the oral plate and fuse together, thus divid-
ing the head-fold into somatic and splanchnic limbs, as previously
described. A median undivided portion of the body-cavity
known as the parietal cavity (forerunner of the pericardium)
is thus established beneath the fore-gut; and it extends back-
ward with the elongation of the fore-gut in the manner already
described. A pair of blind prolongations of this cavity extends
a short distance forward at the sides of the oral plate at the 10-12 s
stage (cf. Fig. 62), lying lateral and ventral to the ventral aortse.

The median angle of the body-cavity, where the somatic
and splanchnic layers meet, is a point of fundamental morpho-
logical importance. In the region of the somites the nephrotome
is attached here, and in the head the wdng of cells leading to the
axial mesoblast (cf. Figs. 68 B, 53, and 54). In an embryo
with ten somites this angle may be traced forward to near the
hinder end of the oral plate, lying beneath the lateral angles of
the pharynx.

Mesoblast of the Head. ]\Iesoblast exists in two forms in
the embryo: (1) in the form of epithelial layers or membranes
(mesothelium), and (2) in the form of migrating cells which
usually unite secondarily to form a syncytium in the form of a
network, the meshes of which are filled with fluid; the nuclei
lie in the thickened nodes. This form of the mesoblast is known
as mesench3'me. It is always derived from a pre-existing epi-
thelial layer, usually, but not necessarily, mesothelium, for, as
we shall see, parts of it are derived from ectoderm and entoderm;
on the other hand, mesenchyme may secondarily take on an
epithelial arrangement (endothelium). The terms mesothelium
and mesenchyme have therefore merely descriptive significance
in the early embryonic stages. The mesenchyme has no single

HEAD-FOLD TO TWELVE SOMITES 117

embryonic significance either as to origin or fate, but is to be
regarded as a mixed tissue.

The mesoblast of the head is derived from several sources:
(1) from a continuation forward of the paraxial mesoblast; (2)
by proliferation from the fore-gut; and (3) from proliferations of
ectoderm.

(1) The axial mesoblast of the head is an anterior continua-
tion of that of the trunk; it terminates at the anterior end of the
fore-gut with which it is continuous from the stage of the head-
process up to about the 6 s stage (Figs. 43 and 49). In the
anterior part of the head it is mesenchymal in its general struc-
ture, grading posteriorly into the mesothelial paraxial mesoblast
of the hinder part of the head and trunk. It is continuous at
first with the lateral mesoblast in which the amnio-cardiac
vesicles are forming; but this connection is lost in the anterior
part of the head that projects forward above the blastoderm;
that is, in front of the head-fold.

(2) The anterior end of the fore-gut proliferates mesenchyme
from the time of its first formation to about the 6 s stage (Fig.
49). The proliferation is so rapid that it may give rise to the
appearance of diverticula. The extreme anterior end of the floor
forms a sac which lies just in front of the oral plate at the 4 s
stage (Fig. 52 A), but soon after breaks up into mesenchyme.
There is a considerable mass of mesenchyme formed from this
source in the space bounded by the anterior end of the fore-gut,
the neural tube and the ectoderm ; at the 4 s stage this appears
fused with the floor of the neural tube and the surface ectoderm,
and probably receives cells from both; the anterior end of the
notochord also disappears in this mass (cf. Fig. 67).

(3) Ectodermal proliferations forming mesenchyme in the
head. (This subject is discussed in the next chapter.)

Vascular System. The origin of the blood-islands in the
opaque area was described in the preceding chapter. They lie
between the coelomic mesoblast and the yolk-sac entoderm de-
rived from the germ-wall. When the somatopleure and splanch-
nopleure are formed the blood-islands lie between the two layers
of the latter, and the somatopleure is entirely bloodless. About
the stage of 1 somite a vascular network continuous with the
original network of the opaque area begins to appear in the
pellucid area, at first at the margin of the opaque area, but by

118 THE DEVELOPMENT OF THE CHICK

degrees nearer and nearer to the embryo, until, by the 7 or 8 s
stage, blood-vessels begin to appear in the embryo itself. It is
important to note that the order of appearance of the vascular
primordia is first in the area opaca in the order previously de-
scribed, then in the pellucid area and finally in the embryo itself.
Moreover, the parts appearing later are, usually at least, in con-
tinuity with those first formed.

Before discussing the way in which the blood-vessels arise
in the pellucid area and in the embryo, we should consider the
first differentiation within the original, or peripheral, blood-
islands. Between the 3 and 5 s stage it may be noticed in
sections that vacuoles are forming within the peripheral blood-
islands near the entodermal surface. The expansion of these
vacuoles carries the peripheral layer of cells away from the main
mass of cells composing the blood-islands, and by degrees the
process is carried completely around the blood-island, so that
the peripheral layer becomes entirely separated from the central
mass and encloses it (See Fig, 68 C). The enclosing cells become
flattened during this process to form an endothelium; inasmuch
as the blood-islands are not separate, but anastomose to form a
network, the process results in the formation of a network of
endothelial tubes enclosing cell-masses. Thus arise the first
blood-vessels. The enclosed masses of cells rapidly acquire
hsemoglobin, become separated from one another, and form
blood-cells.

There is a great difference in the relative amounts of blood-
cells formed in different regions. Thus in the anterior part of
the opaque area and in the pellucid area the original blood-
islands are relatively small (Figs. 44 and 45), and furnish material
sufficient only for the formation of the blood-vessels. On the
other hand, in the peripheral part of the vascular area, especially
towards its posterior end, the largest masses of blood-cells are
found; and these conditions grade into one another. In other
words, the formation of blood-cells is restricted at this time to
the opaque area, and is most abundant posteriorly. In the
pellucid area only empty blood-vessels are formed. Similarly
the blood-vessels of the embryo itself are at first empty; they
become filled secondarily from the opaque area when circulation
begins.

The appearance of blood-vessels within the pellucid area

HEAD-FOLD TO TWELVE SOMITES 119

and the embryo has been interpreted in two principal ways:
(1) that they are an ingrowth from the original vascular primor-
dium of the opaque area; and (2) that they arise by differentia-
tion in situ. The first view was originally stated by His, and
has been supported by Eolliker and others. The second is sup-
ported by Riickert, P. Mayer and others. The observations,
on which the ingrowth theory of His were based, were made
originally on whole blastoderms of the chick, and concerned
primarily the order of origin of the blood-vessels, which is cen-
tripetal and continuous. But it is obvious that such observations
do not in themselves demonstrate the existence of an independent
ingrowing primordium; they are not altogether inconsistent with
the view that the blood-vessels differentiate from cells in situ.
Within the embryo itself parts of certain vessels appear in sections
to arise separately, and form secondary connections with the
vessels formed at an earlier time; this is the case for instance
with the dorsal aorta in the region of the head. But such appear-
ances seen in sections may be deceptive, as Evans has shown by
injections of the ingrowing vascular system of early chick embryos.
The entire system appears in such injections to be continuous
from the first and there was found no evidence of independently
formed parts.

Origin of the Heart. The embryonic heart possesses two
layers: an internal delicate endothelium, the endocardium, and
an external strong muscular layer, the myocardium. The endo-
cardium arises in continuity with the blood-vessels of the pellucid
area, and is in no wise different from them; the myocardium, on
the other hand, arises from the splanchnic mesoblast. The heart
is thus to be regarded as a portion of the embryonic vascular
system, specially provided with a muscular wall for the propul-
sion of the blood. The first incUcation of the heart is a thicken-
ing of the splanchnopleure of the amniocardiac vesicles, which
forms the primordium of the myocardium. This is situated a
short distance lateral to the hind-brain region of the embryo, and
makes its appearance between the stage of 3 and 5 somites.

The endocardium soon appears between the thickened ento-
derm and the myocardium, in the form of a delicate endothelial
vessel on each side, continuous with the extra-embryonic blood-
vessels. This is, indeed, the place where the blood-vessels first

120 THE DEVELOPMENT OF THE CHICK

reach the embryo. The myocardium then becomes arched
towards the body-cavity and includes the endocardium in its
concavity (Fig. 53). The heart thus comes to consist of two
parts on each side: a myocardial gutter semicircular in cross
section, open towards the entoderm, and an endothelial tube
lying in the gutter, and in contact with the entoderm. At this
time the lateral limiting sulci appear in the splanchnopleure
just central to the endocardium on each side, and, as the fore-
gut closes from in front backwards, the following changes take
place (Figs. 54 and 54 A): (1) the entoderm withdraws completely
from the fused apices of the lateral folds in the splanchnopleure,
and thus a wide separation is made between the floor of the pharynx
and the splanchnopleure below; (2) the right and left endocardial
tubes come into immediate contact in the floor of the pharynx;
(3) the two myocardial gutters coming together form a single
tube around the endocardium, suspended by a double mesoder-
mal membrane {mesocafdium or dorsal mesentery of the heart) to
the floor of the pharynx, and attached by a similar mesentery
{ventral mesentery of the heart) to the splanchnopleure beneath
(Fig. 54). The latter connection is ruptured almost as soon as
formed, so that the floor of the myocardium becomes complete
(Fig. 54 A). Soon after the completion of the floor of the phar-
ynx the two endocardial tubes press together until the common
wall becomes reduced to a vertical partition, which then ruptures;
and finally (10-12 s) all traces of the original duplicity of the
heart disappear (Figs. 60, 62, 64).

The heart thus arises from two lateral halves which fuse sec-
ondarily to form a single tube. This fusion takes place from
in front backwards, hence the anterior end of the heart is formed
first. Indeed, the full length of the cardiac tube is not formed
in the period covered by this chapter; the definitive hindermost
division is established by concrescence after the 12 s stage. But
the actual hind end is always continuous with the extra-embryonic
network of blood-vessels and this connection develops into the
main splanchnic veins.

As a rare abnormality the lateral primordia of the heart may meet
and fuse dorsal to the embryo, instead of in the floor of the pharynx.
This condition is known as omphalocephaly; in other rare cases the lateral
halves may fail to unite, and two hearts may be formed.

There are three views concerning the origin of the endocardium:

HEAD-FOLD TO TWELVE SOIMITES 121

(1) that it is an ingrowth of the extra-embryonic vessels, (2) that it arises
from the mesoblast in situ, (3) that it arises from the entoderm in situ.
Appearances such as that shown in Fig. 53 favor the last view.

The heart is then a double-wallecl tube attached to the floor
of the pharynx. The posterior end rests squarely against the an-
terior intestinal portal and is continuous with the rudiments of
the splanchnic veins running in the diverging folds of the portal;
the anterior end of the heart is continued as a simple endothelial
tube (ventral aorta) as far forward as the oral plate, where it is
divided in two (Figs. 62, 64, etc.).

This primitive simplicity of the cardiac tube continues through-
out the period considered in this chapter without substantial
alteration. The heart increases in length wdth considerable
rapidity, but being attached at its anterior and posterior ends by
the aortic and venous roots respectively, it is forced to bend,
nearly always to the right, so that a convexity of the heart
appears to the right of the embryonic head, at about the 11-12 s
stage (Figs. 63, 64). About this time the mesocardium
(dorsal mesentery of the heart) disappears except at the posterior
end, and the cardiac tube thus becomes free except at its two
ends.

The Embryonic Blood-vessels. The dorsal aorta arises from
the median edge of the vascular network, which extends across
the pellucid area in the splanchnopleure. At the stage of 7-9
somites, it has reached the nephrotomic level. The marginal
meshes gradually straighten themselves out into a longitudinal
vessel, continuous with the net-work at the sides and behind.
Onh^ the trunk part has been shown to arise in this manner. The
cephalic part may arise by a forward growth of the trunk part or
from mesenchyme in situ. A connection is formed around the
anterior end of the fore-gut with the ventral aortse (Fig. 55), and
an arterial pathway is thus established from the heart by way
of the ventral and dorsal aortae to the vascular network of the
splanchnopleure.

The arterial system consists at thirty-three hours (12 s stage)
of the following parts: (1) ventral aorta; (2) first visceral or
mandibular arteries connecting 1 and 3 ; (3) dorsal aortae ; (4) seg-
mental branches of the dorsal aortae. The ventral aorta is, as

122 THE DEVELOPMENT OF THE CHICK

we have seen, the anterior prolongation of the endocardium
extending between the extreme anterior end of the heart proper
and the oral plate. At the oral plate it divides into two branches,
right and left mandibular arteries or arches, that surround the
anterior end of the fore-gut, and arch over to be continued into
the two dorsal aortse. The tissue in which these arches run is
destined to form the mandibular arch or lower jaw. The two
dorsal aortse are very large vessels running above the roof of the
pharynx near its lateral angles. They give off no branches in
the head. In the trunk they pass backwards in the splanchno-
pleure beneath the somites (Fig. 68 B), and are connected at
intervals with the extra-embryonic blood-vessels. These con-
nections are more important in the region of the primitive streak
(Fig. 63) where the dorsal aortse disappear in the general extra-
embr3'onic network. Slight diverticula of the dorsal aortse
ascend in the interspaces between successive somites (segmental
arteries).

Concerning the veins in the period under consideration there
is nothing additional to be said.

V. Description of an Embryo with 10 Somites

It will now be in place to describe rather fully the anatomy
of the stage at which we have arrived; this will serve as a point
of departure for the next chapter.

The blastoderm is a circular membrane covering a consider-
able portion of the yolk (cf. Fig. 32 A). The embryo appears
to the naked eye as a whitish streak in the central pear-shaped
pellucid area. The surface views and the two views of the em-
bryo viewed as a transparent object show the topography of the
various parts of the embryo (Figs. 63-66).

A section across the entire blastoderm at the stage of 10 s,
through the sixth somite (Fig. 68), shows the following parts:

The ectoderm bounds the section above; it is thickened in the
angle between the neural tube and the somites, and becomes
thinner as it is traced peripherally; at the extreme periphery of
the blastoderm it merges into a mass of cells that interpenetrate
the yolk. Ventrally the boundary of the section is formed by
the entoderm which is slightly arched upwards in the middle line.

HEAD-FOLD TO TWELVE SO:\IITES

123

In the region of the area pellucida the entoderm is very thin; at
its boundary it passes rather abruptly into the large rounded vesi-
cular cells of the yolk-sac entoderm, which becomes continuous
at the margin of the vascular area with the germ-wall; the
latter continues to the periphery where it merges in the undifferen-
tiated cell-mass (zone of junction) (Figs. 68 A-68 E). The large
neural tube is not vet closed. Beneath the neural tube is a sec-
tion of the solid rod-like iiotochord.

Fig. 67. — Median longitudinal section of the head of an embryo of l.'i s.

Ectam., Ectamnion. F. B., Fore-brain. H. B., Hind-brain. Inf., In-
fundibulum. M. B., Mid-brain, pr'c. pi., Precardial plate. T. p., Tuber-
culum posterius. Other abbreviations as before.

The mesoderm (Fig. 68 A, B, C) lies between the parts already
named; it consists on each side of the middle line of the following
parts: (1) the mesohlastic somite, a block of cells that radiate
from a central cavity filled with irregularly disposed cells; (2) the
intermediate cell-mass or nephrotome, forming a narrow connect-
ing bridge between the somite and the lateral plate; (3) the
lateral 'plate, split into two layers, external, known as the somatic
layer, and internal or splanchnic layer. The cavity between the
two layers is the coelome or hody-cavity; it is very narrow next the
nephrotome, but widens as it extends laterally to the margin
of the vascular area, and is divided by various strands of cells
extending from somatic to splanchnic layers, thus indicating its
origin by fusion of coelomic vesicles.

The ectoderm plus the somatic layer constitute the somato-
pleure, from which the body-wall, amnion, and chorion are derived,
and the entoderm plus the splanchnic layer form the splanchno-

124 THE DEVELOPMENT OF THE CHICK .

pleure, from which arises the intestine and all its appendages,
including the allantois and the yolk-sac. Blood-vessels lie be-
tween the splanchnic mesoblast and the entoderm. The large
vessels beneath the somite and nephrotome are the dorsal aortce;
small vessels are present in the area pellucida, and there are
many large ones in the area vasculosa. The walls of the vessels
are constituted of a single layer of flat endothelial cells bulging
in the region of the nuclei; in the vascular area are true blood-
islands with eml:)ryonic blood-cells more or less fully filling the
cavity.

In a median sagittal section (Fig. 67) the following points
should be noticed: (1) the neural tube is enlarged in the region of
the head to form the brain, more fully described below; (2) the
entoderm forms a tube in the head known as the pharynx or
cephalic enteron (cephalic part of the fore-gut), opening behind
the heart into the space between the entoderm and yolk. The
floor of the anterior end of the fore-gut is fused to the ectoderm
in the middle line forming the oral plate. The entoderm forming
the floor of the fore-gut turns forward around the hind end of
the heart, and beneath the anterior part of the head forms part
of the proamnion or mesoderm-free region of the pellucid area;
(3) the large pericardial (parietal) cavity lies beneath the floor
of the fore-gut. Attached to the posterior wall of the pericar-
dium one sees the hind end of the heart with its two walls, the
endocardium and the myocardium a fold of the mesoblastic lin-
ing of the pericardium. Between the anterior end of the pericar-
dium and the oral plate is seen the endothelial ventral aorta; (4)
the notochord lies between the fore-gut and neural tube and ends
anteriorly in a mass of mesenchyme lying between the infundib-
ulum and fore-gut.

The Nervous System. The neural tube is closed at the 12 s

Fig. 68. — A. Transverse section across the axis of the embryo and the en-
tire blastoderm of one side. The section passes through the sixth somite
of a 10 s embryo, and is intended to show the topography of the blastoderm.
The regions B, C, D, E are represented under higher magnification in the
Figs. B, C, D, E.
a. V. e., Area vitellina externa, a. v. i.,Area vitellina interna. Bl. i., Blood
island. Bl. v., Blood vessel. Coel, Coelome. G. W., Germ-\yall. M. O.,
Margin of overgrowth. N'ph., Nephrotome. S., Somite. Som'pl. Soma-
topleure. Sprpl., Splanchnopleure. Som. Mes., Somatic layer of mesoblast.
spl. Mes., splanchnic layer of the mesoblast. S. T., Sinus terminalis. Y. S.
Ent., Yolk-sac entoderm. Z. J., Zone of junction.

>50/77/', <

L_-»

^>ip

BJ/

'■- fiiu?*

I)

^M.e.

126 THE DEVELOPMENT OF THE CHICK

stage (Figs. 63 and 65) to a point a little behind the last meso-
blastic somite; beyond this the medullary folds diverge and are
lost to view towards the hind end of the primitive streak. We
may distinguish a cephalic portion {brain or encephalon) and a
trunk portion (spinal cord or myelon) of the neural tube; the
boundary lies between the fourth and fifth somites, for the first
four somites enter into the composition of the head. The brain
is thus at this time about as long as the portion of the cord formed
or indicated by the medullary folds. For description, see p. 108.

Alimentary Canal. The alimentary canal and its appendages
exist only potentially in this embryo in the form of the splanchno-
pleure, except in the head. The cephalic enteron of this stage
corresponds to a large part of the pharynx. The oral plate has
already been described in connection with the sagittal section
(Fig. 67). In transverse section the extreme anterior end of the
fore-gut is quite narrow, elsewhere it is very wide laterally, and
in one place its lateral expansions come in contact with the
ectoderm on each side and fuse to it, thus indicating the hyoman-
dihular cleft. The floor and lateral walls of the pharynx are com-
posed of columnar cells, the roof of flattened squamous cells
(Fig. 54).

Vascular System. The heart lies in the parietal cavity be-
neath the pharynx; it is bent near its middle to the right. It is
an undivided double-walled tube, the internal wall or endocardium
being a continuation of the blood-vessels, and the external wall,
myocardium or muscular heart, being a duplication of the wall
of the pericardium. It has not yet reached the stage of regular
contraction, though it may be observed to twitch from time to
time. The chambers of the heart are indicated, but not clearly
defined at this time; one can only say that the posterior end is
the venous end from which the sinus and auricles are to form,
and the anterior two thirds, the arterial end, destined to form the
ventricles and bulbus.

The endocardium is continued anteriorly into the ventral
aorta, which divides on each side of the oral plate (Fig. 64), to
form the mandibular arches that describe a loop around the
anterior end of the fore-gut and are continued posteriorly as
the dorsal aortce, which run above the roof of the pharynx, lateral
to the notochord, into the trunk, where they lie ventral to the
nephrotome, and send off short blind branches (segmental arteries)

HEAD-FOLD TO TWELVE SOMITES 127

between the somites. Near the primitive streak they disappear
by merging in the vascular network of the blastoderm.

The posterior end of the endocardium divides in two branches
that pass out along the postero-lateral margins of the fore-gut
into the general vascular network of the blastoderm (Fig. 64j.
This connection constitutes the beginning of the vitelline veins
through which the blood from the yolk-sac enters the posterior
end of the heart.

General. The elongated form of the entire embryo and the
preponderance of the head are marked features of this stage.
The latter condition is largely due to the order of origin of parts:
the anterior parts preceding the more posterior in their appear-
ance. The head is really, therefore, in a more advanced stage
of development than the trunk, hence larger. The elongated
condition of the head and the arrangement of all its organs in
longitudinal sequence, however, are probably conditions of
phylogenetic significance, and point towards an ancestral con-
dition. The topographical values of the cUvisions of the em-
bryonic head are very different from those of the adult, to attain
which certain regions develop to a relatively enormous extent,
and others comparatively little.

A number of features in the anatomy of the 12 s stage are
purposely omitted from this description, as they represent the
primordia of structures described more fully beyond; such, for
instance, are the neural crest, the pronephros, etc.

Zones of the Blastoderm. The following zones may be recog-
nized in the blastoderm : (1) the pellucid area surrounding the
embryo; (2) the vascular zone of the opaque area; (3) area vitel-
lina interna; (4) area vitellina externa. The pellucid area is
readily defined by its transparency and by the existence of the sub-
germinal cavity beneath it. The vascular zone is most readily
defined by the extension of the blood tissue which has a very
definite margin, coincident with the extension of the mesoblast.
The area vitellina includes all of the blastoderm peripheral to the
vascular area, and it is characterized by the presence of two
layers only, ectoderm and entoderm (germ-wall). It is again
divided into two concentric zones, internal and external. The
internal is much the wider (Fig. 32 A), and is characterized by
the existence of a perilecithal space, i.e., a slight fluid-filled
cavity between the entoderm and yolk continuing the subgerminal

128 THE DEVELOPMENT OF THE CHICK

cavity peripherally. The external vitelline area is relatively
narrow, and consists (1) of the zone of junction adjoining the
internal vitelline area, and (2) a free margin separate from the
3^olk (margin of overgrowth). The zone of junction is the per-
sistent embryonic or formative part of the blastoderm from
which the extra-embryonic ectoderm and entoderm arises. Thus
as it spreads peripherally over the surface of the yolk, it leaves
on its central margin the differentiated extra-embryonic ecto-
derm and entoderm; in other words, the zone of junction is the
youngest part of the blastoderm, and the concentric zones that
may be drawn within it represent successively older stages in a
centripetal direction. Therefore in a transverse section through
the entire blastoderm successive stages of differentiation of the
ectoderm and particularly of the entoderm are met as one passes
from the zone of junction towards the center.

The free margin arises from the zone of junction in the manner
already described in Chapter II. It may be considered as a part
of the ectoderm and it terminates in a row of enlarged cells that
often exhibit amoeboid prominences on their margins. It would
appear that these cells have the function of a marginal wedge
that separates the vitelline membrane and yolk.

The germ-wall has been the subject of many extended re-
searches, but a definitive solution of its origin and function has
not hitherto been obtained, mainly on account of the incomplete
knowledge of its early histor}^ The ground here taken is in some
respects different from that of the various authors, but it is based
on a study of its early history given in ChajDter II. There is no
deviation from the mode of formation of the zone of junction in
the stage under consideration from what was found in earlier
stages, and there is no reason to believe that its subsequent history
varies in any important respect. It appears to be produced by
continuous proliferation of the cells in the 3'olk as in earlier stages
(see Fig. 68 E). These cells actively engulf the large yolk gran-
ules, and the histological structure becomes in consequence diffi-
cult of analysis. The cells lose their individuality and constitute
an extended syncytium, the protoplasm of which is packed with
yolk-granules. In removing the blastoderm from the egg in salt-
solution one finds always, after removing the yolk that may be
washed off, a narrow submarginal zone of adherent yolk that is
not readily removed, and this is the site of the zone of junction.

HEAD-FOLD TO TWELVE SOMITES 129

Centrally to the zone of junction we have the differentiated
ectoderm and germ-wall sharply separated from the yolk by the
perilecithal space. The ectoderm of the inner zone of the vitelline
area requires no extended notice ; it consists at this time of a sin-
gle layer of flattened cells. The germ-wall next to the zone of
junction consists of two or three layers of large, more or less
rounded, cells with definite boundaries, each of which contains
one or more yolk-spheres and smaller yolk-granules (Fig. 68 E).
We may say roughly that whereas in the zone of junction we
have cells in the yolk, in the vitelline area we have yolk in the
cells. This mav indicate sufficientlv the wav in which a several
layered epithelium becomes differentiated from the zone of junc-
tion. As this epithelium is traced centrally we find usually a
short distance from the zone of junction a thinner area (Fig.
68 D), and beyond this again the several layers of cells even
more laden with yolk-spheres and granules than previously; so
that it would appear that these cells may actively engulf yolk-
granules. At the margin of the vascular area the entoderm be-
comes one-layered, and is composed of columnar cells with swollen
free margins turned towards the yolk and still containing some
yolk-granules and spheres (Fig. 68 C). At the margin of the
pellucid area there is a rather sudden transition to the flat ento-
dermal epithelium characteristic of this area.

CHAPTER VI

FROM TWELVE TO THIRTY-SIX SOMITES. THIRTY-
FOUR TO SEVENTY-TWO HOURS

I. Development of the External Form, and Turning of

THE Embryo

In the embryo of twelve somites only the head is distinctly
separated from the blastoderm; and there is no sharp boundary
between the embryonic and extra-embryonic portions of the
blastoderm in the region of the trunk; but this changes very
rapidly. The progress of the developmental processes, that have
marked out an embr^^onic axis in the blastoderm, produces in
the course of about eighteen hours a sharp distinction everywhere
between embryo and extra-embryonic blastoderm. The latter,
together with an outgrowth of the embryonic hind-gut (allantois),
then constitute the so-called embryonic membranes, which become
very complicated, and which provide for the protection, respira-
tion, and nutrition of the embrvo. We shall consider the forma-
tion of the embryonic membranes separately in order not to
confuse the account of the development of the external form of
the embrvo.

In considering the development of the external form of the
embryo, we must distinguish between those processes that sepa-
rate it from the extra-embryonic blastoderm, and those that occur
within its own substance leading to various characteristic bend-
ings and flexures; we may consider them separately, although
they are going on at the same time.

Separation of the Embryo from the Blastoderm. The separa-
tion of the embryo from the blastoderm takes place by the
formation of certain folds or sulci that may be named: (1) the
head-fold or anterior limiting sulcus; (2) the lateral limiting sulci,
appearing as prolongations of the head-fold along the sides of the
embryonic axis; and (3) the tail-fold or posterior limiting sulcus.

The head-fold has been described in detail in the preceding

130

FROM TWELVE TO THIRTY-SIX SOMITES

131

chapter. The lateral limiting sulci are a continuation of the
lateral limbs of the head-fold; they owe their origin to the folding
of the splanchnopleure and somatopleure adjacent to the embryo
towards the yolk, at the line of junction of embryonic and extra-
embryonic parts. The tail-fold arises about the stage of 26 to
27 somites (Fig. 93), and is similar to the head-fold, except that
it is turned in the opposite direction. The sulci combine to form
a continuous ring around the embryo and gradually pinch it off,
so to speak, from the extra-embryonic blastoderm.

In the splanchnopleure the lateral limiting sulci (Fig. 69)

L:^:iam

^C/ior.

fcfam.

Spl'jO/.

- Transverse section through the fifth somite of the 23 s stage.

Amnion. Ao., Aorta, a. i. p., Anterior intestinal portal. Coel.,

Ectamnion. E. E. B. C, Extra-cmhry-
1. 1. s., Lateral limiting sulcus. My.,

Fig. 69.

Amn
Coelome. Chor., Chorion. Ectam.,
onic body-cavity. Int., Intestine.

Myotome, s. a., Segmental artery. So'pl., Somatopleure. Spl'pl., vSplanch
noplcure. s., Somite, s. 5, Fifth somite. V. O. M. R. and L., Right and left
omphalo-mesenteric veins. V. V., Vitelline vein.

come together and fuse both in a caudal direction from the fore-
gut, and subsequently in a cephalic direction from the hind-gut (see
below), so as to convert the splanchnic gutter into a tube (the ali-
mentary canal). There is thus a ventral suture along the ali-
mentary canal in which the entoderm of the alimentary canal
becomes separated from the extra-embryonic entoderm, leaving
a double layer of the splanchnic mesoblast (ventral mesentery)
connecting the alimentary canal with the extra-embryonic splanch-
nopleure; but this disappears everywhere as soon as formed,
except in the region of the posterior part of the heart and the
liver, where it forms the dorsal mesocardium and gastro-hepatic
ligament (Fig. 118), and in the region of the neck of the allantois.

132

THE DEVELOPMENT OF THE CHICK

The fore-gut is thus being continually lengthened backwards
by fusion of the lateral limbs of the splanchnopleure. At the
31 s stage this has proceeded about to the fourteenth somite.
At about the 21 s stage the tail-fold appears in the splanchno-
pleure, thus establishing the hind-gut (Fig. 70) which gradually

f.f.So-pl.

So'p/.

5p-pl.

j?iQ_ 70. — Median longitudinal section through the hind end of an embryo

of about 21 s.
an. pi., Anal plate, an. t., Anal tube. p. i. p., Posterior intestinal portal.
T. B., Tail-bud. t. f. So'pL, Tail fold in the Somatopleure. t. f. Sp'pl., Tail
fold in the splanchnopleure. Other abbreviations as before.

elongates forwards. There remains then an open portion of the
alimentary tract, where its walls are continuous with the extra-
embryonic splanchnopleure or yolk-sac. This is known as the
yolk-stalk. The entrance from the yolk-sac into the fore-gut
is known as the anterior intestinal portal, and that from the
yolk-sac into the hind-gut as the posterior intestinal portal (Fig.
70). At the 27 s stage the yolk-stalk is long and narrow (Fig.
106); the stems of the splanchnic (omphalo-mesenteric) veins run
to the heart in its anterior portion, and the omphalo-mesenteric
arteries pass out about its center. As it gradually closes, the
stems of the omphalo-mesenteric arteries and veins are brought
closer together. At about five daj's it becomes a tubular, thick-
walled stalk, connecting intestine and yolk-sac, and so remains
throughout embryonic life.

The limiting sulci in the somatopleure lead to the formation
of the body-wall. In the trunk the somatopleure is separated
from the splanchnopleure by the coelome (Fig. 69), and the folds
in the somatopleure take the same general direction as those in
the splanchnopleure; they thus lead to the formation of a tube
(body-wall) outside of a tube (alimentary canal), the intervening

FROM TWELVE TO THIRTY-SIX SOMITES 133

cavity being the body-cavity. The unclosed part of the body-
wall is continuous with the extra-embryonic somatopleure, more
specifically the amnion (see below), and this connection is known
as the somatic stalk or umbilicus. The yolk-stalk and neck of the
allantois pass out of the body-cavity through the somatic stalk,
which therefore remains open until near the end of incubation.

The Turning of the Embryo and the Embryonic Flexures.
We have described the separation of the embryo from the extra-
embryonic blastoderm without reference to its turning from a
prone to a lateral position or to the formation of the flexures
of the entire head and body that are so characteristic of amniote
embryos generally. These changes begin about the 14 s stage
and are first indicated by a slight transverse bending of the origi-
nally straight axis of the head in the region of the mid-brain
(Fig. 67). By means of this bending, known as the cranial flex-
ure, the fore-brain is directed toward the yolk; but almost simul-
taneously another tendency manifests itself, viz., rotation of the
head on its side, at first affecting only the extreme end. (See
Figs. 71, 73, 99, etc.) By the 27 s stage these two processes
have resulted in the conditions shown in Fig. 105: by the cranial
flexure the fore-brain is bent at right angles to the axis of the
embryo, and owing to the rotation the head of the eml^ryo lies
on its left side. But inasmuch as the trunk is still prone on the
surface of the volk the axis of the embrvo is twisted in the inter-
mediate region. This twist is transferred farther and farther
backwards as the turning of the head gradually involves the
trunk, until finally, at about ninety-six hours, the embryo lies
entirely on its left side.

Exceptionally the rotation may be in the inverse direction
(heterotaxia) ; in such cases it is often associated with situs in-
versus viscerum. Heterotaxia has been produced experimentally
(Fol and Warynsky).

After the appearance of the cranial flexure a second trans-
verse flexure appears in the embryo, this time at about the
junction of head and trunk, hence known as the cervical flexure
(Figs. 73, 99, etc.). This flexure gradually increases in extent
until the head forms a right, or even smaller, angle with the
trunk; thus the fore-brain is turned to such an extent that its
anterior end points backwards and its ventral surface is opposed
to the ventral surface of the throat (Fig. 117).

134

THE DEVELOPMENT OF THE CHICK

H.EAm,

S.16.

Pr.atr:

Fig. 71. — Entire embryo of 16 s, drawn
from above as a transparent object. Note
the cranial flexure; the rotation of the
head on its left side is beginning,
au. P., Auditory pit. F. B., Fore-brain.
H. B. 1, First division of the hind brain.
H. F. Am., Head-fold of the amnion. Hm. F.,
Hyomandibular furrow. Pr'am., Proam-
nion. M. B., Mid-brain, op. Yes., Optic
vesicle, pr. str., Primitive streak, s 2, s 4,
s 16, Second, fourth, and sixteenth somites.
V. o. m., omphalo-mesenteric vein. ^TI-V^I,
The acustico-facialis primordium. IX-X,
Primordium of the glossopharyngeus and
vagus.

The entire trunk tends also to bend ventrally, i.e., to develop
a dorsal convexity, and this approximates its posterior end to the
tip of the head. These flexures are characteristic of amniote

FROM TWELVE TO THIRTY-SIX SOMITES

135

vertebrate embryos; the cause appears to lie in the precocious
development of the central nervous system, of which more here-
after. Only the cranial flexure remains as a permanent con-
dition.

II. Origin of the Embryonic Mp:mbranes

The period from about 12 to 36 somites also includes the early
history of the embr3^onic membranes, amnion, chorion, yolk-sac
and allantois. The first three arise from the extra-embryonic
blastoderm, and the allantois arises as an outgrowth of the ven-
tral wall of the hind-gut.

3^i.jt?.

Fig. 72. — The head of the same embryo from

below.

a. i. p., Anterior intestinal portal. B. a.,
Bulbils arteriosus. Inf., Infundibuliim. or. pi.,
Oral plate. Tr. a., Truncus arteriosus.
Ven., Ventricle, v. Ao., Ventral aorta.

Origin of the Amnion and Chorion. The amnion is a thin
membranous sac, forming a complete investment for the embryo
and continuous with the body-wall at the umbilicus; it lies beneath
the chorion to which it remains attached throughout incubation
by a plate of tissue (sero-amniotic connection), and it arises in
common with the chorion from the extra-embryonic somatopleure.
The entire somatopleure external to the embryo is used up in
the formation of these two membranes. The amnion arises from
a portion immediately adjoining the embryo itself; the remainder
of the somatopleure peripheral to the amniogenous part forms
the chorion. Thus the extra-embryonic somatopleure may be
divided into two zones; an amniogenous zone immediately adja-

136

THE DEVELOPMENT OF THE CHICK

Cr.Fl.

Mete/2C.
Myelenc./.

QU.P.

Alye/enc.2

3.Z

S.5.

^.lO.

-Mm

prstr '

Fig. 73. — Entire embryo of 20 s, viewed
as a transparent object from above.
The cranial flexure and the rotation of
the head of the embryo have made
considerable progress.
A. o. m., Omphalo-mesenteric artery.
Or. Fl., Cranial flexure. D. C, Duct of
Cuvier. Dienc, Diencephalon. Mesenc,
Mesencephalon. Metenc, Metencepha-
lon. Myelenc. 1, and 2, Anterior and
posterior divisions of the myelcncepha-
lon. Telenc, Telencephalon. Vel. tr.,
Velum transversum. Other abbrevia-
tions as before, x 30.

cent to and surrounding the embryo, and a choriogenous zone,
comprising the remainder.

The method of formation of amnion and chorion is as follows:

FROM TWELVE TO THIRTY-SIX SOMITES

1 o'-

(a diagrammatic outline is first given and a detailed descrij^tion
follows). The somatopleure becomes elevated in the form of
a fold surrounding the embryo; this fold begins first in front of
the head of the embryo as the head-fold of the amnion^ whicli

ofi. Ves.
Mesenc

Fig. 74. — Head of the same embryo
from the ventral side. Abbreviations
as before.

^/>^/77.

€^

Td

Rec.opt

Fig. 75. — Median sagittal section of the head of an embryo of 18 s.

H. F. Am., Head-fold of the amnion. Ph., Pharynx. Isth., Region of
the isthmus, pr'o. g., Preoral gut. or. pi., Oral plate. Ree. opt., Recessus
opticus. S. v., Sinus venosus. Other abbreviations as before.

immediately turns backwards over the head, forming a complete
cap (Figs. 67, 71, 75, etc.); the side limbs of the head-fold are
then elongated backwards, and are here known as the lateral
folds of the amnion; these rise up and arch over the embryo

138 THE DEVELOPMENT OF THE CHICK

(Figs. 109 and 110). In each fold one can distinguish an amniotic
or internal limb, and a chorionic or external limb meeting at or
near the angle of the folds, the line of junction being marked
by an ectodermal thickening, the ectamnion. Fusion of the
right and left lateral folds begins at the head-fold, and progresses
backwards in such a way that the right and left amniotic limbs
become continuous with one another, similarly the right and
left chorionic limbs; and, when fusion is complete, the amnion
and chorion become separate continuous membranes. In this
way the amnion extends, by the 27 s stage, back to the seventeenth
somite (Fig. 105). At this time a new fold arises behind the
rudimentary tail-bud and covers the tail precisely as the head-
fold covers the head (Fig. 105) ; the tail-fold of the amnion then
apparently is prolonged forward a short distance and soon meets
the anterior lateral folds, forming a continuous lateral fold. Fu-
sion continues until, about the 31 s stage, the opening into the am-
niotic cavity is reduced to a small elliptical aperture lying above
the buds of the hind-limbs (Fig. 99). This then rapidly closes,
but a connection, sero-amniotic connection, remains at the place
of final closure. Elsew^here the separation of chorion and amnion
is complete.

The formation of the amnion is an extremely interesting
process from the standpoint of developmental mechanics, and
involves a number of details that are best understood after such
a general review of the process as has been given in the preceding
paragraphs. Returning then to the 12 s stage for consideration
of these details, we must first note that the extension of the meso-
blast prior to this period has left an area situated in front of
the head free from mesoblast (Figs. 65, 67, 71, 75, etc.). This
area, in which the ectoderm and entoderm are in contact, is
known as the proamnion. The formation of the amnion begins
within this area by a thickening in the ectoderm (ectamnion)
near the anterior boundary of the proamnion at a stage with
about eight or nine somites. The thickening, which is very
narrow, extends right and left, and turns backwards along the
sides of the head to about the region of the middle of the heart,
gradually becoming more peripheral in position and fading out
(Fig. 76). It represents the junction of the amniogenous and
choriogenous somatopleure and thus corresponds to the angle
of the future amniotic folds. The head of the embryo lies in a

FROM TWELVE TO THIRTY-SIX SOMITES

139

e.a.

e,a.

depression bounded in front by the ectamnion, and on the sides
by the amnio-cardiac vesicles of the body-cavity (Fig. 65). The
floor of the depression is the proamnion. Just before the for-
mation of the head-fold proper, the ectamnion in front of the
head becomes irregularly thickened to
such an extent as sometimes to present
an actually villous surface (Fig. 77; cf.
Fig. 67).

The head-fold of the amnion begins
to form at about the same time as the
cephalic flexure. The great expansion
of the body-cavity on each side of the
head (amnio-cardiac vesicles) causes an
elevation of the anterior angle of the
ectamnion, and a pocket is formed by
fusion of its lateral limbs. This slips
over the head of the embryo with aid
of the ventral flexure of the head just
developing. Inasmuch as the anterior
angle of the ectamnion is in the pro-
amnion, where there is no mesoderm,
and where the ectoderm is in immediate
contact with the entoderm, the ento-
derm as well as the ectoderm of the pro-
amnion is drawn into the head-fold, so
that the latter is not at first a fold of
the somatopleure. But in the chick the

proamniotic part of the head-fold is

, 1 , , A. Region of the soma-

never very extensive and does not at any topleure destined to form

time extend back of the beginning of the body-wall.

^1 .... ,, . . . B. Amniosrenous soma-

the mid-bram. Moreover, it is soon in- topleure.

vaded (Fig. 75) bv the bodv-cavitv, and ^- Choriogenous soma-

then the entoderm is withdrawn and

becomes part of the general splanchnopleure. The proamnion

ventral to the head is not invaded by mesoderm until a much

later period.

The ectodermal thickening marking the junction of amniotic

and chorionic somatopleure extends backwards very rapidly and

always precedes the origin of folds in any region. The lateral

folds themselves appear to owe their origin to the progressive

Fig. 76. — Entire embryo
of 13 s, to shoAV the rela-
tions of the ectamnion.

a. c, Inner margin of
amnio-cardiac vesicles,
e. a., Ectamnion.

140 THE DEVELOPMENT OF THE CHICK

fusion of the ectodermal thickenings of the opposite sides,
beginning at the posterior angle of the head-fold and proceeding
backwards. The energy of fusion is sufficient in itself to lift the
somatopleure up in the form of a fold around the body of the
embryo. Thus new parts of the ectodermal thickening are con-
stantly being brought together and the fusion progresses steadily,
and this in its turn prolongs the lateral amniotic folds. These
possess no independent power of elevation of any considerable
amount, for, when the initial fold of one side is destroyed by
cauterization, the fold of the opposite side remains as an insig-
nificant elevation in the somatopleure a long distance lateral to
the embryo.

Fig. 77. ■ — Transverse section through the anterior angle of

the eetamnion a few sections in front of the tip of the head.

Stage of 14-15 s.

b. c Extra-embryonic body-cavity, c, Cavity in the
entoderm, e. a., Eetamnion.

The tail-fold arises in an analogous manner to the head-fold,
except that there is no proamnion here. The progress of the
various folds and their final fusion follows from what has already
been said.

Practically all of the somatopleure of the pellucid area is
amniogenous with the exception, naturally, of that part internal
to the limiting sulci that forms the body-wall. What effect has
the turning of the embryo on its left side on the amniogenous
somatopleure? We will suppose that the latter is primitivelv
of equal width on both sides and that the notochord represents
approximately the axis of rotation. During the process of rota-
tion, the embr3'0 sinks and the lateral limiting sulci become deeper.
A direct consequence of the rotation must be, therefore, a strong
tension on the somatopleure belonging to the under (left) side,
a-h, and practically none on the upper (right) side, c-d. (See
Fig. 78 A, B).

FROM TWELVE TO THIRTY-SIX SOMITES

141

Even though the difference may be partly compensated by
drawing of the embryo to the left, the tendency would be to
stretch a-h. If there were no such compensation and a and b
were practically fixed points, the length of a-b at the conclusion
of the rotation would much exceed that of c-d (Fig. 78 B), and

J^

a

C

Fig 78. A, 5, and C. Diagrams to represent the effect of
rotation of the embryo on the amniogenous somatopleure.
a represents in all figures the position of the ectamnion on
the left (lower) side; d represents in all figures the position
of the ectamnion on the right (upper) side, h and c repre-
sent the junction of amnion and body-wall on left and right
sides respectively. In Fig. A, a-b and c-d are equal. In
Fig. B, rotation of the embryo is assumed to have taken
place without formation of the amnion; the distance a-b has
become greater than c-d. In Fig. C is represented rotation
of the embryo with synchronous formation of the amniotic
folds, as is actually the case; c-d is inevitably thrown into
secondary folds. The vertical lines at the extreme right
and left represent the margins of the pellucid area.

if, during this process, there were actual independent growth
of a-b and c-d, the latter would of necessity be thrown into folds,
but not the former. Finally, if the amniotic folds were forming
at the same time (as is actually the case), the right one would

142

THE DEVELOPMENT OF THE CHICK

inevitably be thrown into secondary folds by the approximation
of points c and d (Fig. 78 C).

Study of the fusion of the amniotic folds in actual sections
shows, that the line of fusion of the opposite amniotic limbs is
over the dorsal surface of the embryo only so long as the latter
lies flat on the yolk; it does not follow the turning of the embryo
on to its left side, and the consequence is that, after rotation of
the embryo, the line of fusion lies over the upper (right) side of
the embryo, often opposite the horizontal level of the intestine
(Fig. 79). Thus one fold of the amnion passes all the way from
the under side over the back of the embryo and around on the
other side to the line of fusion, and thus is several times as long
as the opposite limb. Moreover, the amniotic fold of the right

Fig. 79. — Section of an embryo of about 60 hours to show the sec-
ondary fold (s. f .) of the amnion on the right side.
e. a., Ectamnion. s. f., Secondary fold. 1., Left. r.

Right.

side is invariably thicker than that of the left side, and is always
thrown into secondary folds at the place of turning (Fig. 79).
These conditions are satisfactorily explained, as noted above, by
the mere turning of the embryo on its side.

One must therefore distinguish in the upper limb of the am-
nion two kinds of folds: (1) The ordinary amniotic fold induced
by the fusion of the right and left folds, and (2) secondary folds
formed simply by the process of twisting of the embryo.

These secondary folds of the amnion are very transitory,
except in two regions: (1) Above the hind end of the heart (apex
of ventricle), and continuing a short distance behind it; (2) in
the region immediately in front of the allantois, at sixty to seventy
hours, thus in the neighborhood of the final closure of the amniotic

FRO:\r TWELVE TO THIRTY-SIX SOMITES 143

folds. The former are of very constant occurrence and persist
a long time (Fig. 93).

Elsewhere the effect of the twisting of the embryo is rapidly
compensated so that the secondary folds of the right half of the
amnion do not persist long.

The subsequent history of the amnion and chorion is given
in another place. It should be noted here that the chorion, at
the stage of seventy-two hours, is continuous peripherally with
the splanchnopleure at the margin of the vascular area, and that
it ])ecomes separate from it only as the body-cavity extends
more and more peripherally. The sero-amniotic connection
remains throughout the entire embryonic period and modifies in
an important fashion the subsequent history of the membranes.

The yolk-sac is the name given to the extra-embryonic
splanchnopleure, because in the course of expansion of the blasto-
derm and extension of the extra-embryonic body-cavity over the
surface of the yolk, it finally becomes a separate sac enclosing
the yolk. It remains connected by the yolk-stalk with the intes-
tine until finally, some time after hatching, it is absorbed com-
pletely. The yolk is absorbed by the entodermal lining and is
carried to the embryo in solution by means of the vitelline veins.

Origin of the AUantois. The allantois arises as a diverticulum
of the hind-gut soon after the formation of the latter by the tail-
fold. It is not indicated before the formation of the tail-fold as
stated by some authors, but the tube identified by them as the
primordium of the allantois at this early stage is really the in-
testinal diverticulum leading to the anal plate (Fig. 70). At the
stage of twenty-eight somites the allantois is indicated by the
depth of the hind-gut, the ventral portion of which in front of
the anal plate soon becomes constricted from the upper portion,
and forms the primordium of the allantois. In longitudinal sec-
tions of an embryo of about thirty-five somites it can be seen to
include nearly the entire floor of the hind-gut between the anal
plate and the posterior intestinal portal (Fig. 80). It is lined
with entoderm and has a thick mesodermal floor in which numer-
ous small blood-vessels are already present. A transverse section
(Fig. 81) shows that the thick mesodermal wall is broadly fused
with the somatopleure in the region of the neck. In other
words, the allantois is developed within the ventral mesentery.
It will also be seen by comparing these figures that the amnion

144

THE DEVELOPMENT OF THE CHICK

arises from the neck of the allantois both behind and also at the
sides, (cf. Fig. 82.)

During the fourth day the distal portion of the allantois
pushes out into the portion of the extra-embryonic body-cavity
beneath the hind end of the embryo and rapidly expands to form
a relatively large sac. But the neck of the allantois remains
embedded in the ventral mesentery and does not expand; the
terminal portion of the intestine has in the meantime formed

Amcav. Ect.

-■Spl'pl.

Afesam.

Fig. 80. — Sagittal section through the tail of an embryo of about 35 s.

All., Allantois. An. pi., Anal plate, c. C, Central canal of the neural
tube. CL, Cloaca. Ectam., Ectoderm of the amnion. Mesam., Mesoderm
of the amnion, p'a. G., Post-anal gut. p. i. p., Posterior intestinal portal.
s. A., Segmental arteries. Other abbreviations as before.

the primordium of the cloaca, from which, therefore, the neck of
the allantois appears to arise (Fig. 183) ; at all stages of incuba-
tion the neck of the allantois forms an open connection between
the cloaca and the allantoic sac.

The Umbilicus. The closure of the bod^^-wall progressivel}^
reduces the communication between the embryonic and extra-
embryonic body-cavity to a narrow chink between the yolk-stalk

FROM TWELVE TO THIRTY-SIX SOMITES

145

and allantoic stalk on the one hand and the attachment of the
amnion on the other. The mnbilical cord thus consists of an
outer tube (somatic stalk) continuous with the body-wall, enclosing
the yolk-stalk and the stalk of the allantois, together with the
arteries and veins of yolk-sac and allantois. It is important to
bear in mind that in the region of the neck of the allantois the
amnion is attached to the latter at the sides and behind; only
the anterior wall of the allantoic stalk is free (Fig. 82). In other
words, the somatic umbilical stalk is fused with the lateral and
caudal wall of the neck of the allantois, a relation that is common
to all amniota.

Fig. 81. — Transverse section through the hind-gut and allantois of an em-
bryo of 35 s; the section passes through the thirtieth somite. Details
diagrammatic.
All, Allantois. H. G., Hind-gut. L. B., Leg bud. v. M., Ventral

mesentery. W. I)., Wolffian duct. Other abbreviations as before.

Summary of Later History of the Embryonic Membranes.

The full history of the embryonic membranes will be given later
(Chap. VII), but it seems desirable to give an outline here in order
to avoid repeated recurrence to this subject. The extension of
the body-cavity in the blastoderm is at first very rapid, but about
the fifth day it becomes slow, and the yolk-sac is never com-
pletely separated from the chorion. The allantois extends out
into the extra-embryonic body-cavity as a small pear-shaped
vesicle by the end of the fourth day. It then enlarges very
rapidly and extends in the form of a flattened sac over and around
the embryo immediately beneath the chorion with which it forms

146

THE DEVELOPMENT OF THE CHICK

an inseparable union. As the extra-embryonic body-cavity
extends, the allantois continues its expansion between the chorion
and the yolk-sac, and finally wraps itself together with a duplica-
tion of the chorion, completely around the albumen of the egg,
which has become very viscid, and aggregated in a lump opposite
to the embryo. The allantois is very vascular from the start,
and serves as an embryonic organ of respiration. It also receives
the excretion of the embrvonic kidneys and absorbs the albumen.

I. Br -

Ao.m.

Am.

Fig. 82. — Model of the caudal end of a four-day chick
to show the relations of the amnion to the allantois
and umbilicus. (After Ravn.)

All., Neck of the Allantois. Am., cut surface of

the amnion. A. o. m., Omphalo-mesenteric artery.

an. pi., Anal plate. L. B., cut surface of leg bud.

T., Tail.

The yolk-sac becomes much shriveled during incubation owing
to absorption of its contents, and on the last day of incubation
is withdrawn into the body-cavity through the umbilicus, which
finally closes. The chorion, amnion, and allantois shrivel up
when the chick begins to breathe air, and are cast off with the
shell at hatching.

FROM TWELVE TO THIRTY-SIX SOMITES 147

III. The Nervous System

The Brain. The description of the nervous system in the pre-
ceding chapter forms our starting-point. During the period now
under consideration the foundation of the main parts of the adult
brain are laid down, and its five chief divisions become sharply
characterized. It is important to correlate these with the earliest
morphological characters (original anterior end of medullary
plate, neuromeres, etc.) in order to trace these fundamental
landmarks through to definitive structures.

As we have already seen, the primary fore-brain includes the
first three neuromeres, the mid-brain the fourth and fifth, and
the hind-brain the sixth to the eleventh, as well as the region
opposite to the first four mesoblastic somites. It is clear that a
second point of fundamental morphological significance is the
original anterior end of the medullary plate which would naturally
form the center for a description of the anterior part of the neural
axis, if recognizable throughout the development. This point
may be recognized for a considerable period after the closure of
the anterior part of the neural tube, as the ventral end of the
-anterior cerebral fissure (Fig. 62), opposite the center of the
primary optic vesicles, thus in the region of the recessus opticus
(Figs. 87 and 88), which is to be regarded as marking the original
anterior end of the neural axis. Even after closure of the anterior
cerebral fissure a connection remains at its dorsal end between
the ectoderm and the neural tube. To this we may apply the
name neuropore, though no actual opening is found here at this
time. The median stretch of tissue between the recessus opticus
and the neuropore constitutes the lamina terminalis which remains
as the permanent anterior wall of the neural tube. It must not
be forgotten that the original anterior end of the medullary plate
lies at the ventral end of the lamina terminalis, i.e., in the re-
cessus opticus. A third landmark of fundamental morphogenic
significance is the infundibulum, which coincides in position, as
we have seen, with the anterior end of the notochord. Thus we
may distinguish prechordal and suprachordal portions of the neu-
ral axis (cf. Fig. 67).

Dorsal and Ventral Zones in the Wall of the Brain. The con-
ception of His, that the walls of the neural tube may be consid-
ered as formed of four longitudinal strips, viz., floor, roof, and

148

THE DEVELOPMENT OF THE CHICK

Fig. 83. — Five stages in the history of the neuromeres of the brain of the
chick. (After Hill.) All figures drawn from preparations of the embryonic
brain dissected out of the embryo.

A. Neural groove in an embryo with 4 somites. Right profile view, x 44.

B. Brain of a 7 s embryo, 26 hours old. Dorsal view; the three anterior
neuromeres are practically obhterated. x 44.

C. Brain of 14 s embryo. Dorsal view, x 44. The neuromeres have
now disappeared in the mid-brain rearion.

D. Right side of the brain of a chick embryo. 47 hours old. x 44.

E. Right side of the brain of an embryo, 80 hours old. x 17.

1-11, Neuromeres 1 to 11. IH, V, VII, interneuromeric grooves. A'f.,
Root of acustico-facialis (seventh and eighth cranial nerves), au. vs.. Audi-
tory pit. ep., Epiphysis, r., Groove between the tel- and diencephalon.
s., Groove between the par- and synencephalon. Tr., Root of trigeminus.

FROM TWELVE TO THIRTY-SIX SOMITES 149

two lateral walls, is a useful one. Each lateral wall may also
be divided into a dorsal and ventral zone, the former of which
is related to the sensory nerve roots and the latter to the motor.

Cerebral Flexures. The cerebral flexures correspond to the
cranial and cervical flexures of the entire head already described.
Their form and rate of progress may be more readily learned
from the figures (Figs. 67, 73, 83, etc.) than from any verbal
description. Only the cranial flexure is permanent, and the angle
thus formed ventrally in the floor of the mid-brain is known as
the plica encephali ventralis. A third flexure is formed later in
the anterior portion of the hind-brain, by a ventral bending of
the floor which is barely indicated in the period now under de-
scription, but becomes much more pronounced later; this is known
as the pontine flexure.

We may now take up separately the changes in each of the
primary cerebral vesicles.

The Prosencephalon. The principal events in the early de-
velopment of the prosencephalon are: (a) the separation of the
optic vesicles; (h) the delimitation of the tel- and diencephalon;
(c) special differentiation of the walls.

(a) A section across the optic vesicles of the 12 s chick shows
the prosencephalon as a central division with its cavity widely
confluent with the cavities of the optic vesicles. This wide com-
munication is rapidly narrowed by a ventrally directed fold of the
roof at the line of junction of the optic vesicles and prosencephalon
proper (Fig. 84); the fold also involves to a certain extent the
anterior and posterior line of junction. In the 20 s embryo the
connection of the optic vesicles and prosencephalon has been re-
duced in this way to about one third of its original diameter
(from actual measurements), forming a narrow tubular stalk, the
optic stalk, attached to the ventral portion of the fore-brain
(Figs. 73 and 74); the cavities of the optic vesicles are still con-
tinuous through the stalk with the cavity of the prosencephalon,
dipping into the recessus opticus; the ventral wall of the optic
stalk thus becomes continuous with the floor, and the dorsal wall
with the lateral wall of the prosencephalon (Fig. 84). Growth
of the mesenchyme situated above the original optic stalk appears
to be an active factor in the separation; at least it grows at a
rate sufficient to fill in the space produced by the constriction.
At the same time there is a slight increase in the dorso-ventral

150

THE DEVELOPMENT OF THE CHICK

diameter of the fore-brain itself, though this is relatively slight
up to twenty somites, but it enhances the general effect of the
change in position of the optic stalk. The subsequent history
of the optic vesicles is given beyond.

(h) The delimitation of the tel- and diencephalon is initiated
by a forward expansion of the anterior end of the primary fore-
brain, which becomes the telencephalon or secondary fore-brain,
the remainder being then known as the diencephalon or 'tween
brain. The expansion proceeds very rapidly from the 14 s stage,
and it is probable that it involves only the dorsal zones. It is,

Ectjm

Am.F.

;gMmm

/Irn.F.

V.-;

EE.B.C.

SO'p/.

^.o*^^-

E.E.B.C.

/TB.

/-•W'X€f^>.//,^0k

R

-r

op.

sprpi.

Fes.

L

Pr'a.

op. St.

Fig. 84. — Transverse section through the fore-brain and optic vesicles of a

16-s embryo.
Am. F., Amniotic fold. Ectam., Ectamnion. L., Left side, op.st.,
Optic stalk. R., Right side. Other abbreviations as before.

however, difficult to establish an exact line of demarcation be-
tween the two subdivisions of the primary fore-brain, until about
the 18 to 20 s stage, when a slight transverse fold or indentation
in the roof (velum trans versum) gives a dorsal landmark (Figs.
73, 85); the recessus opticus forms the ventral boundary between
the two. The velum transversum lies a considerable distance
above the dorsal end of the lamina terminalis, but it is difficult
to say just how far, owing to the indefiniteness of this point for
some time after the disappearance of the neuropore. A line
drawn between the velum transversum and the recessus opticus
mav be taken as the boundary between the two divisions of the

FROM TWELVE TO THIRTY-SIX SOMITES

151

primary fore-brain; but, owing to the simultaneous lateral expan-
sion of the telencephalon, the line of separation in the lateral
walls forms a curve with the convexity directed posteriorly
(Figs. 83 E and 86).

(c) The next stage in the differentiation of the telencephalon
(20 s to 36 s) is characterized by a rapid expansion and evagina-
tion of its lateral walls, while the entire median strip extending
from the velum transversum to the recessus opticus remains prac-

FiG. 85. — Optical sagittal section of the head of an embryo of 22-23 s.
The heart is represented entire.
Atr., atrium. Hyp., anterior lobe of the Hypophysis. Inf., Infun-
dibulum. Md., Mandibular arch, or.' pi., Oral plate. Pr'o. G., Pre-
oral gut. Th., First indication of thyroid. T. p., Tuberculum posterius.
V. tr., Velum transversum. Other abbreviations as before.

tically unaltered, and thus acts like a rigid band stretched over
the surface between these two points. The effect of this is to
form a pair of outgrowths that soon begin to project dorsally,
anteriorly, and posteriorly (Fig. 83 E); these are the primordia
of the cerebral hemisi:)heres, the cavities of which thus appear
as lateral diverticula of the median cavity of the telencephalon
(Fig. 86). The central part of the telencephalon may be called
the telencephalon medium, and the lateral outgrowths the hemi-
spheres. The walls of the hemispheres become considerably
thicker in this period, but quite uniformly at first, so that the
distinction between mantle and basal ganglia is indicated only
by position. (See Chap. VIII.)

152

THE DEVELOPMENT OF THE CHICK

The median strip includes the tela choroidea, beginning at
the diencephalon, and the lamina terminalis, which ends at the
recessus opticus. These divisions are of great prospective signifi-
cance, though at the stage of 36 s they are but slightly differen-
tiated, save by their position. A slight thickening of the lamina
terminalis just in front of the recessus opticus marks the site of
the future anterior commissure (Figs. 87 and 88).

Metenc.

J

Mesenc

MijeJenc

Te/enc

Fig. 86. — Inner view of the brain of a chick of al^oiit 82 hours, drawn from
a dissection.
Ch. opt., Chiasma opticus. Ep., Epiphysis (pineal gland). Isth., Isth-
mus. Pl.enc. v., PHca encephah ventrahs. Rec. opt., Recessus opticus.
V. tr., Velum Transversum. Other abbreviations as before.

The Diencephalon. The portion of the primary fore-brain pos-
terior to the telencephalon is known as the diencephalon. It in-
cludes the second and third neuromeres and probably also the
ventral zones and floor of the first (Fig. 83). A slight constriction
in the roof that appears about the 18 to 20 s stage near the junc-
tion of the middle and last third may represent the boundary be-
tween the second and third neuromeres; this persists for a long
time and may be traced in the lateral walls to the region of the

FROM TWELVE TO THIRTY-SIX SOMITES

153

infimdibiilum (Fig. 83 E) ; thus the diencephalon may be divided
into an anterior and posterior division, parencephalon and synen-
cephalon (Kupffer) (Fig. 87). Tlie optic stalks are attached to
the floor and ventral zones at the extreme anterior end. The
diencephalon includes part of the roof, floor, and dorsal and ven-
tral lateral zones of the original neural tube. These may be de-
scribed as follows (Figs. 87 and 88):

Oes

5t0/7f. — '

''Jy/?e/)c

Parenc.

Aw.

Fig. 87. — Optical longitudinal section of the head of an eml^ryo of 30 s.
The heart is represented entire.
Atr., Atrium (auricles). B. a., Bulbus arteriosus. D. v., Ductus venosus.
Lg., Laryngo-tracheal groove. Oes., Oesophagus, or. pi., Oral plate, which
has begun to rupture. Parenc, Parencephalon. Ph., Pharynx. Stom.,
Stomach. Synenc, Synencephalon. Th., Thyroid. S. v., Sinus venosus.
Yen. R., Right ventricle. Other abbreviations as before.

The roof rises quite sharply from the velum transversum, and
is indented between the parencephalic and synencephalic divi-
sions as already noticed. It is relatively thin. About the 30-
35 s stage the epiphysis (pineal body) begins to form as an
evagination from about the middle, and by the 36 s stage is a
small hemispherical protuberance (Figs. 86 and 88). The floor
becomes extremely thin in the center of the recessus opticus, which
marks its anterior end; immediatelv behind this is a sudden and

154

THE DEVELOPMENT OF THE CHICK

conspicuous thickening, the optic chiasma, which is continued
as a ridge in tlie lateral ventral zones on each side (Fig. 86).
The infunclibulum follows just behind this, and constitutes a
considerable pouch-shaped depression from which the saccus
infundibuli grows out later. The posterior wall of this depression
rises sharply and joins the thickened tuberculum posterius which
is the end of the floor of the diencephalon. The diencephalon is
compressed laterally (Fig. 97); the dorsal zones are slightly
thickened, indicating the future thalami optici.

Fig. 88. — Optical longitudinal section of the head of an enil^ryo of 39 s.
Abbreviations as before.

The anterior lobe of the hypophysis should be mentioned here,
although it is not embryologically a part of the brain. It arises as
a median tubular invagination of the ectoderm of the ventral sur-
face of the head immediately in front of the oral plate at about
the 20 s stage (Fig. 85), and grows rapidly inward in contact with
the floor of the diencephalon. At about the 30 s stage its end
reaches nearly to the infimdibulum (Fig. 87). At first part of
its wall is formed by the oral plate, and when this ruptures the
effect is to shorten the apparent length of the hypophysis (Fig.
88) . At about the 36 s stage its distal portion flattens laterally

FROM TWELVE TO THIRTY-SIX SOMITES 155

and shows indication of branching. Subsequently it becomes
much branched and quite massive and unites with the infun-
dibuhim to form the pituitary body. (See Chap. VIII.)

The Mesencephalon. This portion of the brain comes to
occupy the summit of the cranial flexure, which indeed owes its
origin largely to the rapid growth in extent of the roof of the
mesencephalon. In longitudinal section it thus appears wedge-
shaped, with short floor and long arched roof (Figs. 87 and
88). Its walls remain of practically uniform thickness up to
the seventy-second hour. The lateral walls expand more rapidly
than the roof and thus form the optic lobes. But these are
barely indicated at the 36 s stage.

Isthmus. The great expansion of the mesencephalon does
not involve the portion immediately adjacent to the hind-brain,
which is henceforth known as the isthmus (Figs. 87, 88).

The Rho7nbencephalon (Primary Hind-brain). Two divisions
of the embryonic brain arise from the rhombencephalon, viz.,
the metencephalon and the myelencephalon; the former becomes
the region of the cerebellum and pons of the adult brain,
and the latter the medulla oblongata. The metencephalon is a
relatively short section of the original rhombencephalon, and
includes only the most anterior neuromere of the rhomben-
cephalon or the sixth of the series (Fig. 83 D, E). It may be
distinguished at the beginning of the period under consideration
by the fact that its roof remains as thick as that of the mesen-
cephalon. At the end of this time, i.e., seventy-two hours, the
roof in sagittal sections appears to rise sharply from the isthmus
and thins towards the summit, where it passes into the thin epi-
thelial roof of the myelencephalon (Figs. 87 and 88). The rudi-
ment of the cerebellum is slightly thicker on each side of the
middle line at seventy-two hours.

The myelencephalon becomes sharply characterized by the
thinness of its roof and thickening of ventral lateral zones and
floor. The epithelial roof has a triangular form, the base resting
against the metencephalon. The neuromeres remain very distinct
(Figs. 83, 89), but change their form. Up to about twenty-three
somites they still form external expansions, but as the wall
thickens the external surface becomes smooth, and the neuro-
meres may now be recognized as a series of concavities in the
lateral wall, with intervening projections (Fig. 89). The arrange-

156

THE DEVELOPMENT OF THE CHICK

ment of the nuclei leaves thin non-nucleated strips (septa) be-
tween adjacent neuromeres. The interneuromeric projections are
most pronounced laterally and fade out dorsally and ventrally.

Behind the neuromeric portion of the hind-brain is a portion
extending to the posterior end of the fourth mesoblastic somite
from which the twelfth cranial nerve arises.

The Neural Crest and the Cranial and Spinal Ganglia. The
cranial and spinal ganglia owe their origin to a structure known
as the neural crest, which is a practically continuous cord of cells,
h^ng on each side in the angle between the neural tube and
the ectoderm, extending from the extreme anterior to the pos-
terior end. Like other meristic structures the anterior portion

Fig. 89. — Frontal section of the hind-brain region of an embryo of about
36 s.
Ot., Otocyst. N. 6, N. 7, N. 8, N. 9, N. 10, N. 11, Neuromeres, 6 to 11,
according to Hill's enumeration, s. 1, s. 2, s. 3, First, Second, and third
somites. V, Primordium of the trigeminus. VII-VIII, Primordium of the
acustico-facialis.

of the neural crest is the first to arise (at about 6-7 s stage),
and the remainder appears in successive order during or shortly
after the closure of the neural tube in each region; thus it is not
until after the completion of the neural tube that the last portion
of the neural crest is established.

But before this time successive enlargements of the cranial
part of the crest have formed the primordia of the cerebral gan-
glia, and similar successively arising enlargements of the parts
of the crest opposite the mesoblastic somites form the rudiments
of the spinal ganglia. The intervening portions of the crest form
the so-called interganglionic commissures, which subsequently

FRO:\I TWELVE TO THIRTY-SIX SOMITES

157

appear to form mesenchyme. The formation of mesenchyme
from certain parts of the neural crest is most marked in the
region of the brain.

The primordia of the gangUa contain the cells (neuroblasts)
which form the dorsal root fibers of the spinal nerves and parts
of certain cranial nerves. They also appear to contain the cells
from which the sheaths of the nerve fibers are formed; thus
three kinds of cells at least are found in the neural crest, viz.,
mesenchyme forming cells, neuroblasts, and sheath cells.

The Cranial Neural Crest and its Derivatives. The neural
crest in the head may be divided into pre- and post-otic divisions,
and these arise at different times.

„ Pr- Slit. ctr.

Gi:

Fig. 90. — Transverse section of the fore-brain, and optic
vesicles at the stage of 7 s.
M'ch., Mesenchyme, n. Cr., Neural crest. Ph., Phar-
ynx. Sut. cer., Anterior cerebral suture. X., Mass of cells
in which the anterior end of the intestine, the neural tube
and the notochord fuse.

(1) The pre-otic division, which extends from the extreme
anterior end of the neural tube to about the center of the audi-
tory pit, is well developed at a stage of 7-8 somites, but it is not
found at the 5 s stage. The origin is everywhere the same, viz.,
from the dorsalmost cells of the medullary plate and the ecto-
derm immediately adjacent; it arises at the time of contact of
the medullarv folds and is thus thickest in the region of the
suture. Fig. 90 is a section through the developing optic vesicles,
and shows the neural crest continuous with the tube and ectoderm

158

THE DEVELOPMENT OF THE CHICK

in the neural suture; it is separated from the mesenchyme in the
region of the fore-gut by a considerable space. (We shall call
the latter portion of mesenchyme the axial mesenchyme of the
head, to distinguish it from the mesenchyme derived from the

neural crest, which later lies lat-
eral to it, and which may thus
be known as the periaxial layer.)
The crest may be followed ante-
riorly to the extreme tip of the
neural tube, and posteriorly to
the region of the anterior intesti-
nal portal, which lies at about the
transverse level of the future au-
ditory pit (cf. Fig. 91). In the
region of the mid-brain it spreads
out laterally until its peripheral
cells reach the axial mesenchyme.

Goronowitsch divides the pre-otic
portion of the neural crest into pri-
mary and secondary ganglionic crests,
the post-otic portion being the terti-
ary crest. According to his account
there is a decided difference in time
of origin of the primary and second-
FiG. 91. - Diagram of the cephalic ^ry crests ; the primary, involving the
neural crest of a chick of about region of fore- and mid-bram, aris-
12 s. (After Wilhelm His.) ing before the secondary which in-

cludes the region of the trigeminus
and acustico-facialis. I have not, however, found such a difference in
my preparations.

At the stage of 10 somites the cells of the pre-otic neural
crest have lost their connection with the neural tube. Behind
the optic vesicles they have spread out laterally between the
axial mesenchyme and the ectoderm, where they form a prac-
tically continuous periaxial layer, distinguishable from the axial
mesenchyme by its greater density, and hence deeper stain;
but apparently mingling with it at the surface of contact.

In the stages immediately following (10-20 s), the portions
of the periaxial layer lying above the mandibular and the hyoid
arches condense and thicken, and form strong cords extending

FROM TWELVE TO THIRTY-SIX SOMITES

159

from the superior angles of the neural tube into the arches in
question; here they form connections with the ectoderm of the
arches, which proliferates so as to contribute to their substance
(Fig. 92). Elsewhere the periaxial layer gradually merges with
the axial mesenchyme. The periaxial cords are the primordia
of the trigeminus and acustico-facialis ganglia, and mark the
paths of the trigeminal and facial nerves. Their connection with

c .

/>*■-
'...

9'

(' - ' - .1_

£MW^^^^'

*1

ifmv^.

Fig. 92. — Transverse section immediately be-
hind the first visceral pouch of a chick
embryo of thirteen somites. (After Gorono-
witsch.) Note connection of the periaxial
cord with the ectoderm of the visceral arch.

Ad., Aorta descendens. c. Rounded me-
senchyme cells, g. Place where cells derived
from neural crest unite with the mesenchyme
cells of the periaxial cord. f. Fusion, p. Spin-
dle-shaped peripheral mesenchyme cells.

the ectoderm in the neighborhood of the first visceral pouch
must not be confused with the so-called branchial sense-organs,
for the primary connection is soon lost, and secondary connec-
tions arise at about the 27 s stage, and constitute the true branchial
sense-organs of these arches.

160 THE DEVELOPMENT OF THE CHICK

The acustico-facial periaxial cord attains definite ness some
time before the trigeminal (cf. Fig. 71), and indeed appears almost
from the first as a specially strong part of the periaxial layer:
whereas in the region of the trigeminus the cells of this layer are
first Avidely dispersed and secondarily aggregate, between the
stages of 14 and 18 somites. Both cords are attached to the
brain, the trigeminus to the first neuromere of the myelenoepha-
lon, and the acustico-facialis to the third (Fig. 83 E).

The trigeminal and facial periaxial cords are supplemented,
as we have seen, by proliferations of the ectoderm on each side
of the first visceral pouch; the trigeminal cord then enters the
mandibular arch, and the facial the hyoid arch, and in the stages
between 20 and 27 somites form at least part of the mesenchyme
of these arches. The axial mesoblast likewise contributes to the
mesenchyme of these arches, and it becomes impossible in later
stages to separate these two mesenchymal components. The
ganglia proper differentiate from the upper portions of the cords.
The trigeminal periaxial cord divides over the angle of the mouth
and sends out a process into the rudimentary maxillary process.
A third projection of the same cord towards the eye forms the
path of the ophthalmic division of the trigeminus (Fig. 117).

At the stage of about 27 s the trigeminus forms a connection
with a thickening of the ectoderm (placode of the trigeminus)
situated in front of and above the first visceral cleft; and the
facial connects similarly with a larger ectodermal thickening
(placode of the facialis) situated on the posterior margin of the
uppermost part of the first visceral furrow. These ectodermal
thickenings are rudimentary structures of very brief duration,
representing parts of the sensory canal system of the head of
aquatic vertebrates. Their occurrence in the chick is an interest-
ing example of phylogenetic recurrence. A third and fourth
like organ arises in connection with the post-otic ganglia.

At the stage of 72 hours there are two ectodermal thicken-
ings (placodes) in connection with the trigeminus, one in front
of the other, derived probably by division of the original first.
The facialis placode is more fully developed.

(2) The post-otic ganglionic crest is a direct continuation of
the pre-otic behind the ear, and it is at first difficult to make an
exact boundarv between them. At the stage of 13 s the pre-otic
crest extends beneath the auditory epithelium nearly to its middle

FROM TWELVE TO THIRTY-SIX SOMITES 161

in the form of a thick mass of cells in the roof of the neural tube.
Towards the posterior end of the auditory epithelium the crest
becomes smaller, and this is the beginning of the post-otic crest.
Behind the ear the crest becomes larger again and extends later-
ally so as to form a periaxial layer between the ectoderm and
the axial mesoblast which extends back, above the first, second,
and third somites to the middle of the fourth. The part between
the ear and the first somite is, however, by far the best developed,
the continuation behind being a relatively slight cord of cells.

At about the stage of 17 somites the anterior part of the crest
condenses to form a well-defined periaxial cord, which arises
from the neural tube above the middle of the auditory pit, arches
back behind its posterior margin and extends down into the
third visceral arch, where it enlarges. This is the glossopharyn-
geal periaxial cord. There is an enlarged jwrtion of the crest
just behind this overlying the site of the future fourth and fifth
arches, but its substance is not yet condensed to form a distinct
periaxial cord.

At the stage of 20 somites the anterior cardinal vein and the
duct of Cuvier form the posterior boundary of the enlarged por-
tion of the post-otic crest (Fig. 73). The part of the periaxial
layer immediately in front of this is somewhat condensed to
form the periaxial cord of the vagus, and this is only indistinctly
separated from that of the glossopharyngeus.

The formation of the third visceral cleft definitely splits the
periaxial layer into the periaxial cords of the glossopharyngeus
and vagus (25 s). This division is carried up indistinctly, at
first, into the roots which occupy the space between the auditory
sac and the first somite. The formation of the fourth visceral
pouch similarly divides the distal portion of the vagus cord,
so that part of it lies in front of the pouch and part behind.

At the stage of seventy-two hours the ganglion petrosum
(glossopharyngeus) is definitely formed by an enlargement of
the cord just above the third visceral arch, and the ganglion
nodosum (vagus), similarly formed from the vagus cord, lies
above the fourth visceral pouch, thus extending over the fourth
and fifth arches. Branchial sense organs are formed at the dorsal
angles of the second and third visceral furrows in connection
with the IX and X nerves respectively.

It would appear that the neural crest in the head is the

162 THE DEVELOPMENT OF THE CHICK

source of much of the mesenchyme, and it is an interesting ques-
tion whether or not such mesenchyme has a different fate from
that of different origin. Nothing definite, however, is known in
regard to this, owing to the impossibihty of separating the various
kinds after they have once merged.

The Neural Crest in the Region of the Somites. The neural
crest is very sUghtly developed in the region of the first five so-
mites, which is correlated with the fact that these somites are
devoid of ganglia. But the mode of origin is the same through-
out the somitic region. Shortly after the closure of the neural
tube in any region the neural crest forms an aggregation of cells
in the roof, more or less sharply separated from the remainder
of the tube both by the arrangement of the cells and also by their
lighter stain (Figs. 107, 109, 112, 113). The early history may be
followed in a single embryo, by comparing the conditions opposite
the last somite with that of more anterior somites where develop-
ment is more advanced. Figs. 107, 108, 109, 110 represent
transverse sections through the twenty-ninth, twenty-sixth,
twentieth, and seventeenth somites of a 29 s embryo. In Fig.
107 the cells of the crest are extending towards the upper angle
of the somite, with which they are connected by protoplasmic
strands. The aggregation in the roof of the neural tube is thus
decidedly diminished; the lateral wings of the crest lie in the angle
between the neural tube and the ectoderm. In the twenty-sixth
somite (Fig. 108) the lateral wings extend farther from their point
of origin, and appear to have a more intimate connection with
the myotome. In the more anterior and older somites, twenty
and seventeen (Figs. 109 and 110), the process has progressed
much farther and the neural crest cells are completely expelled
from the neural tube, which closes after them (Fig. 110). A j-et
later stage is shown in Fig. Ill, through the twenty-third somite
of a 35 s embryo.

The dorsal commissure uniting the right and left sides of the
crest ruptures, and the cells of the crest aggregate so as to form
a pair of ganglia in each somite. Thus, although the neural crest
is primarily a median structure, it becomes divided into two
lateral halves, and although it is primarily a continuous structure
it becomes divided into a series of pairs of metameric ganglia.
The fate of the interganglionic commissures is conjectural. The
ganglia are ill-defined from the mesenchyme when they are first

FROM TWELVE TO THIRTY-SIX SOMITES

163

V.

Md.

V.C.f

■^•^-l

Ot.

'i^~

V.C.2^

h

S.2.

D.C.

';-,_!^DJenc.

3.J0.

— ' — •'^-'^^^SsSt-- '■■--■

v5.2C

^.27

■— i/?//:

^/77.

r^.^y^

-■ ,

... :^:

L.

.•^r^-rff !ili.

v-iJiC— -L

ii^L ■-■

; Tv,

^^i

Fig. 93. — Entire embryo of 27 s viewed as a

transparent object from above.

a. a. 1, a. a. 2, a. a. 3, First, second, and third
aortic arches. Car., Carotid loop. Ret., Retina.
V. C. 1, V. C. 2, First and second visceral clefts.
Other abbreviations as before, x 20.

164 THE DEVELOPMENT OF THE CHICK

formed, but they rapidly become well differentiated.

IV. The Organs of Special Sense (Eye, Ear, Nose)

Embryologically a sharp distinction must be drawn between
the essential percipient part of the organs of sense (retina of the
eye, olfactory epithelium, and epithelium of the membranous laby-
rinth) and the parts formed for protection and for the elaboration
of function. The sensory part proper is the first to arise in the
embryo, and is protected later by modifications of surrounding
tissues or parts. We may thus distinguish between primary and
secondary parts in the case of all organs of sense. Only the early
history of the primary parts falls within the period covered by
this chapter, except the formation of the lens in the case of the
eye.

The Eye. The primary optic vesicles arise, as we have seen,
as lateral expansions of the anterior end of the neural tube;
their position is indicated by an enlargement of the neural tube
even before the meeting of the medullary folds in this region.
The shape and relations of the early optic vesicles have already
been described and figured. The cavity may be called the Ven-
triculus opticus. The origin of the optic stalk by constriction
of the base of the vesicle was described in a preceding section
of this chapter (p. 149). The stalks remain attached to the
ventral end of the lateral walls of the diencephalon in the region
of the recessus opticus, and constitute tubular connections between
the vesicles and the brain, in the walls of which the optic nerve
develops later (Fig. 84).

Locy found six pairs of " accessory optic vesicles " occurring in series
immediately behind the true optic vesicles; they form low rounded
swellings of the side-walls of the neural folds before the true brain
vesicles are indicated, and last only about three hours in the chick
(twenty-fourth to twenty-seventh hours of incubation). "Their exist-
ence supports the hypothesis that the vertebrate eyes are segmental, and
that the ancestors of vertebrates were primitive)}' multiple-e3'ed.'' (Locy.)

The external surface of the optic vesicle early reaches the
ectoderm, to which it appears to be cemented at the 10 s stage.
In the 17-18 s stage, the optic vesicles project decidedly behind
the attachment of the optic stalk, and the external wall is slightly
thicker than that next the brain. . The ectoderm then becomes
thickened over a circular area in contact with the optic vesicle

FROM TWELVE TO THIRTY-SIX SOMITES

165

and this constitutes the primordium of the lens (Fig 94). The
thickening of the external wall of the optic vesicle and of the
lens primordium now proceed rapidly, and soon an invagination
is formed in each (Fig. 95).

Fig. 94. — Section through

the primordium of the eye

of a chick embryo of 21 s.

(After Froriep.)

d., Distal wall of optic
vesicle, p., Proximal wall
of optic vesicle.

Fig. 95. — Section through the
primordium of the eye of a
chick embryo at the end of
the second day of incubation.
(After Froriep.)

It is probable that a stimulus is exerted by the optic vesicle on the
ectoderm with which it is in contact, causing it to thicken and become
the primordium of the lens. This has been demonstrated experimentally
to be the case in the embryo of the frog, and the morphological rela-
tions are the same in the chick. The invagination of the primary optic
vesicle to form the secondary optic vesicle is not mechanically produced
by the growth of the lens, as some have supposed, for it has been shown
(see Fol and Warynsky) that the secondary optic vesicle is formed in
the absence of the lens.

We may now consider the formation of the optic cup and of
the lens separately.

The Optic Cup. The invagination of the outer wall of the
primary optic vesicle gradually brings this wall into contact
with the inner wall and obliterates the primary cavity. Thus

166 THE DEVELOPMENT OF THE CHICK

is established the secondary optic vesicle or optic cup (aipula
optica). Special attention must be given to the form of the in-
vagination, for this determines relations of fundamental impor-
tance. The invagination may be stated to consist of two parts.
The first is directly internal to the lens primordium, and the second,
which is continuous with the first, involves the ventral wall of
the primary optic vesicle as far as the optic stalk. Two parts
may thus be distinguished in the mouth of the optic cup — (1) an
external part, which becomes the pupil of the eye, and (2) a ventral
part, continuous with the pupil, which is known as the choroid
fissure. Figs. 96 A, B, and C exhibit these relations better than
a detailed description.

The choroid fissure is a transitory embryonic structure, sub-
sequently closing by fusion of its lips. However, it establishes
a relation of fundamental importance in that the ventral wall
of the optic-stalk is kept continuous in this way with the inner
or retinal layer of the secondary optic vesicle (Figs. 96 B, and 97),
and thus a path is provided for the development of the optic
nerve (see Chap. IX). It also provides an aperture in the wall
of the optic cup for the entrance of the arteria centralis retinae.

The optic primordium at the 36 s stage, with the omission of
the lens, is composed as follows:

(1) Optic-stalk attached to the floor of the brain; this is
still tubular.

(2) The optic cup or secondary optic vesicle consisting of
two layers, viz., (a) a thick internal or retinal layer continuous
at the pupil and choroid fissure with {b) the thin external laj^er.
The cavity of the cup is the future posterior chamber of the eye;
it has two openings, viz., the pupil filled by the primordium of
the lens, and the slit-like choroid fissure extending from the pupil
to the optic stalk along the ventral surface. The retinal layer
is continuous with the floor of the optic-stalk, and thus with the
diencephalon.

The optic cup expands with extreme rapidity between the
stages of 26 and 36 somites, as may be seen from the figures by
comparing the relative size of the lens and optic cup at different
stages.

The Lens. The invagination of the thickened ectoderm
external to the optic vesicle soon leads to the formation of a deep,
thick-walled pit which rapidly closes (26-28 somites) and thus

FROM TWELVE TO THIRTY-SIX SOMITES ]67

forms an epithelial sac, which at first practically fills the cavity
of the optic cup. However, it very soon becomes detached from
the posterior wall of the optic cup, which expands with great
rapidity, and the lens is left at the mouth of the cup. The walls

§■

5o

;/

5

^

^ v

•to

~>5

<

O
CO

I

O o3
to

O O
O

^ '^ '

"5 .'o

o

73

>5 P O

^ 'IS -^^

-^ o

d ~^

r-* O t^

c o "

S S fcn

C ;^ O

^ - <^

C •" CO

Is . ^

_ o _a

-M O til

1^ S Oi

M 2 .

U2

tC r/":.

a;

be bi^. c g^
c o ^ ^ +^

I

£ e3.3i Si a^ 2

O fH

c3

•- o

I «&

5 =^ xa 5^

cs c: .1

O ci 3

X

.0 o t^

o o

o

O M

P^

of the lens sac are at first of practically even thickness (28 s),
but by the 35 s stage a great difference has arisen by the elonga-
tion of the cells of the inner wall, which are destined to form
lens fibers: the cells of the anterior (outer) wall elongate much

168

THE DEVELOPMENT OF THE CHICK

less during this period, and are destined to form the ei^ithelium
of the lens (Fig. 97). Intermediate conditions are found around
the equator of the lens. The subsequent history is given in
chapter IX.

The Auditory Sac. At about the 12 s stage the first evidence
of the auditory sacs is found in the form of a pair of circular
23atches of thickened ectoderm situated on the dorsal surface of
the head opposite to the ninth, tenth, and eleventh neuromeres,
and thus a short distance in front of the first mesoblastic somite;
it lies between the rudiments of the acustico-facialial and glosso-
pharyngeal ganglia. In the 14 s stage the auditory epithelium

/fiw. p.C/i

Lens .

Fig. 97. — Transverse section through the eyes and heart of an embryo of
about 35 s. The plane of the section will be readily understood by com-
parison of Fig. 117.

ch. Fis., Choroid fissure. D. C, Duct of Cuvier. Lg., Lung. pi. gr.,
Pleural groove. V. c, Posterior cardinal vein. Y. S., Yolk-sac. Other
abbreviations as before.

is slightly depressed, and in the 16 s stage it forms a wide-open
pit. At about the 20 s stage the mouth of the pit narrows slightly,
and gradually closes (28-30 s), thus forming the auditory sac or
vesicle (otocyst) (cf. Figs. 71, 73, 89, and 93).

The method of closure of the pit, which is of interest, may
readily be observed in mounts of entire embryos; at first the
lips fold over most rapidly from the anterior and posterior mar-
gins; thus the mouth of the pit becomes elliptical with the long
axis vertical (stage of 22 somites) and extending from the apex
nearly to the base. The ventral lip then begins to ascend (stage
of 24 somites) and the closure gradually proceeds towards the

FROM TWELVE TO THIRTY-SIX SOMITES

169

^- D.

B.end'l.

M.

<;a

rf§^

'<*".

apex, so that by the stage of 29 somites the opening is reduced
to a minute eUipse situated on the external side of the dorsalmost
portion of the otocyst (see Fig. 93). This portion of the otocyst
now begins to form a small conical
elevation, and the final closure takes
place on the external side of this
elevation, which is destined to
form the endolymphatic duct. The
latter remains united to the epi-
dermis at this point for a consid-
erable period of time by a strand
of cells which may preserve a
lumen up to 104 hours (Fig. 98).
The final point of closure of the oto-
cyst is thus very definitely placed,
and it coincides with the middle of
the endolymphatic duct, that is,
with the junction of the later formed
saccus and ductus endolymphaticus.
In the Selachia this duct remains
in open communication with the
exterior throughout life; the rela-
tively long persistence of its con-
nection with the epidermis in the
chick may thus be interpreted as a Fig. 98. — Section of the otocyst
phylogenic reminiscence of the an- of an embryo of 104 hours. The
, i-^. original opening of the otocyst

cestral condition. .^ ^^^^^^^ ^^^^ .^^^ ^ ^^^^^^ ^^_

The Nose (Olfactory Pits). At ^^.^j ...^j^h connects with the

about the 28 s stage, the ectoderm endolymphatic duct (recessus

on the sides of the head a short dis- labyrinthi).

i^noP' in front of the eves aDDears ^•' ^^^^ ^^ ^^^^^ ^^ ^^^^ otocyst

tance m iiom oi ine eyes appeaib (.^^^jj^^.,)^ b., Canalleading from

thickened. Two circular patches of the surface to the otocyst. D.

ppfnrlprm nrp thus marked off the end'l., Endolymphatic duct. D.,
ectoderm are tnus maiKea on,^ me j^^^^^^j ^^^^ Ectoderm of the

beginning of the olfactory epithe- surface of the head. Gn., Audi-

lium; at first this grades almost im- tory ganglion. L Lateral. M.,

' '^ . , , . Median. V., ventral,

perceptibly into the neighboring

ectoderm. In the stages immediately following the olfactory

plates appear to sink down towards the ventral surface of the

head, due no doubt to more rapid growth of the dorsal portion

of the head. Thus they appear at the ventro-lateral angles of

if-'-

V.

170 THE DEVELOPMENT OF THE CHICK

the anterior part of the head at the stage of 36 somites. During
the displacement a depression appears in the center of each olfac-
tory plate, and as this becomes deeper, the olfactory pits are
formed (Figs. 99 and 117). At the stage of 36 somites each is
a deep pit situated at the junction of the sides and ventral sur-
face of the anterior portion of the head, with the wide mouth
opening outwards and ventrally.

The olfactory epithelium now becomes sharply differentiated
from the ectoderm of the head, owing to the formation of a super-
ficial la3^er of cells (teloderm, see p. 285) above the columnar cells
in the ectoderm, but not in the region of the sensory epithelium,
where the cells still form a single layer. In the center of the
olfactory pit the epithelium is very much thickened owing to
elongation of the cells, and the nuclei lie in five or six layers;
there is a gradual thinning of the epithelium to the lips of the
pit and then a sudden, but graduated, decrease to the general
ectoderm. The line of junction of olfactory epithelium and
indifferent ectoderm of the head is a little distance beyond the
margin of the pit, as may be determined by the edge of the telo-
dermic layer; in other words, all of the olfactory epithelium is
not yet invaginatecl.

It is probable that the invagination of the olfactory plates is
due mostly, up to this time, to the processes of growth within
the plates themselves, although there has been considerable
accumulation of mesenchyme in this region. But the subsequent
deepening of the pits appears to be due largely to the formation
of processes around the mouths of the primary pits. (See
Chap. IX.)

V. The Alimentary Tract and Its Appendages
We have already learned that the main portion of the alimen-
tary tract arises from the splanchnopleure; a portion of the mouth
cavity is, however, lined with ectoderm and arises from an inde-
pendent ectodermal pit, the stomodceum, which communicates
only secondarily with the entodermal portion; similarly the last
portion, external to the cloaca, arises from an ectodermal pit,
the proctodceum, which communicates only secondarily with the
entodermal part. We shall thus have to consider the origin of
the stomodseum and the proctodeum in connection with the
alimentary tract.

FROM TWELVE TO THIRTY-SIX SOMITES

171

Of l/ll-V/l/ jV'm V. Mef-er/c. ^^'^•

\cr.Ff.

cerv.FJ.

■'A

5 JO

• Jens.
■ -c/i.F/s.

:C^pcM

S20r

5JCK^-

M

.V.

; i^

^d /

/^S

5*

-^.K

-r-om.

Umb.

•■=*:'

/

Fig. 99. — Entire embryo of 31 somites viewed as a
transparent object,
am. Umb., Amniotic umbilicus. B. a., Bulbus
arteriosus, cerv. Fl., Cervical flexure, ch. Fis., Cho-
roid fissure, cr. Fl., Cranial flexure. D. C, Duct of
Cuvier. ex. o. c, External layer of the optic cup.
int. o. c, Internal layer of the optic cup (retina.)
N'm., Neuromere of myelencephalon. olf., Olfactory
pit. pc. W., Line of attachment of amnion to peri-
cardial wall. V. C. 1, 2, 3, First, second, and third
visceral clefts. Other abbreviations as before.

172 THE DEVELOPMENT OF THE CHICK

From the embryological point of view the aUmentary tract
may be divided into fore-, mid-, and hind-gut. The fore-gut
inchides the anterior portion as far back as the hver diverticula,
the mid-gut extends from here to the coecal appendages, and the
hind-gut inchides the remainder. From each division there
arise certain outgrowths which may be termed collectively
appendages of the alimentary tract, and these will also be
considered here, so far as they arise within the period covered
by this chapter. Thus from the fore-gut there arise the visceral
pouches, the thyroid and thymus glands, the postbranchial
bodies, the respiratory tract, and the liver and pancreas; from
the mid-gut the 3^olk-sac, and from the hind-gut the ccecal
appendages and allantois.

The enlargement of the body-cavity towards the middle line
gradually reduces the broad mesodermal septum situated between
its inner angles to a relatively narrow plate, which forms the dor-
sal mesentery of the intestine (Figs. 107, 109, 110, and 111). This
elongates in the course of development and forms a sheet of tissue
suspending the intestinal tube to the mid-dorsal line of the body-
cavity. It is composed of two layers of mesothelium (peritoneum)
continuous with the lining of the body-cavity and enclosing a
certain amount of mesenchyme; the dorsal mesentery extends
along the entire length of the intestinal canal.

A ventral mesentery uniting gut and yolk-sac is also estab-
lished by the meeting of the limiting sulci in the splanchnopleure.
When the body-wall closes, the ventral mesentery consists of
two layers of mesothelium attaching the intestinal canal to the
mid-ventral line of the body-wall. The dorsal and ventral mesen-
teries, together with the alimentary canal, thus constitute a
complete partition between the right and left halves of the body-
cavity. However, the ventral mesentery is a very transient
structure except in the region of the fore-gut and liver, and in
the extreme end of the hind-gut. In these places it is persistent
and is the seat of formation of important organs.

The wall of the intestine contains three embrvonic lavers:
viz., entoderm, mesenchyme, and mesothelium. The first forms
the lining epithelium of the intestine, and of all glandular attach-
ments, as well as of the respiratory tract and allantois; the last
forms the serosa; and the mesenchyme the intermediate layers.

We shall now consider the development of each region of the

FROM TWELVE TO THIRTY-SIX SOMITES 173

alimentary tract and the appendages proper to each in the follow-
ing order: (1) Stomodseum, (2) Pharynx, (3) CEsophagus, (4)
Stomach, (5) Hepato-pancreatic division of the fore-gut, (6) Mid-
gut, (7) Hind-gut.

The stomodaeum owes its origin to an expansion of the em-
bryonic parts surrounding the oral plate, and it gives rise to a
large part of the buccal cavity, which is therefore lined by ecto-
derm. (See Chap. X.) It will be remembered that at the 12 s
stage the oral plate lies between the pericardium and the fore-
brain (Fig. 67), and that it consists of a fusion between the
ectoderm of the ventral surface of the head and the entoderm
composing the floor of the anterior end of the fore-gut. It lies
in a slight depression on the under surface of the head which
is the beginning of the oral cavity. This small beginning owes
its enlargement (1) to the cranial flexure, by which the ventral
surface of the head becomes bent at right angles to the oral
plate instead of forming a direct continuation of it, and (2) to
the formation and protrusion of the mandibular arches and
maxillary processes at the sides and behind. (See fuller account
in Chap. VII.) In this waj' it becomes a deep cavity closed
internally by the oral plate. The series of figures of sagittal
sections through the head illustrates very well the gradual deep-
ening of the stomodseum by these processes (Figs. 75, 85, 87, 88).

The oral plate thins gradually from the 12 to the 30 s stage
when it breaks through (Figs 87 and 88), thus establishing an
opening into the alimentary tract. The remnants of the oral
membrane then gradually disappear and leave no trace. The
subsequent extension of the maxillary region to form the upper
jaw greatly enlarges the extent of the ectodermal portion of the
buccal cavity. It will have been noted (Figs. 85 and 87) that
the hypophysis opens in front of the oral plate on the ectodermal
side, and this constitutes a most important landmark for deter-
mining the limit of the ectodermal portion of the buccal cavity
in later stages.

The Pharynx and Visceral Arches. The pharynx may be briefly
defined as the alimentary canal of the head. It is the most
variable part of the alimentary canal in the series of vertebrates.
]\Iodified, as it is in all vertebrates, for purposes of respiration,
the transition from the aquatic to the terrestrial mode of respira-
tion brought about great changes in it. It is thus marked em-

174 THE DEVELOPMENT OF THE CHICK

bryologically first by the development of structures, the visceral
arches and clefts, whose primary function was aquatic respira-
tion, and second by the development of the air-breathing
lungs. Such fundamental changes in function have left a deep
impression, not only on the embryonic history of the pharynx
itself, but also on the development of the nervous and vascular
systems.

The extreme anterior end of the pharynx extends at first
some distance in front of the oral plate, and may hence be called
the pre-oral gut (Figs. 75, 85, etc.). After the rupture of the
oral plate, the pre-oral gut appears like an evagination of the
pharynx immediately behind the hypophysis and is now known
as Seessel's pocket (Fig. 87), but it gradually flattens out and
disappears (Fig. 88).

The form of the pharynx at thirty-three hours has l^een
already described; briefly, it is much expanded lateralh^, exhibiting
a crescentic form in cross-section (Fig. 54 A). The horns of the
crescent are in contact with the ectoderm in front of the auditory
pit, marking the site of the future hyomandibular cleft, which
arises by perforation in the fused area at about forty-six hours.
A second pair of lateral expansions brings about a second fusion
of the lateral wings of the pharynx just behind the auditory pit
at about the stage of 19-20 somites. This is followed b}^ the
formation of a third and a fourth pair of lateral evaginations of
the pharynx which reach the ectoderm at about 23 s and 35 s
respectively. The walls of the pharynx appear considerably
constricted between the evaginations which are known as vis-
ceral pouches (Figs. 100 and 101).

Corresponding to each visceral pouch there is formed an
ectodermal invagination of much lesser extent, which may be
known as the visceral furrow. The furrows do not form directly
opposite the pouches, but slightly behind them so as to overlap
the margins of the latter (Fig. 101). The ectoderm of the visceral
furrows forms a close union with the entoderm of the pouches,
and openings arise within these areas, excepting the fourth,
forming transitory visceral clefts.

There are thus four pairs of visceral pouches and furrows,
known as the first, second, third, and fourth; the first is some-
times called the hyomandibular.

According to Kastschenko, there are evidences of three pairs of

FROM TWELVE TO THIRTY-SIX SOMITES

>3

175

visceral furrows in front of the first at the 14-16 s stage. These he in-
terprets as phyletic rudiments. It is certain that the lower vertebrates
had pouches posterior to the fourth. The post-branchial bodies (see
p. 309) are probably rudiments of a fifth pair of pouches.

The tissue between the visceral pouches thickens, by accumu-
lation of mesenchyme, to form the visceral arches, of which there
are five, viz.: (1) the tnandibular in front of the first pouch, form-
ing also the posterior boundary of the oral cavity, (2) the hyoid
between the first and second pouches, (3) the third visceral arch
between the second and third pouches, (4) the fourth visceral
arch between the third and fourth pouches, and (5) the fifth

vP2 vC..a2

Fig. 100. — Reconstruction of the fore-gut of a chick of 72 hours.

(After Kastschenko.)

Hyp., Hypophysis, lar-tr. Gr., Laryngotracheal groove. Lg.,
Lung. Md. a., Mandibular arch. Oes., Oesophagus, pr'o. G., Preoral
gut. Stom., Stomach. Th., Thyroid, v. C. d, 1, 2, Dorsal division of
the first and second visceral clefts, v. C. v. 2, Ventral division of the
second visceral cleft, v. P. 1, 2, 3, 4, First, second, third, and fourth
visceral pouches.

visceral arch behind the fourth pouch. Each arch is bounded
internally by entoderm, externally by ectoderm. The main portion
of its substance is formed of mesenchyme; each contains also a
branch of the ventral aorta (aortic arch) and a branch of a cranial
nerve. TTnderstanding of their relations is therefore essential to
knowledge of the development of the nervous system, vascular
system, and skull.

We shall now consider the history of each visceral pouch
and arch separately:

The first visceral pouch becomes adherent to the ectoderm
of the first visceral furrow at its dorsal and ventral ends, leaving

176

THE DEVELOPMENT OF THE CHICK

an intermediate free portion. At about the 26 s stage an opening
(cleft) forms at the dorsal adhesion, but none at the ventral;
thus the first visceral cleft is confined to the dorsalmost portion
of the pouch (Fig. 100). This opening closes about the end of
the fourth day; the ventral portion of the pouch then flattens
out, and the dorsal portion expands upwards towards the otocyst

(Fig. 102).

The first visceral (mandibular) arch thickens greatly between
the 14 and 35 s stages, the ventral ends project a little behind
the oral invagination, and subsequently meet to form the primor-
dium of the lower jaw (Figs. 125 and 126, Chap. VII). A pro-

C.oor.

yim. /// ^

VAIJA2 „^.j ^_^^

VS.

<?c?./. '■'■■ -'-■■■ ^,

~ ^

Fig. 101. — Frontal section through the pharynx of a 35 s embryo.

a. a. 1, 2, 3, 4, First, second, third, and fourth aortic arches. Hj-p., An-

terior lobe of the Hypophysis. J., Jugular vein,
branchial portion of pharynx. Ph., Pharj-nx
3, First, second, and third visceral arches.
F. 2, 3, Second and third visceral furrows.

V

or., Oral cavitv. p. br., Post-
Th., Thyroid, v. A. 1, 2,

v. C. 1, First visceral cleft.
V. P. 2, 3, 4, Second, third.

and fourth visceral pouches.
HI, Third cranial nerve.

jection of the upper anterior border just behind the eye is
the beginning of the maxillary process, or primordium of the
maxillary portion of the upper jaw.

The second visceral pouch likewise becomes adherent to the
ectoderm of the second visceral furrow at its dorsal and ventral
ends, and openings are formed in each adhesion by the 35 s stage
(Fig. 100) ; the dorsal opening is small and oval (later becoming
more elongated) while the ventral one is a long, narrow fissure;
they are separated only by a narrow bridge of tissue, and close
during the fourth day.

The third visceral pouch behaves like the second, forming a

FROM TWELVE TO THIRTY-SIX SOMITES

177

small round dorsal, and long fissure-like ventral cleft at about
the 40 s stage (Fig. 102). These close during the fifth day.

The significance of the separate dorsal and ventral divisions of the
visceral clefts is an interesting question. It is probable that the dorsal
division had a special function, as they have a special connection with
the branchial sense organs.

Cdr./.

KPa

— y.Pd.

Fig. 102. — Reconstruction of the pharyngeal organs of the chick
at the end of the fourth day of incubation. (After Kastsch-
enko.)
a. a. 3, a. a. 4, a. a. 6, Third, fourth, and sixth aortic arches.
Car. e., External carotid. Car. i.. Internal carotid. G. Gn., Ge-
niculate ganglion. G. n. X., Ganglion nodosum. G. pr.. Gan-
glion petrosum. ot., Otocyst. p. A., pulmonary artery. Th.,
Thyroid, v. P. 1, 2, 3, 4, First, second, third, and fourth visceral
pouches.

V, VH, VIII, IX, X, XII, Cranial nerves and ganglia.

The fourth visceral pouch connects with the ectoderm at its
dorsal end, about the 35 s stage, but no cleft develops. Its pos-
terior wall develops an evagination (postbranchial body) which
by some is considered to be a rudimentary fifth pouch, and
which contributes to the formation of the thymus. (See
Chap. X.)

178 THE DEVELOPMENT OF THE CHICK

The second visceral arch is the largest of the arches and over-
laps both the first and third. See Figs. 117 and 125 in place of
description. All of the arches are wedge-shaped, corresponding
to the wedge-like form of the hind-brain region. The fourth
arch is small and incomplete ventrally; the fifth a mere transitory
rudiment. The greatest development of the arches is at about
the end of the fourth day.

According to Kastschenko the closure of the visceral clefts takes
place external to the meeting-place of the visceral furrows and clefts,
and in this way some of the ectoderm of the furrows remains attached
to the visceral pouches.

The thyroid arises as a small, spherical evagination of the
epithelium of the floor of the pharynx situated between, and a
little in front of, the ventral ends of the second pair of visceral
pouches (Figs. 85, 87, 88, 101). In the 18-20 s stage, it is repre-
sented by a sharply defined plate of high, columnar cells in the
same situation, which may be recognized even at the stage of
12 s. At the stage of 26 s this plate forms a deep, saucer-shaped
depression, and at the 30 s stage it is a well-developed sac with
wide-open mouth which gradually closes, thus transforming the
sac into a small spherical vesicle lying beneath the floor of the
pharynx (Fig. 102).

The Pulmonary Tract. The portion of the pharynx that
includes the visceral pouches may be called the branchial portion,
because it is homologous to the gill-bearing portion in fishes and
amphibia, and because the visceral pouches are phylogenetic
rudiments of branchial clefts. The larnyx, trachea, and lungs
develop from the ventral division of the postbranchial portion
of the pharynx. At about the 23 s stage a reconstruction shows
this respiratory division of the pharynx slightly constricted from
the broader branchial portion, enlarged on each side at its pos-
terior end and with a ventral depression; the latter rapidly
deepens to form a narrow groove, the primordium of the larynx
and trachea, while the posterior lateral expansion begins to form
outgrowths, the primordia of the lungs and air-sacs. By the
stage of 35 s (Fig. 100) the postbranchial portion of the pharynx
has become narrow transversely and its ventral half is a deep
groove (laryngotracheal groove) leading back to the lung pri-
mordia. A true median sagittal section at this time shows the

FRO:\I TWELA^E TO THIRTY-SIX SO:\IITES

179

floor of the laryngotracheal groove directly continuous with the
floor of the branchial portion of the pharynx at its hind end; the
former bends up at about right angles to enter the narrow
oesophagus (Figs. 87 and 88).

Thus the whole pulmonary tract communicates widely with
the pharynx at the 35 s stage. Its complete delimination falls
within the period covered by Chapter X. The continuity of
the expansions that form the lung primordia, with the series of
visceral pouches as shown in Fig. 100, is especially noteworthy
^s suggesting a theory of the phylogenetic derivation of the lungs.

||f7

a.i.p.

A.

I.ddAcr)
Ld.v.(cduc/)

Fig. 103. — Reconstructions of the liver diverticula of the chick.
(After Hammar.)

A. On the third day of incubation; from the left side; the divertic-
ula arise from the anterior intestinal portal.

B. Beginning of the fourth day; from the left side.

a. i. p., Anterior intestinal portal. D. V., Indicates position of
ductus venosus. g. b., Gall bladder. 1. d. d. (cr.)., Dorsal or cra-
nial liver diverticulum. 1. d. v. (caud.), Ventral or caudal liver
diverticulum, pc. d., Dorsal pancreas. X., Marks the depression in
the floor of the duodenum from which the common bile duct is
formed.

(Esophagus and Stomach. Immediately behind the pharynx,
at the stage of 36 s, the intestine narrows suddenly (primordium
of oesophagus) and enters a small, spindle-shaped enlargement,
the primordium of the stomach (Figs. 87, 88, 100).

The liver arises in the chick as two diverticula of the entoderm
of the anterior intestinal portal, one situated immediately above
and the other below the posterior end of the ductus venosus, or
fork of the omphalomesenteric veins (Fig. 103 A). This portion

180 THE DEVELOPMENT OF THE CHICK

of the anterior intestinal portal becomes incorporated in the
floor of the intestine as the anterior intestinal portal retreats
backwards, and the original dorsal liver diverticulum therefore
becomes anterior or cephalic and the ventral becomes posterior
or caudal (Fig. 103 B). Before this transposition occurs, how-
ever, the diverticula have grown forward towards the sinus
venosus in the ventral mesentery of the stomach, the anterior
diverticulum above and the posterior diverticulum below the
ductus venosus. The stretch of entoderm between the two liver
diverticula thus lies in the angle made by the union of the two
omphalomesenteric veins. At the stage of 26 somites, the anterior
diverticulum has grown forward above the ductus venosus
to the level of the Cuvierian veins and is large and flattened
laterally. The posterior diverticulum is barely indicated at this
time.

The anterior diverticulum was originally described as left and the
posterior as right (Goette, 1867), and this description was taken up
by Foster and Balfour. This was corrected by Felix (1892). Subse-
quent writers do not agree exactly as to the time or precise relations
of the diverticula; however, it is generally agreed that the two diver-
ticula are subdivisions of a common hepatic furrow, inasmuch as the
entoderm between them lies below the level of the entoderm in front
and behind (Fig. 103 B). Brouha maintains that at first the hepatic
furrow lies in front of the anterior intestinal portal, and that the latter
secondarily moves forward so as to include the hepatic furrow, which
later again comes into the floor of the intestine with the definitive retreat
of the anterior intestinal portal. This view does not rest on very secure
evidence, and is probably based on interpretation of slight individual
variations as successive stages of development. Choronschitzky places the
time of appearance of the hepatic diverticula at about the thirty-sixth
hour. It is probable, however, that this is too early. I have found the
first unmistakable diverticulum at a stage of 22 somites, a slight rudi-
ment of the anterior diverticulum in the anterior intestinal portal.

At the 30 s stage the anterior or dorsal diverticulum has ex-
panded much more, mainly to the left of the middle line, as though
to embrace the ductus venosus, and the posterior or ventral
diverticulum has an even greater development and embraces
the right side of the ductus venosus, but it does not extend as
far forward as the anterior diverticulum. Both diverticula
now branch rapidly and profusely, forming secondary anasto-

FROM TWELVE TO THIRTY-SIX SOMITES

181

^■d.d.fcr.)

moses where branches meet, so that a complete ring of anas-
tomosing columns of hepatic cylinders is rapidly formed around
the center of the ductus venosus
(Figs. 103 B and 104, cf. also Figs.
119 and 120). But the anterior
and posterior ends of the ductus
venosus are not yet completely
surrounded by the basket-work of
liver substance, owing to the ab-
sence of any part of the posterior
diverticulum in its anterior por-
tion, and of the anterior divertic-
ulum in its posterior portion.

The floor of the intestine be-
tween the anterior and posterior
liver diverticula is depressed; later
it becomes separated from the
intestinal cavity to form a tem-
porary common bile-duct; which
then receives the tw^o primary di-
verticula (Figs. 103 B, 104 and
187).

The pa7icreas arises from a dor-
sal and a pair of ventral primordia.
The former is an outgrowth of
the dorsal wall of the intestine
immediately above the posterior
liver diverticulum (Figs. 103 B
and 104). At the 35 s stage it is
a solid thickening of the dorsal
wall of the intestine of consider-
able extent; a little later the base
of the thickening is hollowed out,
and the free margin sends off solid
buds into the dorsal mesentery
just behind the stomach. The ventral primordia arise from the
posterior liver diverticulum in a manner to be described later
(Chap. X).

Mid-gut. At the 35 s stage the mid-gut is still open to the
yolk-sac. Its subsequent history is given in Chapter X.

Fig. 104. — Reconstruction of the
liver of the chick at the end of
the fourth day of incubation.
(After Hammar.)

du., Duodenum. L., Substance
of liver. Other abbreviations as
before.

182 THE DEVELOPMENT OF THE CHICK

Anal Plate, Hind-gut, Post-anal Gut, and Allantois. At about
the 14 s stage a thickening of the ectoderm in the middle line
just behind the primitive streak extends towards the entoderm
which is folded up so as to nearly meet it, thus cutting off the
extra-embryonic mesoblast from the primitive streak. The ecto-
derm and the entoderm then come into contact here, and form
a firm union, the anal plate (Fig. 70), which is subsequently
perforated to form the anus. At first, however, the anal plate lies
entirely behind the embryo, and the post-anal portion of the
embryo arises from the thickened remnant of the primitive streak
(tail-bud) which grows backwards over the blastoderm beyond
the anal plate. Even before this, however, the hind-gut begins
to be formed by a fold of the splanchnopleure directed forwards
beneath the tail-bud, and the hind end of the tube thus formed
ends at the anal plate (Fig. 70). The entoderm in front of the
anal tube is fused with the substance of the tail-bud, and as the
latter grows backwards beyond the anal plate it carries with it
a pocket of the hind-gut, and this forms the post-anal gut (Fig.
80).

The formation of the tail brings the anal plate on to the ven-
tral surface of the embr3^o at the junction of tail and trunk, and
the post-anal gut then appears as a broad continuation of the
hind-gut extending behind the anal plate, and ending in the tail
at the hind end of the notochord (Fig. 80). The further elonga-
tion of the tail draws out the post-anal gut into a narrow tube
lying beneath the notochord in the substance of the tail; it
then gradually disappears and leaves no trace.

The formation of the hind-gut takes place prior to the for-
mation of the embryonic body-cavity at this place. It thus
happens that the splanchnic mesoderm, forming the floor of the
hind-gut, is directly continuous with the somatic mesoderm.
When the body-cavity does penetrate this region it is without
direct lateral connections with the extra-embryonic body-cavity,
so that the connection of the splanchnic and somatic mesoderm
persists, forming the ventral mesentery of the hind-gut (Fig. 81).
This is a thick mass of mesoblast binding the hind-gut to the
somatopleure. The hind-gut is deep from the first, and its ven-
tral division soon begins to extend into the ventral mesentery
as a broad evagination, the allantois (see p. 143).

FROM TWELVE TO THIRTY-SIX SOMITES

183

VI. History of the ^Mesoderm

The history of the extra-embryonic mesoderm is considered
sufficiently in the first part of this chapter. The history of the
embryonic mesoderm will be considered under the following
heads: (1) Somites, (2) Intermediate Cell-mass, (3) Vascular
System, (4) Lateral Plate and Body-Cavity, (5) Mesoblast of
the Head.

-"-■'f^^' tr.Am

Fig. lOo. — Embryo of about 27 somites drawn in alcohol by re-
flected light; upper side, x 10.
Am., Amnion, ot., Otocyst. t. F. Am., Tail fold of amnion.

(1) Somites. The rate of formation of the somites from the
segmental plate and their number at different times is given in
the normal table of embryos (p. 68), and may be seen in various
figures of entire embryos. The formation of new somites con-
tinues after the end of the period discussed in this chapter, up
to about the sixth day. Each somite has a definite value in the
developmental history.

184 THE DEVELOPMENT OF THE CHICK

Fig. 106. — The same embryo Irom beiieatli. x lU.

a. i. p., Anterior intestinal portal. A. V., Vitelline artery.
Int., Intestinal groove.

In an embryo of 42 somites (about ninety-six hours), the value of
the somites as determined by their relations and subsequent history
is as follows:
1 to 4. Cephalic; entering into the composition of the occipital region

of the skull.
5 to 16. Prebrachial; i.e., entering into the region between the wing

and the skull.
17 to 19. Brachial.
20 to 25. Between wing and leg.
26 to 32. Leg somites.
33 to 35. Region of cloaca.
36 to 42. Caudal.

IMore somites are fonned later, the maximum number recorded being

FROM TWELVE TO THIRTY-SIX SOMITES

185

52, (see Keibel and Abraham, Xormaltafeln). In an eight-day chick
the number of somites is again about 42, including the four fused with
the skull. Thus the ten somites formed last are again lost. This points
towards a long-tailed ancestr}- for birds.

''Although the somites have the same fundamental structure
in all parts of the body, they differ greatly in many respects"
(Williams). It is not, however, our purpose to consider the indi-
vidual characters of each pair of somites, but rather the relations
common to all.

Each somite is composed of an epithelial wall of high, columnar
cells, enclosing a core of cells that nearly fills the cavity (Figs.
112, 113, etc.). From each somite there arise three parts of
fundamental significance, viz., the sclerotome, the muscle plate,
and the cutis plate (dermatome), the primordium of the axial

Fig. 107. — Transverse section through the last somite of a 29 s embryo.

n. Cr., Neural crest. Neph., Nephrotome. W. D., Wolffian duct. Other
abbreviations as before.

skeleton, the voluntary muscles (excepting those of the head),
and derma respectively. The manner of origin of these parts
may be studied fully in an embryo of 25 to 30 somites, by com-
paring the most posterior somites, in which the process is begin-
ning, with somites of intermediate and anterior positions in the
series, which show" successively later stages.

Figs. 107, 108, 109, and 110 represent transverse sections
through the tw'enty-ninth, tw^enty-sixth, twentieth, and seven-
teenth somites of a 29 s embrvo. In the twentv-ninth somite

186 . THE DEVELOPMENT OF THE CHICK

(Fig. 107) the primitive relations of the parts are still preserved.
In the twenty-sixth somite (Fig. 108) it will be seen that the
cells of the core and of the ventral and median wall of the somite
extending from the nephrotome to about the center of the neural
tube are becoming mesenchymal; they spread out towards the
notochord and the space between the latter and the dorsal aorta.
These cells constitute the sclerotome. The muscle plate extends
from the dorsal edge of the sclerotome to the dorso-median angle
of the w^all of the somite, and the dermatome from this point
to the nephrotome.

/y Cr

■L. /B^Si^"'' "*"'■■"

^h9H^

... S26.

Der/n-

",.# - - '"

g|^^^

:3i ^:. -^c/er

Scler.

_^Bi^

Pfcp.

'-^m^-m$:

' . m

^^^ ^
-1%.

\ %: . ^^.^

Coe.\

'•^^^jBIo : :. v^ ^

Xc.

Coel.

:\^S:^^

^1
Nep/i.

IV.D. '^

Fig. 108. — Transverse section through the twenty-sixth somite of a 29 s
embryo. (Same embryo as Fig. 107.)
Derm., Dermatome. My., Myotome. Scler., Sclerotome. V. c. p., Pos-
terior cardinal vein. Other abbreviations as before.

Fig. 109 is a section through the twentieth somite of the same
embryo. The sclerotome is entirely mesenchymal, and its cells
are extending between the notochord and aorta, and along the
sides of the neural tube. The muscle-plate has now bent over
so that its inner surface is being applied against the dermatome,
but there is still a considerable cavity (myocoele) between the
two, at the lateral angle of the dermo-myotomic plate. The
lateral edge of the dermatome is freed from the nephrotome, and
turns in to a slight extent. Other details are readily understood
from the figure.

The growth of the free edge of the muscle-plate towards the
free lateral edge of the dermatome continues as illustrated in

FROM TWELVE TO THIRTY-SIX SOMITES

187

Vvf-

o

Xs^ii

-^

PI

^

» , .•'-'■''„

-

\\

Ci

^

^

kj, :^

"S:

C-'^^'-
&^-'.^

-c

s

K^

^ ; ' -, -■

*

-li.

O'

6

1—1

o

^■•-H

bl.

^»>

F—H

r/)

rt

V)

o

r^

>^

o

• p-H

c

c3

>

o

>-

^

,-^

c3

X

^

o

l-*-H

,

-i^

c

O

p_l

^^

a;)

f— '

3

o

V)

'J}

w

-i-^

^1

■Ji

— '

r;

o

r*

^^H

a

w

bf)

o

C

u

-^

-r3

.^ -^

o >>

o
o
a;

'^ '^

m O

C O

I <

S f=H

-<

188

THE DEVELOPMENT OF THE CHICK

Figs. 109 and 110, until complete union of the two takes
place (Fig. Ill) and there is established a complete dermo-
myotomic plate in each somite, which therefore includes two
layers: the external cutis-plate or dermatome, and the internal
muscle-plate or myotome. With the elevation of the axis of
the body, the dermo-myotome gradually assumes a nearly vertical
position.

S-A/7?.

G/7 CAo/: ^,

U.S.

Fig. 110. — Transverse section through the seventeenth somite of a 29 s
embryo. (Same embryo as Fig. 107.)
am. Cav., Amniotic cavity. E. E. B. C, Extra-embryonic body-cavity.
Gn., Ganghon. mes'n. V., Mesonephric vesicle. S.-Am., Sero-amniotic con-
nection. Other abbreviations as before.

Other details concerning the early history of the sclerotome
are given in Chapter XIII, and it remains to add here only a short
description of certain changes in the cells of the myotome (mj^o-
blasts). In longitudinal sections the cells of the myotome are
seen to become spindle-shaped soon after the folding towards
the dermatome begins. The nuclei of the myoblasts are large
and stain less deeply than those of adjoining tissues. They
become elliptical in correspondence with the form of the cell-
bodies. Each myoblast soon stretches from anterior to pos-
terior faces of the somite, and this represents the first stage in
the differentiation of the voluntary muscles.

In later stages the myotomes send outgrowths into the limb-
buds and ventral body-wall for the formation of the voluntary

FROM TWELVE TO THIRTY-SIX SOMITES

189

ill

/-S,

o

11

• * •

o

^ t»

— IB

.2

2 >

o
>

73

o

l>

O

190 THE DEVELOPMENT OF THE CHICK

muscles of these parts. The voluntary muscles of the head, on
the other hand (excepting the hypoglossus musculature), arise
in front of the somites; the mesoblast from which they arise is,
however, part of the original paraxial mesoblast, in large part
at least. It is important to note that the voluntary muscles
are epithelial in origin. The involuntary, or smooth, muscle
fibers, on the other hand, are mesenchymal in origin.

The dermatome remains epithelial in all the somites well
into the third day; the cells then begin to separate and form
mesenchyme; this process begins at the anterior somites and
proceeds backwards. The mesenchyme thus formed is the
foundation of the derma.

The Intermediate Cell-mass or Nephrotome. This is the
cord of cells uniting somite and lateral plate; it reaches its typical
development only from the fifth to the thirty-third somites, in
which it contributes to the development of the excretory system.
Behind the cloaca, that is in the region of the tail, there is no lateral
plate and no nephrotome.

Origin of the Excretory System. The history of the excretory
system in Amniota is of particular interest, because it shows a
succession of three separate organs of excretion or kidneys, the
first of which is a mere functionless rudiment, the second is the
principal organ of excretion during embryonic life (at least in
reptiles and birds), and the third finally becomes substituted
for the second, which degenerates and is mostly absorbed;
however, parts of the second remain and contribute to the
formation of the organs of reproduction. The first, known as
the head kidney or pronephros, is probably homologous to the
permanent kidney of Amphioxus; the second or mesonephros,
is the homologue, in part, of the permanent kidney of Anamnia,
and the third or metanephros is the permanent kidney. The
secreting parts of all arise from the intermediate cell-mass, though
not in the same manner. The development of the metanephros
does not begin until the fourth day; it is therefore not considered
in this chapter.

Pronephros and Wolffian Duct. The pronephros extends
over only eleven or twelve somites, viz., from the fifth to the
fifteenth or sixteenth inclusive; it consists originally of as many
parts or tubules as the somites concerned. Each tubule arises
as a thickening of the somatic layer of the intermediate cell-

FROM TWELVE TO THIRTY-SIX SOMITES

191

mass, which grows out towards the ectoderm in the form of a
bUnd, soUd sprout. The distal end of each turns backwards
and unites with the one behind so as to form a continuous cord
of cells, which is thus united with the intermediate cell-mass in
successive somites by the original outgrowths. This cord of
cells is the beginning of the Wolffian duct. Behind the sixteenth
somite, the latter grows freely backwards just above the inter-
mediate cell-mass until it reaches the cloaca with which it unites
about the 31 s stage.

nT. /?C/: cC.

**•-.

5oW

'oel^^^'

jsprpi

Fig. 112. — A. Transverse section through the twelfth somite of a 16 s em-
bryo.

B. Three sections behind A to show the nephrostome of the same pro-
nephric tubule.

V. c. p., Posterior cardinal vein. c. C, Central canal. Ms'ch., mesen-
chyme, n. Cr., Neural crest. N'st. Nephrostome. n. T., Neural tube,
pr'n. 1, 2, Distal and proximal divisions of the pronephric tubule.

The primary pronephric tubules are originally attached to
the nephrotome opposite the posterior portion of the somite,
about half-way between the somite and the lateral plate (Figs.
112 and 113). The part of the nephrotome between the attach-
ment of the primary tubule and the lateral plate is continuous
with the primary tubule and forms a supplementary part of the
complete pronephric tubule; the remainder of the nephrotome
then becomes converted into mesenchyme and the connection
with the somites is lost (Figs. 112 and 113). Thus each pro-
tiephric tubule forms a connection between the Wolffian duct

192 THE DEVELOPMENT OF THE CHICK

and the angle of the body-cavity; it consists of two parts, viz.,
the primary tubule and the supplementary part. It never pos-
sesses a continuous lumen, though there is often a cavity in the
supplementary part, which opens into the body-cavity through
the nephrostome (Fig. 112 B).

The pronephros of the chick is a purely vestigial organ, of
no apparent functional significance. Its development is accord-
ingly highly variable, and it often happens that the right and
left sides of the same embryo do not correspond. It is also of
very short duration and is usually completely lost on the fourth
day. The tubules in the fifth to the tenth somites, moreover.

fi.Gr.

Afj'cA prnJ/SJ
Drhf/4)

Jopl

■: Coe/. \

^"^""^^"^^"^^'^ ^>/

Fig. 113. — Transverse section tlii'ough the fifteenth somite of the same
embryo,
pr'n. (14), (15), Pronephric tubules of the fourteenth and fifteenth somites,
respectively.

hardly pass the first stage when they appear as thickenings of the
somatic layer of the somitic stalk; thus the Wolffian duct does
not extend into this region, and the best developed pronephric
tubules are confined to the tenth to the fifteenth somites.

The pronephric tubules do not form Malpighian corjDuscles;
but glomeruli develop as cellular buds at the peritoneal orifices
of the posterior tubules, projecting into the coelome near the
mesentery. Curiously enough these do not form at the time of
greatest development of the tubules, but subsequently to this
when the tubules themselves are in process of degeneration.
Moreover, they are extremely variable as to number, and degree
of development. They appear to be best developed on the third
and fourth clays. They agree in many respects with the so-called
external glomeruli of the pronephros of Anamnia, and should be

FROM TWELVE TO THIRTY-SIX SOMITES 193

homologized with these. On the other hand, they appear at the
same time as the first glomeruH of the mesonephros (q. v.) and
possess, by way of the intermediate tubules, undeniable resem-
blance to the latter.

At the stage of 10 somites the pronephros is represented by a series
of thickenings of the somatic layer of the intermediate cell-mass extend-
ing from the fifth somite backward to the segmental plate. In an embryo
of 13 somites the connection between the somite and nephrotome is lost,
and the pronephric tubules from the ninth to the thirteenth somites
have united to form the beginning of the Wolffian duct.

In an embryo of 16 somites a single pronephric tubule was found
at the level of the hind end of the fifth somite, and was very distinct
on one side but hardly discernible on the other. Its posterior continua-
tion was soon lost, and the next distinct tubules were between the ninth
and tenth somites ; from here back there was a tubule opposite the hind
end of each somite to the fifteenth, which was the last, and the duct was

continuous.

In an embryo of 21 somites, one finds only isolated remnants of the
pronephros in front of the eleventh somite; from here to the fifteenth
the tubules are well developed and retain their connection both with
the Wolffian duct and the lateral plate. The Wolffian duct extends
back of this place to the region of the posterior half of the segmental

plate.

At the 35 s stage the pronephric tubules are much degenerated,
but the nephrostomes usuafiy remain. In one embryo there was found a
well-developed pronephric tubule on each side in the thirteenth somite.
That of the left side had a wide nephrostome, the lumen of which stopped
short of the tubule; the nephrostome of the right side was rudimentary.
On the right side the Wolffian duct extended no farther forward, but
on the left side it was continued to the eleventh somite, and rudimentary
pronephric strands uniting it to the coelomic epithelium existed in both
eleventh and twelfth somites. Here the Wolffian duct stopped. But
isolated pronephric rudiments and minute nephrostomes were found on
both sides as far forward as the tenth somite.

The Wolffian Duct. The Wolffian duct consists according to
the foregoing account of two parts, (1) an anterior division formed
by the union of the pronephric tubules, and (2) a posterior divi-
sion that arises as an outgrowth of the anterior part. The latter
grows backward above the intermediate cell-mass as a solid
cord (Fig. 107), apparently by active multiplication of its own
cells, without participation of the neighboring mesoderm or

194 THE DEVELOPMENT OF THE CHICK

ectoderm, until it reaches the level of the cloaca at about the
sixtieth hour (30-31 s). It acquires a narrow lumen anteriorly
at about the 25 s stage; but the remainder is solid. At about
the sixtieth hour the ends of the ducts fuse with broad lateral
diverticula of the cloaca, and the lumen extends backwards
until the duct becomes viable all the way into the cloaca (at
about seventy-two hours, 35 s stage).

The Mesonephros or Wolffian Body. The mesonephros de-
velops from the substance of the intermediate cell-mass between
the thirteenth or fourteenth somites and the thirtieth somite.
There are slight local differences in the relations of the tubules
in front and those behind the nineteenth and twentieth somites,
but in general the tubules may be stated to arise as epithelial
vesicles derived from the intermediate cell-mass, which become
transformed into tubules, one end of w^hich unites with the Wolffian
duct and the other forms a Malpighian corpuscle in the manner
described below. It will be seen that the anterior mesonephric
tubules which are relatively rudimentary and of brief duration
overlap the posterior pronephric tubules; they may possess neph-
rostomes, whereas the typical mesonephric tubules formed behind
them, which constitute the main bulk of the mesonephros, never
possess peritoneal connections.

An embryo with 29-30 somites is in a good stage for consid-
ering the early development of the mesonephric tubules. If
one examines a section a short distance behind the last somite,
one finds that the intermediate cell-mass is a narrow neck of
cells uniting the segmental plate and the lateral plate, and that
the cells composing it are arranged more or less definitely in a
dorsal and ventral layer, though some occur l^etween. The
primordium of the Wolffian duct occurs in the angle between
the somatic mesoblast and the intermediate cell-mass, and the
aorta lies in the corresponding angle of the splanchnic mesoblast.
In the last somite (Fig. 107) one finds two important changes:
(1) the intermediate cell-mass is much broader owing to multi-
plication of its cells, and as a consequence the two-layered arrange-
ment is lost; (2) whereas the cells of the intermediate cell-mass
in the region of the segmental plate could not be delimited accu-
rately from either the segmental or lateral plate, it is now easy
in most sections to mark its boundary on both sides. It now
constitutes, therefore^ a rather well-defined but unorganized mass

FROM TWELVE TO THIRTY-SIX SOMITES 195

of cells between the somite and lateral plate, aorta and Wolffian
duct; the posterior cardinal vein appears above the Wolffian duct.

The next change, found to begin in about the twenty-sixth
somite, is a condensation of a portion of the cell-mass lying
median to and below the Wolffian duct (Fig. 108), rendered evi-
dent by the deeper stain in this region; the condensed portion
of the original intermediate cell-mass is not, however, sharply
separated from the remainder, but shades gradually into it both
dorsally and ventrally, so that it can be seen to represent
approximately the central part of the original middle plate. In
view of its prospective function it may be called the nephrogenous
tissue. Following it yet farther forward one finds that it is a
continuous cord of cells with alternating denser and less dense
portions, until in the twentieth somite (Fig. 109), the denser
portions become discrete balls of radially arranged cells. In
the eighteenth and seventeenth somites (Fig. 110) these become
small thick-walled vesicles, which are situated median and ventral
to the duct. Each vesicle is the primordium of a complete
mesonephric tubule. Farther developed tubules are found in the
fifteenth and sixteenth somites, and it is probable that the
nephrogenous tissue forms mesonephric tubules in the four-
teenth, thirteenth, and perhaps yet more anterior segments.

The formation of the tubules proper from the vesicles may
be studied satisfactorily in a 35 s embryo (seventy-two hours).
In the twenty-third somite of such an embryo the nephrogenous
tissue and the nascent tubules lie median to the Wolffian duct
and below the median margin of the cardinal vein (Fig. 111).
The Wolffian duct is triangular in cross-section w^ith its longest
and thinnest side next the coelome. The most advanced vesicle
in this region possesses a hollow sprout extending laterally to the
Wolffian duct with which it is in close contact; this is the pri-
mordium of the tubular part of the mesonephric tubule (cf. Fig.
114 A and B). In more anterior somites it is found that such
sprouts have fused with the wall of the duct in such a manner that
the lumen of the tubule now communicates with that of the duct.

Simultaneously the median portion of the original vesicle
has been transformed into a small Malpighian corpuscle in the
following manner: it has first become flattened so that the lumen
is reduced to a narrow slit; then this double-layered disc becomes
concave with the shallow cavity directed posteriorly and dorsally;

196

THF DEVELOPMENT OF THE CHICK

at the same time the convex wall becomes thin, and the concave
thick. The entire tubule thus becomes S-shaped. Figs. 114 A,
B, C, D illustrate the corresponding processes in the duck, which
are similar in all essential respects to the chick.

B

• r

C D

Fig. 114. — From a transverse series through a duck embryo of 45 s, to
show the formation of the mesonephric tubules. (After Schreiner.)
Fig. 218 shows the position of the sections A, B, and C.
V. c. p., Posterior cardinal vein. W. D., Wolffian duct.
A. and B. represent tubules of the twenty-ninth segment.

C. of the twenty-seventh segment.

D. of the twenty-fourth segment.

In the chick embryo of 35 somites the only differentiated
tubules are in front of the twentieth somite, a region of the
mesonephros that never develops far, and such tubules do not
appear ever to become functional. In the region of the subse-
quent functional mesonephros (twentieth to thirtieth somites) the
development has not progressed beyond the stage of the vesicles
showing the first indications of budding.

FROM TWELVE TO THIRTY-SIX SOMITES 197

The main part of the mesonephros is thus between the twen-
tieth and thirtieth somites. In the anterior half of this region
three or four rudiments of tubules are formed in each somite by
the seventy-second hour. Subsequently five or six tubules are
formed in each segment between the twentieth and thirtieth.
Tubules are formed first from the ventral portions of the neph-
rogenous tissue (see Fig. Ill); those formed later arise from
the unused portions. There is no evidence that they ever arise
in any other way. The tubules may thus be divided according
to the time of origin into primary, secondary and tertiary sets,
but there is no morphological or functional distinction between
the successive sets. (See Chap. XII.)

The collection of tubules causes a projection or fold on each
side of the mesentery into the body-cavity, known as the Wolffian
body, the detailed history of which is given in Chapter XII.

In conclusion it should be noted that the most anterior tubules
of the Wolffian body possess peritoneal funnels like the pronejDhric
tubules. Thus in an embryo of 30 somites I have noticed open perito-
neal funnels in the eighth, ninth, twelfth, thirteenth, fourteenth, fifteenth,
sixteenth, and seventeenth somites. It seems quite certain that the
last of these belong to the mesonephros, though the most anterior are
undoubtedly pronephric rudiments. In the eighteenth, nineteenth,
twentieth, and twenty-first somites, small depressions of the peritoneum
were noticed opposite tubules, but not communicating with them.

The Vascular System. Soon after the thirty-third hour the
heart begins to twitch at irregular intervals, and by the forty-
fourth hour its beatings have become regular and continue unin-
terruptedly. The contraction proceeds in the form of a rapid
peristaltic wave from the posterior to the anterior end of the
cardiac tube, and the blood, already present, is forced out in
front. Through the aortic arches it reaches the dorsal aorta
which distributes part to the body of the embryo, but most of
the blood enters the vascular netv/ork of the yolk-sac. It is
returned to the heart by various veins in the yolk-sac and em-
bryo, and recommences the circuit.

The development of the vascular system will be more readily
understood if we preface the account with a brief description of
the anatomy of the system early in the fourth day (Fig. 115,
cf. also Figs. 135 and 136).

The heart consists of four chambers, viz., the sinus venosus,

198

THE DEVELOPMENT OF THE CHICK

the atrium^ the ventricular loop, and the bulbus arteriosus (Fig.
116).

The truncus arteriosus lies in the floor of the pharynx and
gives off the following vessels: (1) a short branch, the external
carotid, extending into the mandibular arch; (2) complete arches
in the second, third, and fourth visceral arches which join the

Fig. 115. — The circulation in the embryo and yolk-sac between the eightieth
and ninetieth hours of incubation, drawn from a photograph by A. H. Cole.
The arteries are represented in solid black; the veins in neutral tint. A
fold of the yolk-sac covers the fore part of the head,
a. a. 2, .3, 4, Second, third, and fourth aortic arches. Ao., Aorta. Atr.,
Atrium. B. a., Bulbus arteriosus. Car. ext., External carotid. Car. int.,
Internal carotid. D. C, Duct 'of Cuvier. D. V., Ductus venosus. J., Jugu-
lar vein (anterior cardinal). 1. a. V., Left anterior vitelHne vein. p. V.,
Posterior vitelHne vein. S. V., Sinus venosus. V. c. p.. Posterior cardinal
vein. Ven., Ventricle. V. O. M. L., Left omphalomesenteric vein.

FROM TWELVE TO THIRTY-SIX SOMITES 199

dorsal aorta; these are known as the second, third, and fourth
aortic arches; the third arch is the largest.

The original mandibular aortic arches unite with the anterior ends
of the dorsal aortse, forming a loop on each side at the base of the fore-
brain (Fig. 93), and they have, therefore, a different relation from the
other aortic arches; it seems probable also that they have a different
morphological value. The ventral limb of this loop disappears in its
pre-oral part after this stage and a new vessel is formed entirely within
the mandibular arch, bearing the same relation to the visceral arch as
the other aortic arches. At the stage of 35 somites it is a complete arch, in
some embryos at least (Fig. 117), though of very small caliber and very
transitory, possibly sporadic, in its occurrence. It is possible that this
is the true mandibular arch, and the pre-oral portion of the original
mandibular arch should have another interpretation. Kastschenko
suggests that it may have been related to lost pre-mandibular gill-
clefts.

The roots of the dorsal aorta above the pharynx receive the
aortic arches and are continued forward as the internal carotid
arteries, branching in the fore part of the head. Posteriorly the
right and left aortic roots unite just behind the fourth visceral
pouch to form the dorsal aorta, and this continues as an undi-
vided vessel to about the level of the twenty-second somite,
where it divides into right and left dorsal aortse, and at the
same time sends out a large omphalomesenteric artery into the
yolk-sac on each side, and these branch as shown in Figure 115 into
the capillary network of the yolk-sac. The dorsal aortse, now
much diminished in size, continue back into the tail where they
are known as the caudal arteries. The dorsal aorta also sends off
a pair of segmental arteries into each intersomitic septum, and a
pair of small allantoic (umbilical) arteries into the primordium of

the allantois.

The veins enter the heart through three main trunks: (1) the
ductus venosus, (2 and 3) the paired ducts of Cuvier. These
are made up as follows: (1) the ductus venosus is formed at the
level of the posterior liver diverticulum by the right and left
omphalomesenteric veins, which arise in the yolk-sac by union
of the capillaries of the vascular area; the right vitelline vein
also receives two veins coming directly from the anterior and
posterior ends respectively of the sinus terminalis, the anterior
of these is frequently partly double owing to its mode of origin.
(See beyond. Chap. VII.) The vascular area in the yolk-sac thus

200 THE DEVELOPMENT OF THE CHICK

appears strikingly bilateral at this time. (2 and 3) The ducts of
Ciivier are made up by the union of all the somatic veins. Each
is formed primarily by the union of the anterior and posterior
cardinal veins. The anterior cardinal vein receives all the blood
of the head, and thus includes the first three segmental veins.
It also receives at its point of junction with the posterior cardinal
vein a branch from the floor of the pharynx, the external jugular
vein. The posterior cardinal vein receives (1) all the segmental
veins of the trunk, of which there are twenty-nine pairs, running
in the intersomitic septa between the fourth and thirty-third
somites, and the veins of the Wolffian body of which there are
several to each somite concerned, as described in the account
of that organ.

The development of the vascular system up to the stage just
described will now be taken up.

Developmeiit of the Heart, (a) Changes in the External Form.
In the last chapter we traced the origin of the heart up to the
time when it is a practically straight, undivided, somewhat
spindle-shaped tube lying below the floor of the pharynx, to which
it is attached by its dorsal mesentery (mesocardium). Posteriorly
its cavity divides into the omphalomesenteric veins which run
in the side-walls of the anterior intestinal portal. The heart is
lengthened backwards by the concrescence of the omphalo-
mesenteric veins and the most posterior division of the heart
(the sinus venosus) is established in this way between the stages
of 12 and 18 somites; it is marked by a broad fusion with the
somatopleure (mesocardia lateralia) through which the ducts of
Cuvier enter the heart.

At the stage of sixteen somites the duct of Cuvier lies opposite
the hind end of the second somite on the right side, and a little farther
back on the left side; and the somato-cardiac fusion (mesocardium
laterale) in which it lies is of the width of about one and a half somites.
On the right side the duct of Cuvier lies a little in front of, and on the
left side a little behind, the point of union of the omphalomesenteric
veins; thus the posterior end of the heart is not fully formed at the
stage of 16 s, but is at the stage of 18 s. The subsequent fusion of the
omphalomesenteric veins produces the so-called ductus venosus, or
main splanchnic vein, which is therefore a posterior continuation of the
sinus venosus.

The cardiac tube proper lies between the origin of the aortic

FROM TWELVE TO THIRTY-SIX SOMITES 201

arches at the anterior end and a point a Uttle behind the entrance
of the ducts of Cuvier into the heart at the posterior end.

Two main changes characterize the development of the heart
in the period under consideration: (1) folding of the cardiac tube
and (2) differentiation of its walls in successive regions to form
the four primary chambers of the heart, viz. (from behind for-
wards), the sinus venosus, the auricular division (atrium), the
ventricular division and the bulbus arteriosus.

The folding of the heart is caused by the rapid growth between
its anterior and posterior fixed ends, and the places of folding
are determined largely by differences in the structure of the walls
at various places. The folding begins by a curvature to the
right, and this proceeds until the tube has an approximately
semicircular curvature (Fig. 72). At a certain place in the
curved tube a very pronounced posterior projection takes place
(Figs. 73 and 74), and at the same time this bent portion turns
ventrally; the apex of the bend represents the future apex of the
ventricles. The continuation of these two directions of folding
then brings the ventricular division of the heart immediately
beneath the sinu-auricular division which is attached dorsally
by the somato-cardiac connections; further continuation brings
the apex of the heart a little behind the auricular portion (Figs.
85, 87, 88, 93, 99). During all this period the distance between
the two fixed ends has remained practically constant.

During the process of folding, constrictions have arisen
between successive portions of the cardiac tube, owing to expan-
sion of intervening portions, and thus at the stage of seventy-two
hours the heart shows the following divisions and form. From
the dorsal surface (in a dissection, Fig. 116) one sees (1) the sinus
venosus, broad behind and narrow in front where it joins the
auricular division; it receives three veins: (a) the large ductus
venosus, appearing as a direct posterior continuation of the sinus,
and separated from it by only a slight constriction; and (6 and c)
the right and left ducts of Cuvier entering the sinus laterally
and dorsally near its enlarged posterior end; (2) the sinus enters
the atrium through the dorsal wall; the atrium shows two lateral
expansions, the future auricles, of which the left is much the
more expanded at this time; the sinus appears partly sunk in
the right auricle. (3) Only the right limb of the ventricular
loop is visible from the dorsal surface at this time, and is separated

202

THE DEVELOPMENT OF THE CHICK

from (4) the bulbus arteriosus by a slight constriction. The
biilbus thus Hes on the right side; it sweeps around the atrium
anteriorly to the middle line and then bends up to enter the floor
of the pharynx.

From the ventral side one sees the looped ventricular division

behind, in which we distinguish
right and left limbs, the former
of which enters the bulbus in
front, and the latter the auricles.
These two limbs represent ap-
proximately the future right
and left ventricles (Fig. 198,
Chap. XII).

In an ordinary entire mount
of this stage the heart is seen
from the right side, and the dis-
position of the parts may be
readily understood by reference
to Fig. 117, and the preceding
description.

Another change that should
be noted here is the disappear-
ance of the mesocardium during
the folding of the cardiac tube,
except in the region of the
sinus venosus where it remains
permanently and becomes much
broadened (seventy-two hours).

(6) Changes in the Internal Structure of the Heart. We have
already seen that the heart consists of two primary layers, viz.,
the endocardium, which is endothelial in nature, and the myo-
cardium, which is derived from the splanchnic mesoblast. The
distinction between the sinu-auricular and the bulbo-ventricular
divisions of the heart is indicated internally at about the time
the first external evidence is seen, by the fact that the endocar-
dium is more closely applied to the myocardium in the former
than in the latter division. In the sinus and atrium but little
change takes place in the period under consideration. In the
ventricle, on the other hand, and especially in the right limb,
the wide space originally existing between endocardium and

Fig. 116 . — Heart of a chick embryo

of 72 hours, dissected out and drawn

from the dorsal surface.

Aur. 1., Left auricle. Aur. r., Right
auricle. B. a., Bulbus arteriosus.
D. C. r. 1., Right and left ducts of
Cuvier. D.V., Ductus venosus. S.V.,
Sinus venosus. Tr. a., Truncus arte-
riosus. V. r., Right limb of ventricle.

FROM TWELVE TO THIRTY-SIX SOMITES 203

myocardium becomes more or less filled by multiplication of
the endocardial cells. On the side of the myocardium there is
first a thickening, and then anastomosing processes are sent out
towards the endocardium. Cavities also arise within the thick-
ened myocardium and all communicate. The endocardial cells
then form a covering to all myocardial processes and cavities,
and the cavities thus lined communicate with the main endo-
cardial cavity. Thus the wall of the ventricles becomes spongy
and all the cavities in it are lined by a layer of endocardium
and communicate with the endocardial cavity. In the bulbus
finally there is a great thickening of the endocardium produced
by multiplication of its cells, but no corresponcUng change in
the myocardium; thus the bulbus at seventy-two hours shows
a thin myocardial and a thick endocardial wall. The later
development is described in Chapter XII.

The Arterial System. The description of the development of
the arterial system proceeds from the stage of 12 somites described
in the last chapter.

The primitive vascular system of vertebrate embryos is a
capillary netw^ork in all parts of the blastoderm and of the
embryo. Main trunks arise by development of parts of the
network corresponding to the rate and direction of embryonic
growth and thus answering to the vascular needs of growth.
The vascular system forms at all stages a continuous endothelial
tree whose primitive form in all parts is a capillary network.
This idea, which we owe originally to Aeby, has been worked out
in a masterly way by H. M. Evans. (See lit. Chap. V.)

The Aortic Arches. An arch of the aorta is formed in each vis-
ceral arch; they arise successively as buds from the roots of the dor-
sal aorta in the order and time of formation of the visceral arches.
Thus the first or mandibular aortic arch is formed at the stage of
9-10 somites; the second or hyoicl aortic arch arises from the dor-
sal aorta at about the stage of 19 s and joins the ventral aorta at
about the 24 s stage. The third is completely formed at the stage
of 26 somites. The fourth is completely formed at the stage of 36
somites; and the fifth and sixth arise during the fourth and fifth
days. (See Chap. XII for account of the fifth and sixth arches.)

204 THE DEVELOPMENT OF THE CHICK

The first aortic arch loses its connection with the dorsal aorta
at about the stage of 30 somites, and the second arch similarly
during the fourth clay; the ventral ends of these arches retain
their connection with the ventral aorta and constitute the begin-
ning of the external carotid. Thus the third, fourth, fifth and
sixth aortic arches remain. Their transformation belongs to the
subject-matter of Chapter XII.

The ^pulmonary artery appears as a posterior prolongation of
the ventral aorta on each side at about the 35 s stage. It thus
appears successively in later stages as a branch from the base of
the fourth and sixth aortic arches.

The Internal Carotids. The loop where the mandibular arch
joins the dorsal aorta may be called the carotid loop; it is situated
in front of the oral plate at the base of the fore-brain on each
side (Fig. 93). It enlarges to form a sac, and when the connec-
tion with the mandibular arch is lost, sends out branches into
the tissue surrounding the brain. These are of course a direct
continuation of the dorsal aorta on each side.

The segmental arteries are paired branches of the dorsal aorta
in each intersomitic septum. They pass dorsally to about the
center of the neural tube and arch over laterally to enter the
segmental veins, and thus unite with the cardinal veins.

The Development of the Venous System. The main outlines
of the development of the venous system have been already
considered.

The somatic veins, i.e., the anterior and posterior cardinal
veins and their branches, enter the sinus venosus through the
ducts of Cuvier. The original position of this duct as we have
seen is about the level of the second somite. The formation of
the cervical flexure, however, carries a number of somites forward
above the heart, so that at about the stage of 32 s it comes to
lie in the region of the eighth and ninth somites. The relation
betw^een the somatopleure and the heart in this region has been
already described.

The anterior cardinal veins are the great blood-vessels of the
head, and become the internal jugulars in the course of develop-
ment. Owing to the order of development of the body, the
anterior cardinals are formed before the posterior cardinals. At
the 15-16 s stage they lie at the base of the brain, dorsal and
lateral to the dorsal aortse, and extend forward to the region of

FROM TWELVE TO THIRTY-SIX SOMITES 205

the diencephalon. They he internal to the cranial nerves and
pass just beneath the auditory pits.

As the brain develops many branches of the anterior cardinal
veins arise, the most conspicuous of which at seventy-two hours
are a large branch just behind the auditory sac, one between the
auditory sac and the trigeminal ganglion, an ophthalmic branch
extending along the base of the brain to the region of the optic
stalks and a network of vessels on the lateral surfaces of the
fore-brain. The other branches of the anterior cardinal vein
are the three anterior intersomitic veins (Fig. 115); the external
jugular from the floor of the pharynx enters the duct of- Cuvier
just beyond the union of the anterior and posterior cardinal veins.

Up to about forty-eight hours the anterior cardinal veins lie
median to the cranial nerves, but between this time and seventy-
two hours the facial and glossopharyngeal nerves cut completely
through the vessel and thus come to lie median to it; the trigem-
inus and vagus continue to lie lateral to it.

The posterior cardinal arises as a posterior prolongation from
the duct of Cuvier and grows backward above the Wolffian duct,
keeping pace with the differentiation of the intermediate cell-
mass, as far as the thirtv-third somite. It does not enter the
caudal region of the body. As already described it receives
twenty-nine intersomitic veins and the veins of the Wolffian
bodv. At first its connection with the duct of Cuvier is by
means of a network of vessels, which gradually gives place to a
single trunk (cf. Fig. 117).

The Splanchnic Veins. The ductus venosus is the unpaired
vein immediately behind the sinus venosus, formed by fusion of
the two omphalomesenteric veins. It is fully formed at the stage
of 27 somites. Its relations to the liver have already been de-
scribed in connection with that organ. Its subsequent changes
are described in Chapter XII.

The vitelline veins are united at about the stage of seventy-
two hours by a loop passing over the intestine immediately
behind the pancreas. (See Chap. XII.)

YII. The Body-cavity and Mesenteries

The origin of the dorsal and ventral mesenteries was con-
sidered in the section of this chapter dealing with the ali-
mentarv canal. As noted there, the dorsal mesentery extends

206

THE DEVELOPMENT OF THE CHICK

IZS-M G>?V ~~
IZ \ MM \ OpA/j^Jc/f /s/A

y.umi.

Fig. 117. — Entire embryo of 35 s, drawn as a transparent object.
a. a. 1, 2, 3, 4, First, second, third, and fourth aortic arches. Ar.,
Artery. A. V., ViteUine artery, cerv. FL, Cervical flexure, cr. Fl.,
Cranial flexure. D. C, Duct of Cuvier. D. V., Ductus venosus.
Ep., Epiphysis. Gn. V., Gantrlion of trigeminus. Isth., Isthmus.
Jug. ex.. External jugular vein. Md., Mandibular arch. M. M.,
Maxillo-mandibular branch of the trigeminus, olf. P., Olfactory pit.
Ophth., Ophthalmic branch of the trigeminus. Ot., otocyst. V.,
vein. W. B., Wing bud. V. c. p., Posterior cardinal vein. V.
umb.. Umbilical vein. V. V., Vitelline vein. V. V. p., Posterior vitel-
line vein.

FROM TWELVE TO THIRTY-SIX SOMITES 207

the entire length of the ahmentaiy canal, while the ventral
mesentery persists only in the region of the fore-gut and the
cloaca.

The embryonic body-ca\dty shows two divisions from a Yery
early stage, viz., (1) the large cephalic or parietal cavity situated
in the pharyngeal region of the head and containing the heart,
and (2) the general pleuroperitoneal cavity of the trunk. After
the heart is established in the middle line the parietal cavity
is bounded posteriorly by the wall of the anterior intestinal portal
(Figs. 75, 85, etc.), but it communicates with the pleuroperi-
toneal cavity around the sides of the portal, in which the vitelline
veins run. Laterally the parietal cavity communicates with the
extra-embryonic body-cavity.

The mesocardia lateralia are also an important landmark in
the embryonic body-cavity because from them proceed the par-
titions that subsequently separate the pericardial and pleural
cavities on the one hand, and the pleural and peritoneal body-
cavities on the other. (See Chap. XI.) The primordium of the
lateral mesocardia may be recognized in the 10 s stage : just behind
the heart the median portion of the body-cavity is thick-walled,
the peritoneal cells being actually columnar. At this place, a
short distance lateral to the median angle of the body-cavity,
and at the junction of the cylindrical and flat mesothelium, a
fusion of considerable longitudinal extent is formed between
the somatopleure and the proximal portion of the vitelline veins,
projecting up from the splanchnopleure; this fusion is the begin-
ning of the lateral mesocardiam. It separates a more median
portion of the body-cavity from a more lateral, and in it the
duct of Cuvier soon develops.

When this portion of the body of the embryo becomes ele-
vated (forty to fifty hours) the portion of the body-cavity lateral
to the mesocardia lateralia comes to lie ventrally to the median
portion (cf. Fig. 69), and at the same time the lateral mesocardia
rotate around a longitudinal axis through an angle of about
90°, so that the original median border becomes dorsal, and the
original lateral border becomes ventral. The dorsal divisions,
right and left, of the pleuroperitoneal cavity may now be called
the pleural grooves. Inasmuch as the parietal cavit}^ has receded
considerably at the same time into the trunk with the elongation
of the fore-gut, it comes to lie beneath the pleural grooves

208

THE DEVELOPMENT OF THE CHICK

instead of in front of them as before. Therefore in cross-sections, in
front of the lateral mesocardia, the pleural grooves appear as dorsal
projections of the parietal (later pericardial) cavity, separated from
one another in the middle line by the oesophagus (Fig. 118).

The relations of the three divisions of the embryonic body-
cavity thus established may be described as follows: the parietal
cavity contains the heart, and is therefore the prospective peri-

CA

yof-

m.

1^

^■t.dors-

Fig. 118. — Transverse section of an embryo of 35 s, imme-
diately in front of the lateral mesocardia.
Ao., Aorta. Atr., Atrium. B. a., Bulbiis arteriosus. D.C.
r , and'l., Ri^ht and left ducts of Cuvier. Lg., Lung, m's'c.
dors., Dorsal' mesocardium. m's't. dors., Dorsal mesentery.
P. C, Pericardial cavity, pi. gr., Pleural groove. Rec. pul.
ent., Recessus pulmo-entericus. S. V., Sinus venosus.

cardial cavity. It is not, however, a closed cavity, but communi-
cates in front of the lateral mesocardia with the pleural grooves
(Fig. 118), and by way of the latter above the lateral mesocardia
with the peritoneal cavity (Figs. 119 and 120); a second communi-
cation of the parietal cavity with the peritoneal cavity is beneath
the lateral mesocardia around the sides of the anterior intestinal
portal, now being converted into the septum transversum (cf.

FROM TWELVE TO THIRTY-SIX SOMITES

209

Fig. 120). A more complete description of the cavities is given
in Chapter XI.

The median wall of the pleural grooves forms much mesoblast
during the formation of the lung diverticula, and thus initiates
the formation of lobes enclosing the lungs (Figs. 118 and 119).
These lobes descend ventrally and unite with the septum trans-
versum (see below), thus producing blind bays of the coelome

yri6-tdor6'-

\

\

'rv'st.irQTl.

v5.K

/

Fig. 119. — Transverse section of the same embryo through the
lateral mesocardia.

Liv., Liver, m's'c. lat., Lateral mesocardium. m's't. access
Accessory mesentery, m's't. ven., Ventral mesentery. Other
abbreviations as before.

at the sides of the oesophagus, known as the superior recesses
of the peritoneal cavity or pulmo-enteric recesses.

The ventral mesentery extends from the anterior end of the
sinus venosus to the hind end of the fore-gut, where it unites
with the ventral body-wall. It includes the sinus venosus and
the ductus venosus, together with the hepatic diverticula. The
median and lateral mesocardia, together with the ventral mesen-
tery of the fore-gut, form a mass known as the septum transversum.

210

THE DEVELOPMENT OF THE CHICK

At the stage of seventy-two hours, then, the pleural, pericar-
dial and peritoneal divisions of the body-cavity are indicated,
but all are in communication. The pleural cavities connect
with the peritoneal cavity posteriorly, and with the pericardial
cavity anteriorly in front of the lateral mesocardia (Figs. 118, 119,
120); and the pericardial cavity communicates also with the

.-r^ffS

m'6'c'.d.

i~Mjrc

4%./,

SACJ,.'4-,>Vv.»''^'^:~-=rj

Fig. 120. — Transverse section of the same embryo immediately
behind the lateral mesocardia.
ant. hep. Div., Anterior hepatic diverticulum. Duod., Duo-
denum. End'c, Endocardium. D. V., Ductus venosus. My'c,
Myocardium. PI. m's'^., PHca mesogastrica. S-am., Sero-am-
niotic connection, ven. r., 1., Right and left limbs of the ven-
tricle. V. umb., Umbilical vein.

peritoneal cavity beneath the lateral mesocardia around the
roots of the vitelline veins (sides of the anterior intestinal portal).
Thus the ducts of Cuvier and the vitelline veins are the agencies
that introduce the separation of the body-cavities.

The tail-fold forms blind coelomic pockets in the region of
the hind-gut, which end in the region of the thirty-third somite.
(Of. Fig. 81.)

PART II

THE FOURTH DAY TO HATCHING
ORGANOGENY, DEVELOPMENT OF THE ORGANS

CHAPTER VH

THE EXTERNAL FORM OF THE EMBRYO AND THE

EMBRY^ONIC MEMBRANES

L The External Form

General. The development of the external form of the em-
bryo is conditioned by the order of development of the organs.
The early form is thus given by the nervous system, somites

A B

Fig. 121. — A. Embryo of 3 days' and 16 hours' incubation, x 5.

B. Embryo of 5 days' incubation, x 5. (After Keibel and Abra-
ham.)

and viscera. The development of muscles, bones, limbs, etc., that
define the form of the fowl, begins relatively late, and only gradu-
.ally conceals the outlines of the internal parts.

Figs. 121 to 124 illustrate the development of the external

211

212

THE DEVELOPMENT OF THE CHICK

form from three days sixteen hours to ten days,
(three days sixteen hours) the form of the head
the brain, eyes, and visceral arches. The cerv
strongly marked. There is no neck. The heart
protuberance immediately behind the head. The
rounded swellings. In Fig. 121 B (five days one
vical flexure is less marked; the enlargement of

In Fig. 121 A
is defined by
ical flexure is
makes a large
limb-buds are
hour) the cer-
the mid-brain

Fig. 122. — Embryo of 7 days' and 7 hours'
incubation x 5. (After Keibel and Abra-
ham.)

makes a more pronounced protuberance of the head in this region;
the heart has retreated farther back into the thorax, and the
neck is thus indicated. The main divisions of the limbs are
beginning to appear. In Fig. 122 (seven days seven hours)
there are marked changes: The cervical flexure is practically
lost. The elevation of the head and retreat of the heart into
the thorax have produced a well-marked neck. The upper

EMBRYO AND EMBRYONIC MEMBRANES

213

portion of the first visceral cleft alone is visible as the external
auditory meatus; the other visceral arches and clefts have prac-
tically disappeared, excepting the mandibular arch, forming the
lower jaw. The abdominal viscera begin to protrude. Feather
germs have appeared in definite tracts. In the next stage, Fig.
123 (eight days), the contours of the body are decidedly bird-

FiG. 123. — Embryo of 8 days x 5. (After Keibel and Abraham.)

like; the fore-limbs are wing-like. The contours of the head
are much smoother, and determined more by the development
of the facial region and skull than by the brain. The protuber-
ance of the ventral surface caused by the viscera is strongly
marked. Fig. 124 finally shows a ten-day embryo.

Head. The embryonic development of the head depends on
the changes in three important classes of organs, together with

214 THE DEVELOPMENT OF THE CHICK

their supporting and skeletal structures and accessory parts:
(a) the central nervous system, (6) the organs of special sense,
and (c) the visceral organs, mouth and pharynx. The origin of
all these parts has been considered, and it is proposed to take

/

y

^^■i

//

^-

\
•^

<^

Fig. 124. — Embryo of 10 days and 2 hours x 5. (After Keibel and Abraham.)

up here only the development of the external form of the head.
The preceding section gives an account sufficient for our present
purposes, except in the case of the facial region. At four days
this region appears as follows (Fig. 125): the mouth is a large,
ill-defined opening, bounded behind by the mandibular arches,

EMBRYO AND EMBRYONIC MEMBRANES

215

at the side by the maxillary processes, and in front by the naso-
frontal process, which is a broad projection below the cerebral
hemispheres overhanging the mouth. On each side of the naso-
frontal process are the olfactory pits, the cavities of which are
continuous with the oral cavity. Lateral to the olfactory pits
are the external nasal processes, abutting against the eye and
separated from the maxillary process by the lachrymal groove.
The portion of the naso-frontal process bounding the olfactory
pits on the median sides may be called the internal nasal process.

E.p.

na5:Fr. /
Olf.

/Hem.

■ A

/

Im.jjr.- — ^-<f^- . ""x^^

—Or.

y^^ '^:::^^

^i^-^-Ph.

Md. -^— ^C^

.J

' ^^' "' Z

\

vA.d ■ "^

Fig. 125. — Head of an embryo of 4 days' in-
cubation, from the oral surface (N. L. 6
mm.)

Ep., Epiphysis. Hem., Cerebral hemi-
sphere. Hy., Hyoidarch. 1. nas. pr., Lateral
nasal process. Md., Mandibular arch. Mx.,
Maxillary process, nas.fr., Naso-frontal pro-
cess. Olf., Olfactory pit. Or., Oral cavity.
Ph., Pharynx, v. A. 3, Third visceral arch.

During the fourth and fifth days a fusion is graduall}' formed
between the internal nasal process on the one hand, and the
external nasal and maxillary processes on the other (Fig. 126),
thus forming a bridge across the open mouth of the olfactory
pits and dividing the openings in two parts, one within the oral
cavity, which becomes the internal nares or choanae, and one
without, which becomes the external nares or nostrils. During
the same time ihe whole naso-frontal process begins to project

216 THE DEVELOPMExXT OF THE CHICK

forward to form the tip of the upper jaw. The two mandibular
arches have also fused in the middle line and begin to project
forward to form the lower jaw. This projection of upper and
lower jaw causes a great increase in the depth of the oral cavity
(Fig. 148).

The upper jaw is thus composed of three independent parts:
vdz., the median part formed from the naso-frontal process and

■ — .-^.*>»**

\

Fig. 126. — Head of an embryo of about 5 days

from the oral surface. (N. L. 8 mm.)

ch. F., Choroid fissure. E. L., Eye-lid (nic-
titating membrane), ex. nar., External nares.
1. Gr., Lachrymal groove. Other abbreviations
as before.

the two lateral parts formed from the maxillary processes. The
former becomes the intermaxillary and the latter the maxillary

region.

II. Embryonic Membranes

General. The extension of the blastoderm over the surface
of the yolk goes on very rapidly up to the end of the fourth day
of incubation (Fig. 33), at which time there is left a small cir-
cumscribed area of uncovered yolk, that may be called the
umbilicus of the yolk-sac, which remains uncovered for a long
time. Its final closure is associated with the formation of the
albumen-sac.

EMBRYO AND EMBRYONIC MEMBRANES 217

The splitting of the mesoblast of the blastoderm is never com-
plete ; but on the contrary the undivided margin begins to thicken
after the fourth day, and gradually forms a ring of connective
tissue that surrounds the umbilicus of the yolk-sac (Figs. 128 and
129). When this ring closes, about the seventeenth day, it forms
a mass of connective tissue uniting the yolk-sac and albmnen-sac.
(See below.)

During the first few days of incubation the all^umen loses
water rapidly, and becomes more viscid, settling, as this takes
place, towards the yolk-sac umbilicus. Thus the amniotic sac
containing the embryo lies above; beneath the amniotic sac comes
the volk, and the main mass of the albumen lies towards the
caudal end of the embryo (Figs. 128 and 129).

The allantois expands very rapidly in the extra-embryonic
body-cavity, and the latter extends by splitting of the mesoblast
into the neighborhood of the yolk-sac umbilicus. When the
allantois in its expansion approaches the lower pole of the egg,
it begins to wrap itself around the viscid mass of the albumen
accumulated there. In so doing, it carries with it a fold of the
chorion, as it must do in the nature of the case, and thus the
albumen mass begins to be surrounded by folds of the allantois
with an intervening layer of the duplicated chorion. These
relations will be readily understood by an examination of the
accompanying diagrams (Figs. 128 and 129). In this way an
albumen-sac, which rapidly becomes closed, is established out-
side of the yolk-sac, and the two are united by the undivided
portion of the mesoblast around the yolk-sac umbilicus. This
connection is never severed, and in consequence the remains of
the albumen-sac is drawn with the yolk-sac into the body-cavity
towards the end of incubation.

The sero-amniotic connection, which persists throughout incu-
bation, has an important effect on the general disposition of the
embryonic membranes. It is formed, as we have seen, in the
closure of the amnion, by the thickened ectoderm of the suture;
this ectodermal connection is, however, absorbed and replaced
on the fifth to the seventh days by a broad mesodermal fu-
sion, which maintains a permanent connection between amnion
and chorion. One important result of this relation is that the
albumen-sac, which is formed by the duplication of the chorion,
is prolonged by a tubular diverticulum to the sero-amniotic

218 THE DEVELOPMENT OF THE CHICK

plate (see Figs. 128 and 129). The latter becomes perforated
after the eleventh day, and there is thus direct communication
between the albumen-sac and the amniotic cavity. Hirota

Figs. 127, 128, and 129. — Diagrams of the relations of the embryonic mem-
branes of the chick, constructed from preparations, and from figures and
descriptions of Duval, Hans Virchow, Hirota and Fulleborn. In these
figures the ectoderm and entoderm are represented by plain lines: The
mesoderm by a cross-hatched line or band. The yolk-sac is represented
by broken parallel lines. In Fig. 127 the allantois is represented as a sac.
In Figs. 128 and 129, where it is supposed to be seen in section, its cavity
is represented by unbroken parallel lines. The stalk of the allantois is
exaggerated in all the diagrams to bring out its connection with the em-
bryo. The actual relations of the stalk are shown in Figures 33 and 82.
Alb., Albumen. Alb. S., Albumen-sac. All., Allantois. All. 1., Inner

wall of the allantois. All. C, Cavity of allantois. All. S., Stalk of allantois.

All. 4- Am., Fusion of allantois and amnion. Am., Amnion. Am. C,

Amniotic cavity. Chor., Chorion. C. T. R., Connective tissue ring. Ect.,

Ectoderm. E. E. B. C, Extra-embryonic body-cavity. Ent., Entoderm.

Mes., Mesoderm. S.-Am., Sero-amniotic connection. 8. Y. S. U., Sac of

the yolk-sac umbilicus. Umb., Umbilicus. V. M., Vitelline membrane.

Y. S. S., Septa of the yolk-sac.

Fig. 127. — Fourth day of incubation. The embryo is surrounded by the
amnion which arises from the somatic umbilicus in front and behind; the
sero-amniotic connection is represented above the tail of the embryo; it
consists at this time of a fusion of the ectoderm of the amnion and chorion.
The allantois is represented as a sac, the stalk of which enters the umbilicus
behind the yolk-stalk; the allantois lies in the extra-embryonic body-cavity,
and its mesoblastic layer is fused with the corresponding layer of the chorion
above the embryo. The septa of the yolk-sac are represented at an early
stage. The splitting of the mesoderm has progressed beyond the equator
of the yolk-sac, and the undivided portion is slightly thickened to form
the beginning of the connective tissue ring that surrounds the yolk-sac
umbilicus. The ectoderm and entoderm meet in the zone of junction,
beyond which the ectoderm is continued a short distance. The vitelline
membrane is ruptured, but still covers the yolk in the neighborhood of
the yolk-sac umbilicus. The albumen is not represented in this figure.

Fig. 128. — Ninth day of incubation. The yolk-sac umbilicus has become
much narrowed; it is surrounded by the mesodermal connective tissue
ring, and by the free edges of the ectoderm and entoderm. The vitelline
membrane still covers the yolk-sac umbilicus and is folded into the albumen.
The allantois has expanded around the amnion and yolk-sac and its outer
wall is fused with the chorion. It has pushed a fold of the chorion over
the sero-amniotic connection, into which the mesoderm has penetrated,
and thus forms the upper fold of the albumen-sac. The lower fold of the
albumen-sac is likewise formed by a duplication of the chorion and allan-
tois; it must be understood that lateral folds are forming also, so that the
albumen is being surrounded from all sides.

The stalk of the allantois is exaggerated so as to show the connection of
the allantois with the embryo; it is supposed to pass over the amnion,
and not through the cavity of the latter, of course.

EMBRYO A^D EMBRYONIC MEMBRANES

219

All.} Am-.^ Ch

Fig. 127

Fig. 128

220

THE DEVELOPMENT OF THE CHICK

states that, after this connection is estabUshed, the amniotic
fluid coagulates in alcohol, "just like the fluid in the albumen-
sac; owing, presumably, to the presence of albumen which has
found its way through the perforations into the amniotic fluid."
This observation is confirmed by Fiilleborn.

The Allantois. The part of the wall of the allantois that
fuses with the chorion may be called the outer wall; the remainder
of the sac of the allantois constitutes the inner wall. The distal
intermediate part of the allantois is specialized with the chorion
as the wall of the albumen-sac.

All^Am.

A/J.C.

Fig. 129. — Twelfth day of incubation. The conditions
represented in Fig. 128 are more advanced. The albu-
men-sac is closing; its connection with the cavity of
the amnion by w^ay of the sero-amniotic connection
will be obvious. The inner wall of the allantois has
fused extensively with the amnion. The umbilicus of
the yolk-sac is much reduced, and some yolk protrudes
into the albumen (sac of the yolk-sac umbilicus).

In the outer wall there are three layers, viz., an internal epi-
thelial laA^er, formed by the entoderm of the allantois; a thick
very vascular middle or mesodermal laver, formed bv fusion of
the mesoblast of allantois and chorion; and a thin, outer, ecto-
dermal layer derived from the chorion.

EMBRYO AND EMBRYONIC MEMBRANES

221

Rate of Growth of the Allantois. As the embryo lies on its
left side, the allantois grows out on the right side of the embryo
(Figs. 127 and 130 A) and unites with the chorion about the
one hundredth hour. It then spreads rapidly as a flattened sac
over the embryo, increasing the extent of the fusion with the

Fig. 130. — Diagrams showing the relations of the allantois,
represented by the tinted area, at different ages. (After

Hirota.)
Alb., Albumen. Alb. S., Edge of albumen-sac.^ All. V.,
Allantoic vein. am. C, Amniotic cavity. S.-Am., Sero-amm-
otic connection. Y. 8., Yolk-sac. .

A. At 120 hours showing only the amniotic cavity and al-
lantois X 2. . • -x ] 1

B. At 144 hours, showing only the amniotic cavity and al-
lantois X 1.2. ^ n^i 1 ii ] 4-

C. At 192 hours; the entire yolk x .66. Ihe dotted out-
line represents the amniotic cavity. , . i. i, ii

D. At 214 hours. The entire egg after removal ot the shell,
X .66. The allximen mass is at the left ; the albumen-sac is be-
ginning to form.

chorion, hence of its outer wall pari passu. At the end of the
fifth day it covers more than half of the embryo (Fig. 130 A);
at the end of the sixth day the embryo is entirely covered by

222 THE DEVELOPMENT OF THE CHICK

the allantois (Fig. 130 B) ; at the end of the eighth day the alhm-
tois has covered half of the yolk-sac (Fig. 130 C). At the end
of the ninth day, the formation of the albumen-sac is begun
(Fig. 130 D). At the end of the eleventh day, the albumen-sac
is practically closed at the lower pole. On the twelfth day, the
albumen-sac is closed, and on the sixteenth day the contents
are practically entirely absorbed.

Blood-supply of the Allantois. There are two allantoic (um-
bilical) arteries and one allantoic vein. (See Chap. XII.) Both
arteries persist throughout the period of incubation, but the
left is much the better developed. It passes out along the stalk of
the allantois to the inner wall of the allantoic sac, where it divides
in two strong branches, one running cephalad and the other caudad
to the margins of the sac where they pass over to the outer wall;
The allantoic vein runs in the inner wall and passes over to the
outer wall near the sero-amniotic connection. Both arteries and
veins inhibit the expansion of the allantoic sac where they sur-
round the margin; but the vein has by far the greatest effect,
as its action is supplemented by the sero-amniotic connection.
Thus indentations, gradually growing deeper, are established
along the margins of the allantoic sac, and the outgrowth of the
latter on each side of the indentations produce overlapping lobes
(Figs. 130 C and D).

The arrangement of the smaller vessels and capillaries is
very different in the outer and inner walls. In the outer wall
the arteries and veins branch and interdigitate in the deeper
portions of the mesoblast, and end in an extraordinarily fine-
meshed capillary netw^ork situated immediately beneath the thin
ectoderm. "The capillaries form such narrow meshes, and have
relatively so wide a lumen, that they can be compared only with
those of the lungs of higher animals, and of the choroidea of
the eye; indeed, instead of describing it as a vascular network
embedded in tissue, one could as well describe it as a great
blood-sinus interrupted by strands of tissue" (FiiUeborn.) This
capillary network of the outer wall constitutes the respiratory
area of the allantois. At the margins it passes gradually into
the incomparably wider meshed capillary network of the inner
wall. An extensive system of lymphatics is developed, l^oth
in the outer and inner walls of the allantois, accompanying all
the blood-vessels, even to their ultimate terminations.

EMBRYO AND EMBRYOXIC MEMBRANES 223

Structure of the Allantois. (1) Inner wall. The inner wall
of the allantois consists primarily of two layers, an inner ento-
dermal and outer mesodermal layer. The latter soon becomes
differentiated into two layers, an external, delicate, limiting layer
of flat polygonal cells, with interlocking margins, and an inter-
mediate layer of star-shaped cells embedded in a homogenous
mucous ground substance. Parts of the inner wall become
extremely thin, and in these regions the intermediate layer may
become entirely absent. Elsewhere, particularly around the
larger arteries and veins, the intermediate layer may attain
considerable thickness. The entoderm becomes reduced to a
layer of flat, interlocking cells. On the eighth day, spindle-
shaped muscle cells begin to appear in the mesoderm of the
inner wall, and undergo rapid increase in numbers. Their dis-
tribution is somewhat irregular; in certain places they may even
form several layers, and in others are practically wanting.

On the seventh day the inner wall of the allantois begins
to fuse Avith the amnion in the neighborhood of the sero-amniotic
connection, and this fusion rapidly extends over the area of
contact between the two membranes. Within the area of fusion
the muscle lavers of the allantois and amnion mutuallv reinforce
each other, and in places no boundary can be found between
them (Fiilleborn). But during the latter half of incubation the
musculature of the fused area of allantois and amnion degener-
ates almost completely.

Towards the end of incubation, part of the inner wall of the
allantois fuses also with the yolk-sac, and is therefore carried
with the latter into the body-cavity of the chick.

(2) The Outer Wall of the Allantois. As already noted, the
outer wail of the allantois fuses with the chorion. The compound
membrane, which is respiratory in function, must be considered,
therefore, as one. Over the entire respiratory area the ectoderm,
belonging primarily to the chorion, which is elsewhere two layers
of cells in thickness, becomes reduced to an exceedingly thin
layer in direct contact with the walls of the capillaries internally
and the shell membrane externally. According to Fiilleborn,
the ectoderm cannot be distinguished as a separate layer in the
latter half of incubation, and the capillaries appear to be in
immediate contact with the shell-membrane. No muscular
tissue appears to develop in the outer wall of the allantois.

224 THE DEVELOPMENT OF THE CHICK

(3) The Albumen-sac. The allantois in the course of its
expansion over the embryo, between amnion and chorion, reaches
the sero-amniotic connection; it must then either divide and
ffrow round on eacli side of tlie connection, or evaginate the
chorion above the connection and carry it as an overlapping
fold on bej'Ond. The latter is what actually happens, and there
is established as a consequence an overlapping fold of the chorion
containing an extension of the allantois (Fig. 128); the space
beneath this fold terminates, naturally, at the sero-amniotic
connection. In the meantime the cleavage of the mesoblast
has separated chorion and yolk-sac as far as the neighborhood
of the volk-sac umbilicus, where the viscid albumen has accumu-
iated. The latter is situated not opposite to the yolk-stalk,
but near the posterior pole of the yolk-sac, with reference to
the embryo, i.e., usually towards the narrow end of the shell.
Now the allantois growing around the yolk-sac from all sides
reaches the neighborhood of the albumen and enters an evagina-
tion of the chorion that wraps itself around the albumen, thus
initiating the formation of a double sac of the chorion enfolding
the albumen and containing between its two layers an extension
of the allantois. The latter is therefore separated everywhere
from the albumen by the thickness of the chorion. The suj^erior
fold of the albumen-sac is the same fold that overgrows the
sero-amniotic connection, and the albumen-sac is therefore pro-
longed beneath this fold to the sero-amniotic connection itself,
which, as we have seen, becomes perforated, thus admitting
albumen into the amniotic cavitv.

The ectoderm lining the albumen-sac is two-layered, and the
cells next the albumen tend to be cubical or swollen, and fre-
quently vesicular, owing apparently to absorption of albumen.
In the neighborhood of the yolk-sac umbilicus, papilla-like pro-
jections of the ectoderm into the albumen are common (Fig. 129).
But these do not occur over the remainder of the albumen-sac
of the chick, as described by Duval for the linnet; nor do they
possess a mesodermal core.

Prior to the union of the mesoderm over the yolk-sac umbili-
cus, the yolk forms a hernia-like protrusion into the albumen-
sac (sac of the yolk-sac umbilicus, see Fig. 129), which is, hoAvever,
retracted as the mesoderm ring closes over the yolk-sac umbilicus.
The vitelline membrane ruptures at an early period of the incu-

EMBRYO AND EMBRYONIC MEMBRANES 225

bation over the embryonic pole and gradually slips down over
the yolk, and is finally gathered together in the albumen-sac.

(4) The allantois also serves as a reservoir for the secretions
of the mesonephros, and subsequently the permanent kidney,
which reach it by way of the cloaca and neck of the allantois.
The fluid part of the embryonic urine is absorbed, but the con-
tained salts are deposited in the walls and cavity of the allantois.
If the connection between the Wolffian ducts and cloaca be inter-
rupted, the former become enormously extended by the secre-
tions of the mesonephros.

The Yolk-sac. The yolk-sac is established in the manner
already described; it is constituted by the extra-embryonic
splanchnopleure, and is permanently united to the intestine by
the yolk-stalk. A narrow lumen remains in the stalk of the
yolk-sac throughout, and even after, incubation, but the yolk
does not seem to pass through it into the intestinal cavity. The
walls of the yolk-sac, excepting the part derived from the pellucid
area, are lined with a special glandular and absorbing epithelium,
which digests and absorbs the yolk and passes it into the vitel-
line circulation, through which it enters the hepatic portal circu-
lation and comes under the influence of the hepatic cells. The
yolk-sac is thus the primary organ of nutrition of the embryo,
and it becomes highly elaborated for the performance of this
function. Contrary to the statements found in many text-books,
it does not reach its maximum development until the end of
incubation. Throughout incubation it steadily increases in
complexity and efficiency so as to provide for the extremely
rapid growth of the embryo.

The functions of the yolk-sac manifestly require a large sur-
face area, which is provided for by foldings of the wall projecting
into the yolk. At the height of its development the inner surface
of the yolk-sac is covered with numerous folds or septa projecting
into the yolk, which are highest at the equator and decrease in
both directions away from the equator. In general, these folds
follow the direction of the main arteries, i.e., they run in a
meridional direction, repeatedly bifurcating distally (Fig. 132).
Moreover, each one is perforated by numerous stomata, and the
yolk-sac epithelium covers all free surfaces, and a capillary net-
work is found in every part. So far do they project into the
interior towards the close of incubation, that those of opposite

226

THE DEVELOPMENT OF THE CHICK

sides may be approximately in contact, and the cavity of the
yolk-sac is thus broken up into numerous connecting compart-
ments filled with yolk. The outer wall of the yolk-sac is smooth
and not involved in the folds. The beginning of the folds of the
yolk-sac may be found at the time of appearance of the vascular
area of the blastoderm, and they develop pari passu, with the
vessels of the yolk-sac (Fig. 131).

Fig. 131 shows the appearance of the folds at the stage of
twelve somites. It is a view of the blastoderm from below,

^■^4^1

Fig. 131. — Septa of the yolk-sac as seen on

the lower surface of the blastoderm at the

stage of 12 s. (After Hans Virchow.)

m. R., Marginal ridge of entoderm overly-
ing the sinus terminalis.

drawn as an opaque object, and it shows the incipient folds of
the yolk-sac in an arrangement that corresponds roughly, but
not accurately, with that of the blood-islands, which lie in large
part in the bases of the folds. The site of the vena terminalis
is marked bv a circular fold of the entoderm. The folds of the
volk-sac thus coincide in their distribution with the vascular area
and are so limited at all times, being absent in the vitelline area.
There is thus a close connection between the vitelline blood-

EMBRYO AND EMBRYONIC MEMBRANES

227

vessels and the folds of the yolk-sac, which will be considered
more fully beyond.

The interior of the yolk-sac is lined with entoderm which
differs in its structure in different regions: In the area pellucida
the cells are flattened; in the vascular zone of the area opaca
are found the columnar cells with swollen ends described pre-
viously. After the third or fourth day these are found filled
with yellow fatty droplets, which give a yellow tone to the interior
of the living yolk-sac, and which are so abundant in later stages
as to render the layer perfectly opaque. These cells do not con-

FiG. 132. — Part of the interior of the yolk-sac of a
duck at the time of hatchng. In the upper part of
the figure the septa are seen from the side showing
the stomata. In the lower part they are seen on
edge. Note the sinuous course of the arteries along
the free edges of some of the septa. (After H.
Virchow.)

tain entire yolk-granules; apparently, then, the yolk-granules are
digested before absorption in this region. In the region of the
inner zone of the vitelline area, the entoderm is composed of
several layers of large cells containing yolk-granules, constituting
the germ-wall, and in the outer vitelline zone we come to the
periblast. The germinal wall and inner zone of the vitelline area
represent the formative region of the yolk-sac epithelium in the
manner already described (Chap. \).

Blood-vessels of the Yolk-sac. The development of the circu-

228 THE DEVELOPMENT OF THE CHICK

lation in the yolk-sac may be divided into the following stages
(following Popoff) :

1. Indifferent network bounded peripherally by the vena
terminalis, connected by two anterior vitelline veins with the
heart; no arterial trunks.

2. Origin of an arterial path in the network; the right anterior
vitelline vein begins to degenerate.

3. Origin of intermediate veins; the (left) posterior vein
begins to develop.

4. Development of collateral veins; further degeneration of
the right anterior vein; complete formation of the posterior vein.

5. Further branching; development of a rich venous network;
the vena terminalis begins to degenerate.

6. Definitive condition; development of a rich venous net-
work in the folds or septa of the yolk-sac; anastomosis of vessels
of the yolk-sac and allantois.

The changes can be followed only in outline. The earliest
condition has been described in Chapters IV and V. Fig. 133
show^s a condition intermediate between stages 1 and 2 above.
The network is entirely arterial, except towards the anterior
end, i.e., the blood flows outwards away from the heart. It
enters the vena terminalis and is returned by right and left an-
terior vitelline veins to the heart. The beginning of arterial
trunks in the network is indicated particularly on the left side
(right side of the figure). The connection of the arterial network
with the dorsal aorta is still net-like.

Fig. 134 shows an advance of the same processes. The trunks
of the vitelline arteries are better differentiated from the network,
and the blood is still returned to the heart entirely by way of
the vena terminalis and the right and left anterior vitelline veins,
which have come in contact distally, circumscribing in their
proximal parts the mesoderm-free area of the blastoderm. The
beginning of the lateral vitelline veins is indicated, particularly
on the right side (left of the figure).

Fig. 135 represents a great advance. The vitelline arteries
arise from the dorsal aortse as single trunks, and branch in the
vascular network, some of them reaching as far as the vena
terminalis. The two anterior vitelline veins have fused in front,
and the right anterior vein is reduced in size so that most of the
blood reaches the heart through the left anterior vein. But the

Fig. 133. — Circulation in the embryo and the yolk-sac. Stage of about

16 s; from below. The vitelline arteries are beginning to differentiate out

of the vascular network particularly on the loft side. (Observer's right.)

Injected. (After PopolT.;

1, Marginal vein. 2, Region (jf venous network. 3, First and second

aortic arches. 4 r, 4 1, Right and left anterior vitelline veins. 5, Heart.

6, Anterior intestinal portal. 1, Aorta?. 8, Vitelline arteries in process of

differentiation. 9, Blood islands.

Fig. 134. — Circulation in the embryo and the yolk-sac at the stage of about
22 s, drawn from below. Note differentiation of branches of the vitelline
arteries. Injected. (After Popoff.)
1 Marginal vein. 2, Region of venous network. 3, Carotid loop. 4 r,
4 1 iiitrht and left anterior vitelline veins. 5, Heart. 6, Anterior intes-
tinal portal. 7, Dorsal aorta. S, Branches of vitelline arteries.

EMBRYO AND EMBRYONIC MEMBRANES 229

most striking change is the transformation of part of the vascular
network into channels in which the blood flows towards the heart.
Of these there may be recognized the following: 1. Intermediate
veins arising from the vena terminalis at various places and
gradually losing themselves centrally in the vascular network.
2. The vascular network immediatelv behind the embrvo has
assumed a venous character and likewise a large part of the
network immediately surrouncUng the embryo. 3. Lateral vitel-
line veins are beginning to develop from the anterior intestinal
portal backwards.

Fig. 136, representing the circulation at a stage of about 40
somites, shows the completion of the primary circulation in the
yolk-sac. The vitelline arteries branch richly, and end in a
capillary network; very few arterial branches reach the vena
terminalis as such, and then only very fine ones. The vena
terminalis itself is relatively reduced; the lateral vitelline veins
have absorbed the network between themselves and the inter-
mediate veins, which now appear as prolongations of the lateral
veins. The right anterior vitelline vein has disappeared almost
entirely and the posterior vitelline vein is well developed, empty-
ing into the left lateral vein.

The lateral vitelline arteries and veins are superposed as
far peripherally as the original intermediate veins, which lie
between the arterial trunks. Wherever there is superposition
of arteries and veins, the latter are superficial and the former
deep in position as seen from above. The figure also shows the
vascular network in the budding allantois, and some of the em-
bryonic blood-vessels.

In the later stages of development the arteries are carried in
by the septa of the yolk-sac and lie near their free edges; the
veins, on the other hand, remain superficial in position. The
terminal vein becomes progressively reduced in importance up
to about the tenth day, and then gradually disappears as such,
being taken into the terminal capillaries. After the tenth day
the anterior and posterior vitelline veins decrease in importance
and finally become almost unrecognizable. The lateral veins,
on the other hand, increase in importance and return all of the
blood to the embryo.

The rich network of venous capillaries in the septa of the
yolk-sac is shown in Fig. 137. It lies immediately beneath tliQ

230 THE DEVELOPMENT OF THE CHICK

epithelium over the entire extent of the septa and forms loops
along the free border. The arteries do not communicate directly
with this network according to Popoff , and the course of the
circulation from arteries to veins is not clearly described by this
author.

The allantois fuses with the yolk-sac in the region of the
yolk-sac umbilicus, and anastomoses arise between the veins of
the allantois and those of the yolk-sac.

Ultimate Fate of the Yolk-sac. On the nineteenth day of
incubation, the yolk-sac slips into the body-cavity through the
umbilicus; which thereupon closes. The mechanism of this
process is of considerable interest. The yolk-sac is still a volu-
minous organ, and equal to about one sixth the weight of the
embryo. It is therefore inconceivable that it could be "drawn
into" the body-cavity by means of its stalk, which has only the
intestine for attachment. The process is much more complex
and may be briefly described as follows: We have already seen
that the inner wall of the allantois fuses with the amnion on the
one hand; distally it is connected with the yolk-sac. Now this
wall of the allantois is muscular, and it is probable that its con-
traction is the first act in the inclusion of the yolk-sac within the
body-wall. It is aided in this, however, by the inner wall of
the amnion, i.e., that part of the amnion arising from the umbili-
cus and not fused with the allantois. This part of the amnion
surrounds the yolk-stalk, and is itself richly provided with muscle
cells, forming a crossing and interlacing system. It is carried
down and over the yolk-sac to about its equator by the allantois,
and when the yolk-sac is half taken into the body-cavity, it reaches
its distal pole and fuses there. Now if the egg be opened at
this stage in the process and this wall of the amnion cut through,
it contracts rapidly to a fraction of its former area (Virchow).
It is apparent, then, that the tension of this membrane on the
yolk-sac must exert a continuous pressure that tends to force it
into the body-cavity. It is in this way, then, by contraction
of the inner walls of the allantois and of the amnion, that the
yolk-sac is pressed into the body-cavity.

The umbilicus is therefore closed b}- the mere act of inclusion
of the yolk-sac, for the inner amniotic wall is attached on the
one hand to the body-wall, and on the other to the distal pole
of the yolk-sac. A minute opening is left in the center of the

Fig. 135. — Circulation in the embryo and yolk-sac after 74 hours' incuba-
tion. Stage of about 27 s from below. Injected. (After Popoff.)

1, Marginal vein. 2 r, 2 1, Right and left anterior vitelline veins sur-
rounding the mesoderm-free area. 8, Anterior intestinal ]:)ortal. 4, In-
termediate veins connecting with the venous network centrally. 5, Right
dorsal aorta. 6, Posterior \itelline vein in j)rocess of formation. 7, Vitel-
line arteries.

Note that the right anterior vitelline vein (2 r) is much atrophied.

Fig. 136. — Circulation in the embryo and yolk-sac of an embryo of about
40 s, showing the later development of the lateral and intermediate vitel-
line veins. Reduction of vena terminalis (marginal vein). Almost com-
plete atrophy of the right anterior vein. Injected. (After Popoff.)

1, Marginal vein. 2 r, 21, Right and left anterior vitelline veins. 3,
Arch of aorta. 4, Left posterior cardinal vein. or, 51, Right and
left omphalomesenteric veins. 6, Aorta. 6 a, Left dorsal aorta. 7,
Vitelline artery. 8, Posterior vitelline vein. 9, Vascular network in the
allantois.

EMBRYO AND EMBRYONIC MEMBRANES 231

umbilical field, through which dried remnants of the inner wall
of the allantois, w^hich is likewise attached to the distal pole of
the yolk-sac, protrude for a short time. On the inner side the
yolk-sac is attached to the umbilicus by its distal pole, and by
its stalk to the intestine. The absorption of the yolk-sac then
goes on with great rapidity, being reduced from a weight of
5.34 gr. twelve hours after hatching to 0.05 gr. on the sixth day
after hatching, according to a series of observations of Virchow.

The Amnion. The amnion invests the embryo closely at the
time of its formation, but soon after, fluid begins to accumulate
w^ithin the amniotic cavity, which gradually enlarges so that the
embryo lies within a considerable fluid-filled space, which in-
creases gradually up to the latter part of the incubation, and
then diminishes again, so that the embryo finally occupies most
of the cavitv. The connections of the amnion with the chorion,
and later with the allantois, albumen-sac, and yolk-sac, have
been already described.

Muscle fibers appear in the w^alls of the amnion on the fifth
or sixth day and gradually increase in number; though they
subsequently degenerate over the area of fusion with, the allan-
tois. They persist elsewhere, how^ever, and are active in the
inclusion of the yolk-sac in the manner already described. Shortly
after the appearance of the muscle fibers slow vermicular or
peristaltic contractions of the amnion begin, and the embryo is
rocked within the amniotic cavity. Apparently, adhesions are
thus prevented, but they are sometimes formed and lead to various
malformations of the embryo. In some cases the amnion fails
to develop; in such cases, the embryo usually dies at a relatively
early stage, though Dareste records an anamniotic embryo of
thirteen days, apparently full of life and vigor.

The amnion apparently acts first as a protection against all
mechanical shocks and jars which are taken up by the fluid;
second, by protecting the embryo against the danger of desicca-
tion; third, by protecting it against adhesions with the shell-
membrane and embryonic membranes, and lastly by providing
space for the expansion of the allantois and consequent increase
of the respiratory surface. It also has secondary functions in
the chick in connection with the absorption of the albumen and
the inclusion of the yolk-sac. It will be readily understood,
then, why anamniotic embryos usually do not develop far.

232 THE DEVELOPMENT OF THE CHICK

Hatching (after von Baer). About the fourteenth day the
growing embryo accommodates itself to the form of the egg so
as to he parallel to the long axis with its head usually towards
the broad end near to the air-chamber. Sometimes, however,
the embryo is turned in the reverse position (von Baer). The
head is bent towards the breast, and is usually tucked under
the right wing. Important changes preparatory to hatching
take place on the seventeenth to the nineteenth days. The
fluid decreases in the amnion. The neck acquires a double bend
so that the head is turned forward, and, in consequence, the beak
is towards that part of the membranes next to the air-chamber.
The intestine is retracted completely into the body-cavity, and
on the nineteenth day the yolk-sac begins to enter the body-
cavity. On the twentieth day the yolk-sac is completely included,
and practically all the amniotic fluid has disappeared. The
chick now occupies practically all the space within the egg,
outside of the air-chamber. The umbilicus is closing over. The
ductus arteriosi begin to contract, so that more blood flows
through the lungs. The external w^all of the allantois fused with
the chorion still remains very vascular.

Now, if the chick raises its head, the beak readily pierces
the membranes and enters the air-chamber. It then begins to
breath slowly the contained air; the chick may be heard, in some
cases, to peep within the shell two days before hatching, a sure
sign that breathing has begun. But the circulation in the allan-
tois is still maintained and it still preserves its respiratory func-
tion. When the chick makes the first small opening in the shell,
which usually takes place on the twentieth day, it begins to
breathe normally, and then the allantois begins to dry up and
the circulation in it rapidly ceases. It then becomes separated
from the umbilicus, and the remainder of the act of hatching is
completed, usually on the twenty-first day.

Fig. 137. — Part of a septum of the yolk-sac. Injected. 20 days' incuba-
tion. The free edge is above. (After Popoff.)
Ar., Artery. St., Stomata. V. an., Longitudinal anastomoses of venous
network. V., vein.

■ «<

vV

^GicT^

CHAPTER VIII
THE NERVOUS SYSTEM

I. The Neuroblasts

The account given in Chapters V and VI outlines the origin
of the larger divisions of the central nervous system and ganglia.
The subsequent growth and differentiation is due to multiplica-
tion of cells, aggregation of embryonic nerve-cells, or neuro-
blasts, in particular regions or centers, the formation and growth
of nerve-fibers which combine to form nerves and tracts, and
the origin and differentiation of nerve-sheaths, and the support-
ing cells, neuroglia, of the central system. The most important
factors are the origin of the neuroblasts and of nerve-fibers in
connection with them; these fibers form the various nerve-tracts
and commissures within the central nervous system and the
system of peripheral nerves. The origin of neuroblasts and the
development of fibers is the clue to differentiation in all parts
of the nervous system.

Neuroblasts are found in two primary locations in the embryo;
(1) in the neural tube, and (2) in the series of ganglia derived
from the neural crest; these are known as medullary and gang-
lionic neuroblasts respectively.^

The Medullary Neuroblasts. In the neural tube of the chick,
up to about the third day, there are present only two kinds of
ceils, the epithelial cells and the germinal cells (Fig. 138).

The epithelial cells constitute the main bulk of the walls,
and extend from the central canal to the exterior; their inner
ends unite to form an internal limiting membrane lining the
central canal, and their outer ends to form an external limiting
membrane. Each cell in the lateral walls of the tube is much
elongated and usually shows three enlargements, viz., at each
end and in the region of the nucleus, the cell being somewhat
constricted between the nucleus and each end. In different

1 Neuroblasts arise also in the olfactory epithelium. (See Chap. IX.)

233

234

THE DEVELOPMENT OF THE CHICK

cells the nuclei are at different levels; thus in a section several
layers of nuclei appear. These cells are not closely packed
together, except at their outer ends, but are more or less separated
by intercellular spaces that form a communicating system of
narrow channels.

Jm.&K

277. V

Ira.'m

Fig. 138. — Section of the neural tube, 29 s embryo.

c. C, Central canal, ep. C, Epithelial cells, g. C, Ger-
minal cells. 1. m. ex., External limiting membrane. 1. m. in.,
Internal limiting membrane. Ms'ch., Mesenchyme, m. v.,
Marginal velum.

The germinal cells are rounded cells situated next the central
canal between the inner ends of the epithelial cells; karyokinetic
figures are very common in them. According to His the germinal
cells are the parent cells of the neuroblasts alone; it is probable,
however, that they are not so limited in function, and that they
represent primitive cells from which proceed other epithelial
cells and embryonic neuroglia cells as well as neuroblasts.

THE NERVOUS SYSTEM

235

A narrow non-nucleated margin^ known as the marginal
velum, appears in the lateral walls of the neural tube external
to the nuclei (Fig, 138). This is occupied by the outer ends of
the epithelial cells. At this time, therefore, three zones may
be distinctly recognized in the walls of the neural tube, viz.,
(1) the zone of the germinal cells, including also the inner ends
of the epithelial cells, (2) the zone of the nuclei of the epithelial
cells, (3) the marginal velum. No chstinctly nervous elements
are yet differentiated.

Such elements, however, soon begin to appear: Fig. 139 repre-
sents a section through the
cord of a chick embryo of
about the end of the third day;
it is from a Golgi preparation
in which the distinctly nervous
elements are stained black, and
the epithelial and germinal
cells are seen only very indis-
tinctly. The stained elements
are the neuroblasts, and it will
be observed that they form a
layer roughly intermediate in
position between the marginal
velum and the nuclei of the
epithelial cells. They are
usually regarded as derived
from germinal cells that have
migrated from their central
position outwards; but it is

m/Jr~,

MMf

mi.4.

Fig. 139. — Transverse section through

the spinal cord and ganglion of a

chick about the end of the third

day; prepared by the method of

Golgi. (After Ramon y Cajal.)

C, Cones of growth. Nbl. 1, 2, 3, 4,
Neuroblasts of the lateral wall (1 and
2); of the spinal ganglion (3); of the
ventral horn (motor neuroblasts) (4).

possible that some of them may have been derived from epithelial
cells. However this may be in such an early stage, it is certain
that the neuroblasts formed later are derived from germinal cells.
It will be observed that each neuroblast consists of a cell-
body and a process ending in an enlargement. The process
arises as an outgrowth of the cell-body, and forms the axis cylin-
der or axone of a nerve-fiber; the terminal enlargement is known
as the cone of growth, because the growth processes by which
the axone increases in length are presumably located here. It
may be stated as an invariable rule that each axone process of a
medullary neuroblast arises as an outgrowth, and grows to its

236

THE DEVELOPMENT OF THE CHICK

final termination without addition on the part of other cells.
The body of the neuroblast forms the nerve-cell, from which,
later on, secondary processes arise constituting the dendrites.

The view that each nerve-cell with its axone process and
dendrites is an original cellular individual, is known as the neurone
theory. For the central nervous system this view is generally
held, but its extension to the peripheral system is opposed by
some on the ground that the axone in peripheral nerves is formed
within chains of cells, and is thus strictly speaking not an original
product of the neuroblast, though it may be continuous with the
axis cylinder process of a neuroblast. This view is discussed
under the peripheral nervous system.

Each medullary neuroblast is primarily unipolar and the

axone is the original outgrowth.
Soon, however, secondary proto-
plasmic processes arise from the
body of the nerve-cell and form the
dendrites. These appear first in
motor neuroblasts of the ventro-
lateral portion of the embryonic
cord, whose axones enter into the
ventral roots of spinal nerves (Fig.
140). The extent and kind of de-
velopment of these dendritic pro-
FiG. 140. — Transverse section cesses of the nerve-cells varies
through the spinal cord of a extraordinarily in different regions;
chick on the fourth day of Y\g^. 139, 140, and 141 give an idea

of their rapid development in the
motor neuroblasts up to the eighth

dav.

The Ganglionic Neuroblasts, The

ganglionic neuroblasts are located,

as the name implies, in the series of

ganglia derived from the neural

It must not be supposed, however, that all of the cells

incubation; prepared by the
method of Golgi. (After Ra-
mon y CajaL)

C. a., Anterior commissure.
D., Dendrite, d. R., Dorsal root.
Ep. Z., Ependymal zone. W.,
White matter (marginal velum).
Nbl. 4, Neuroblast of the ventral
horn (motor).

crest.

of the ganglia are neuroblasts, for the ganglia contain, in all
probability, large numbers of cells of entirely different function.
(Sheath-cells, see peripheral nervous system.) It is probable
also that the neuroblasts of the spinal ganglia and some cranial
ganglia, at least, are of two original kinds, viz., the neuroblasts of

THE NERVOUS SYSTEM

237

the dorsal root and of the sympathetic system. The first kind
only is considered here, and they are usually called the gan-
glionic neuroblasts s.s., because they alone remain in the spinal
ganglia. Like the medullary neuroblasts these neuroblasts form
outgrowths that become axis cylinder processes; but they differ
from the latter in that each ganglionic neuroblast forms two
outgrowths, one from each end of the spindle-shaped cells, which
are arranged with their long axes parallel to the long axis of the
ganglion (Fig. 139). Thus we may distinguish a central process
and a peripheral process from each neuroblast (Fig. 139) ; the
former corresponds to the axone and the latter to the dendrites
of the medullary neuroblast. The central axone enters the dorsal
zone of the neural tube, and the peripheral process grows out into
the surrounding mesenchyme.

Fig. 141. — Transverse section through the spinal
cord of a 9-day chick, prepared by the method
of Golgi. (After Ramon y Cajal.)
Col., Collaterals, d. R., Dorsal root. G., Gray

matter. Gn., Ganglion. Nbl. 4, Neuroblast of the

ventral horn (motor), v. R., Ventral root. W.,

White matter.

In the course of the later development the cell-body moves
to one side so that the central and peripheral branches appear
nearly continuous (Fig. 141). Farther shifting of the cell-body
produces the characteristic form of the ganglionic nerve-cell with
rounded body provided with stem from which the central and
peripheral branches pass off in opposite directions. . The central
process enters the marginal velum near its dorsal boundary and

238

THE DEVELOPMENT OF THE CHICK

there bifurcates, producing two branches, one of which grows
towards the head and the other towards the tail in the dorsal

CoJ.

Fig. 142. — Six centripetal axones of the dorsal

root, rigorously copied from a good preparation

prepared according to the method of Golgi.

From a longitudinal and tangential section of

the dorsal column of the spinal cord of an 8-

day chick. (After Ramon y Cajal.)

Col., Collaterals. 1, 2, 3, 4, 5, 6, the axones
entering the cord.

column of the white matter. The ascending and descending
branches send off lateral branches, collaterals, which pass deeper
into the cord, and ramify in the gray matter of the dorsal horn.

THE NERVOUS SYSTEM 239

Fig. 142 represents six central processes of ganglionic neuroblasts
entering the cord and branching as described.

After this preliminary account of the neuroblasts we may
take up the development of the spinal cord, brain, and peripheral
nervous system.

II. The Development of the Spinal Cord

We have seen that the epithelial cells of the neural tube
stretch from the lumen of the central canal to the exterior, and
that the nuclei are arranged so as to leave the outer ends free,
thus forming the marginal velum.

In the roof and floor the epithelial cells are relatively low,
and in the lateral zones much elongated. The epithelial cells
are added to at first by transformation of some of the germinal
cells; but they do not appear to multiply by division, and as
development proceeds they become more and more wideh^ sep-
arated, the interstices being filled up by neuroblasts, embryonic
glia cells, and fiber tracts. As the wall of the neural tube grows
in thickness, the epithelial cells become more and more elongated,
seeing that both external and internal connections are retained;
and, as the growth takes place mainly external to their nuclear
layer, the latter becomes reduced, relative to the entire thickness
of the neural tube, to a comparatively narrow zone surrounding
the central canal, and is now known as the ependyma (Fig. 143).
Cilia develop on the central ends of the ependymal cells in the
central canal, and from the outer end of each a branching process
extends to the periphery anastomosing with neighboring epen-
dymal processes so as to form a skeleton or framework enclosing
the other cellular elements and fibers of the central system.

Beginning with the third day a new layer appears between
the nuclei of the epithelial cells and the marginal velum. This
layer, known as the mantle layer, is composed of neuroblasts
and embryonic glia cells, and represents the gray matter (Figs.
140 and 144). The white matter of the cord is laid down in
the marginal velum. The sources of the cells composing the
mantle layer may be twofold, viz., from the young epithelial
cells or from the germinal cells. According to some authors
young epithelial cells may be transformed into either neuroblasts
or neuroglia cells. Thus the form of the youngest neuroblasts
in Fig. 139 indicates derivation from epithelial cells, but this

240

THE DEVELOPMENT OF THE CHICK

cannot be regarded as proved. Similarly intermediate stages
between epithelial and true glia cells are apparently shown in
Fig. 143. However, there can be but little doubt that the prin-
cipal source of the neuroblasts of the mantle layer is the germinal
cells, that migrate outwards between the bodies of the epithelial
cells. The germinal cells continue in active division up to at
least the eleventh day, and their activity seems sufficient to
provide for all the cellular elements of the mantle layer, whereas
the epithelial cells apparently do not divide at all. Moreover,
mitoses are not infrequent in some cells of the mantle layer itself.

Fig. 143. — Transverse section of the cord of a

nine-day chick to show neuroglia and ependymal

cells; prepared by the method of Golgi. (After

Ramon y Cajal.)

D., Dorsal. Ep., Ependymal cells. N'gl., Neu-
roglia cells, v., Ventral.

The form of the gray matter in the cord in successive
stages is shown in Figs. 144, 145, and 146, representing sections
of the cord at five, eight, and twelve days. It will be seen that
the gray matter gains very rapidly in importance between the
fifth and the eighth days.

Attention should be directed to a group of neuroblasts situated at
the external margin of the white matter just above the ventral roots.
This is known as Hoffmann's nucleus; it extends the entire length of the
cord (Fig. 146, twelve days).

The white matter of the cord gains in importance at an equal
rate (Figs. 144, 145, 146). Its production is due to ascending

THE XERVOUS SYSTEM

241

and descending tracts of fibers derived from medullary and
ganglionic neuroblasts. The dorsal and ventral roots of the
spinal nerves divide it on each side into three main columns,
viz., dorsal situated above the dorsal root, lateral situated be-
tween dorsal and ventral roots, and ventral situated below the

.-*?"

■'^.^^■^A^^'^r^^-^

¥

iX

Nil

C.

£P

W.

M'll.

:!?:->

.>iii-

■^%^-

C.d.

blV

d/. y

Fig. 144. — Transverse section through the cervical swelHng
of the spinal cord of a chick, middle of the fifth day. (After
V. Kupffer.)
bl. v., Blood vessel. C. a., Anterior commissure. C, Cen-
tral canal, d., Group of axones at the levelof the dorsal root^
Ep., Ependyma. N'bl., Neuroblasts,
white matter.

V. Ventral column of

ventral roots. The dorsal column begins first as a bundle of
fibers at the entrance of the fibers of the dorsal root (Fig. 144).
Subsequently, other fibers come in this region and gradually
extend towards the dorsal middle line, displacing the ependyma

242

THE DEVELOPMENT OF THE CHICK

and gray matter (Fig. 145, eight days), but the dorsal columns
of the two sides are still separated in the median line by a broad
septum of ependymal cells. Later (Fig. 146, twelve da\^s) this
septum becomes very narrow, and the accumulation of fibers in
the dorsal columns causes the latter to project on each side of
the middle line, thus forming an actual fissure between them.

Fig. 145. — Transverse section through the spinal cord, and the eighteenth
spinal ganglion of an eight-day chick.
Centr., Centrum of vertebra, d. R., Dorsal root. Ep., Ependyma. Gn.,
Spinal Ganglion. Gn. symp., Sympathetic ganglion. Gr. M., Gray matter,
m. N., Motor nucleus. R. com., Ramus communicans. R. d., Ramus dor-
salis. R. v., Ramus ventralis. Sp., Spinous process of vertebra, v. R.,
Ventral root. Wh. M., White matter.

Central Canal and Fissures of the Cord. The central canal
passes through a series of changes of form in becoming the prac-
tically circular central canal of the fully formed cord. L'p to
the sixth day it is elongated dorso-ventrally, usually narrowest
in the middle with both dorsal and ventral enlargements. About

THE NERVOUS SYSTEM

243

the seventh day the dorsal portion begins to be ol^hterated by
fusion of the ependymal cells, and is thus reduced to an epen-
dymal septum. On the eighth day this process has involved the
upper third of the canal; the form of the canal is roughly wedge-
shaped, pointed dorsally and broad ventrally (Fig. 145). The
continuation of this i^rocess leaves only the ventral division as
the permanent canal.

At the extreme hind end of the cord the central canal becomes
dilated to form a relatively large pear-shaped chamber with thin
undifferentiated walls (Fig. 148); the terminal wall is still fused
with the ectoderm at eight days, and the chamber appears to
have a maximum size at this time. At eleven days the fusion
with the ectoderm still exists, and the cavitv is smaller.

s.d-

' ♦.•.'•.•-••:•.'. '.••.:•::••/.■:. ■%

'i '■ ■.

'4tJ^^-

Fig. 146. — Transverse section through the

cervical swelling of the spinal cord of a

12-day chick. (After v. Kupffer.)

C, Central canal, d. H., Dorsal horn of
the gray matter. Ep., Ej^endyma. N. H.,
Nucleus of Hoffmann, s. d., Dorsal fissure,
s. v., Ventral fissure, v. H., Ventral horn
of the gray matter.

The development of the so-called dorsal and ventral fissures
is essentially different. The entire ventral longitudinal fissure
of the cord owes its origin to growth of the ventral columns of
gray and white matter which protrude below the level of the
original floor (Figs. 145 and 146), and the latter is thus left be-
tween the inner end of the fissure and the central canal. The
•dorsal longitudinal fissure on the other hand is for the most part

244 THE DEVELOPMENT OF THE CHICK

a septum produced by fusion of the walls of the intermediate
and dorsal portions of the central canal; there is, however, a true
fissure produced by protrusion of the dorsal columns of white
matter (Fig. 146). This is, however, of relatively slight extent.
The original roof of the canal is therefore found between the
dorsal septum and the fissure.

Neuroblasts, Commissures, and Fiber Tracts of the Cord. The
medullary neuroblasts may be divided into four groups: (1) The
first group, or motor neuroblasts, form the fibers of the ventral
roots of the spinal nerves. These are situated originally in the
ventro-lateral zone of the gray matter (Figs. 144, 145, 146);
they are relatively large and form a profusion of dendrites (Figs.
140, 141). As they increase in number and size they come to
form a very important component of the ventral horn of the gray
matter and contribute to its protrusion. (2) The second group
may be called the commissural neuroblasts. These are situated
originally mainly in the lateral and dorsal portions of the mantle
layer, but are scattered throughout the gray matter, and their
axis cylinders grow ventrally and cross over to the opposite side
of the cord through the floor (Figs. 139 and 140), and thus form
the anterior or white commissure of the cord. (3) The cells of the
fiber tracts are scattered throughout the gray matter, and are
characterized by the fact that their axis cylinders enter the white
matter of the same side; here they may bifurcate, furnishing
both an ascending and a descending branch, or may simply turn
in a longitudinal direction. (4) Finally there are found certain
neuroblasts with a short axis cylinder, ramifying in the gray
matter on the same side of the cord. These are found in the
dorsal horn of the gray matter and develop relatively late (about
sixteen days, Ramon y Cajal).

III. The Development of the Brain

Unfortunately the later development of the brain of birds
has not been fully studied. The following account is therefore
fragmentary. It is based mainly on a dissection and sections of
the brain of chicks of eight days' incubation.

Fig. 147 is a drawing of a dissection of the brain of an eight-
day embryo. The left half of the brain has been removed, and
the median wall of the right cerebral hemisphere also. The
details of the cut surfaces are drawn in from sections. Figs. 148

THE NERVOUS SYSTEM

245

and 150 show median and lateral sagittal sections of the same
stage.

The flexures of the brain at this stage are: (1) the cranial
flexure marked by the 'plica encephali ventralis on the ventral
surface, (2) the cervical flexure at the junction of myelencephalon
and cord, somewhat reduced in this stage, and (3) the pontine
flexure, a ventral projection of the floor of the myelencephalon.

c/^.Pi ^- /J

U

Com.dnt. figc.op.

^ ■ — o/A

Fig. 147. — Dissection of the brain of an 8-day chick. For description see
text. The arrows shown in the figure lie near the dorsal and ventral boun-
daries of the foramen of Monro.

ch. PL, Choroid plexus. Com. ant., Anterior commissure. Com. post.,
Posterior commissure. C. str.. Corpus striatum. Ep., Epiphysis. H.,
Hemisphere. Hyp., Hypophysis. L. t., Lamina terminalis. Myeh, Myel-
encephalon. olf., Olfactory nerve, op. N., Optic chiasma. op. L., Optic
lobe. Par., Paraphysis. Paren., Parencephalon. pi. enc. v., Phca en-
cephali ventralis. pont. Fl., Pontine flexure. Rec. op., Recessus opticus.
S. Inf., Saccus infundibuli. Tel. med., Telencephalon medium. Th., Tha-
lamus. T. tr., Torus transversus. Tr., Commissura trochlearis.

The lines a-a, b-b, c-c, d-d, e-e, f-f, represent the planes of section A,
B, C, D, E, and F of Fig. 151.

Telencephalon. The telencephalon is bounded posteriorly,
as noted in Chapter VI, by the line drawn from the velum trans-
versum to the recessus opticus. The telencephalon medium has
grown but little since the fourth day, but the hemispheres

246

THE DEVELOPMENT OF THE CHICK

i.p.

y.7-

c.G

y?j.a.

TeJ.wed

■ CA
Nem.
Lt.

fiec. op.
C/j.op.

' S./nf.

i DJ/yp.
Vas.

l^/O.

Aom

Fig. 148. — Median sagittal section of an embryo of eight days.

a. A., Aortic arch. AIL, Allantois. An., Anus. A. o. m., Om-
phalomesenteric artery. B. F., Bursa Fabricii. b. P., Basilar plate.
C. A., Anterior commissure, c. C, Central canal. Ch. op., Optic
chiasma. C. p., posterior Commissure. CI., Cloaca. Cr., Crop,
d. Ao., Dorsal aorta. D. Hyp., Duct of the hypophysis. Ep., Epi-
physis. Fis. Eus., Fissura Eustachii. Hem., Surface of hemisphere
barely touched by section. Hyp., Hypophysis. L. t., Lamina ter-
minalis. n. A. 8, neural arch of the eighth vertebra. Nas., Nasal

THE NERVOUS SYSTEM 247

have expanded enormously, particularly anteriorly and dorsally,
and their median surfaces are flattened against one another in
front of the lamina terminalis, which forms the anterior boundary
of the telencephalon medium (Figs. 148, 149). Posteriorly the
cerebral hemispheres extend to about the middle of the dien-
cephalon and their lateral faces are rounded. The lateral walls
of the hemispheres have become enormously thickened to form
the corpora striata (Figs. 147 and 151 A), and the superior and
lateral walls have remained relatively thin, forming the mantle
of the cerebral hemispheres (pallium). Thus the cavity of the
lateral ventricle is greatly narrowed.

The dissection (Fig. 147) shows the corpus striatum of the
right side forming the lateral wall of the hemisphere, and extend-
ing past the aperture (foramen of Monro) between the lateral
and third ventricles tow^ards the recessus opticus, where it comes
to an end.

The olfactory part of the hemispheres is not well differen-
tiated from the remainder in the chick embryo of eight days.
There is, however, a slight constriction on the median and ventral
face (Fig. 147) which may be interpreted as the boundary of the
olfactory lobe.

The telencephalon medium is crowded in between the hemi-
spheres and the diencephalon; its cavity forms the anterior end
of the third ventricle, and communicates anteriorly through two
slits, the foramina of Monro, with the lateral ventricles in the
hemisphere. In Fig. 147, the upper and lower boundaries of
the foramen of Monro, are indicated by the grooves on either
side of the posterior end of the corpus striatum. A hair intro-
duced from the third ventricle into the lateral ventricle through
the foramen of Monro in the position of the arrow in Fig. 147,
can be moved up and down over the whole width of the striatum.
The lateral walls of the telencephalon medium are formed by
the posterior ends of the corpora striata and are therefore very
thick.

The lamina terminalis passes obliquely upwards and forwards

cavity. Oes., Oesophagus, p. A., Pulmonary arch, par., Paraphysis. P. C,
Pericardial cavity. Rec. op., Recessus opticus. R., Rectum. S. Inf., Saccus
infundibuli. T., Tongue. Tel., Med. Telencephalon medium. Tr., Trachea.
V. 1, 10, 20, 30, First, tenth, twentieth and thirtieth vertebral centra, r. A..
right auricle. Vel. tr., Velum transversum. V. o. m., Omphalomesenteric
vein. V. umb., Umbilical vein.

248

THE DEVELOPMENT OF THE CHICK

from the recessus opticus to the region between the foramina of
Monro. It is very thin, excepting near its center, where it is
thickened to form the torus transversus, containing the anterior
commissure. At its dorsal summit it is continuous with the
roof of the telencephalon medium, which has formed a pouch-
like evagination, the paraphysis. Just behind the paraphysis

Fig. 149. — Median sagittal section of the brain of a chick embryo of 7

days. (After v. Kupffer.)

c., Cerebellum, ca., Anterior commissure, cd., Notochord. ch.. Pro-
jection of the optic chiasma. cp., Posterior commissure, e., Epiphysis,
e'., Paraphysis. hy., Hypophysis. I., Infundibulum. It., Lamina termi-
nalis. Lop., Optic lobe. M., Mesencephalon. Mt., Metencephalon.
opt., Chiasma of the optic nerves, p., Parencephalon. ro., Recessus
opticus, s., Saccus infundibuli. se., Synencephalon. tp., Mammillary
tubercle, tp., Tuberculum posterius. tr., Torus transversus. Tr., De-
cussation of the trochlear nerves. Va., Velum medullare anterius. Vi.,
Ventriculus impar telencephali. vp., Velum medullare posterius.

is the velum transversum, where the roof bends upwards sharply
into the roof of the diencephalon. The epithelial wall around
the bend is folded to form the choroid plexus of the third ven-
tricle, which is continued forward into the lateral ventricle along

THE XERVOUS SYSTEM 249

the median wall of the hemisphere, ending anteriorly in a free
branched tip (Fig. 147, ch. PI.)

The principal changes in the telencephalon since the third
day comprise: (1) great expansion of the hemispheres and
thickening of the ventro-lateral wall to form the corpora striata;
(2) origin of the paraphysis which arises as an evagination of the
roof just in front of the velum transversum about the middle of
the fifth day; (3) formation of the choroid plexus; (4) origin of
the anterior commissure within the lamina terminalis; (5) develop-
ment of the olfactory region. The general morphology of the
adult telencephalon is thus well expressed at this time.

The Diencephalon has undergone marked changes since the
third day. The roof of the parencephalic division has remained
very thin, and has expanded into a large irregular sac (Figs.
147 and 148), situated between the hinder ends of the hemispheres.
The attachment of the epiphysis has shifted back to the indenta-
tion between parencephalic and synencephalic divisions, and the
epiphysis itself has grown out into a long, narrow tube, dilated
distally, and provided with numerous hollow buds. In the roof
of the synencephalic division the posterior commissure has de-
veloped (Fig. 147). In the floor the chiasma has become a thick
bundle of fibers, and the infundibulum a deep pocket, from the
bottom of which a secondary pocket (saccus infundibuli) is grow-
ing out in contact with the posterior face of the hypophysis.
Following the posterior wall of the infundibulum in its rise, we
come to a slight elevation, the rudiment of the mammillary
tubercles; just beyond this is a transverse commissure (the in-
ferior commissure) ; and the diencephalon ends at the tuberculum

posterius.

The hypophysis has become metamorphosed into a mass of
tubules enclosed within a mesenchymatous sheath; the stalk is
continuous with a central tubule representing the original cavity
from which the other tubules have branched out (Fig. 148), and
it may be followed to the oral epithelium from which the whole
structure originally arose. (See note at end of this chapter.)

The lateral walls of the diencephalon have become immensely
thickened, both dorsally and ventrally, and a deep fissure (Fig.
147) is found on the inner face at the anterior end, between the
dorsal and ventral thickenings. The deepest part of the fissure
is a short distance behind the velum transversum; from this a

250

THE DEVELOPMENT OF THE CHICK

'""W^: K.

tf

Bth^ \ -'^ ^ r - " ^'^^^^. Go//

/ .

f y''

.i^

AIJ/^.

/

^30

Fig. 150. — Lateral sagittal section of an embryo of 8 days. Right side of
the body.
All. N., Neck of the allantois. Cbl., cerebellum. Cr., Crop. E. T., Egg

THE NERVOUS SYSTEM 251

short spur runs forward, a still shorter one ventrally, and the
longest arm extends backwards, gradually fading out beyond
the middle of the diencephalon. This fissure is not a continuation
of the sulcus Monroi, or backward prolongation of the foramen
of Monro, but is, on the contrary, entirely independent.

The lateral thickenings of the diencephalon constitute the
thalami optici, each of which may be divided into epithalamic,
mesothalamic, and hypothalamic subdivisions. In the chick at
eight days there is a deep fissure between the epi- and meso-
thalamic divisions (the thalamic fissure. Fig. 147). The substance
of the epithalamus forms the ganglion habenulse. The meso-
thalamic and hypothalamic divisions are not clearly separated.
The transition zone between the diencephalon and mesencephalon
is sometimes called the metathalamus.

The mesencephalon has undergone considerable changes since
the third day. The dorso-lateral zones have grown greatly in
extent, at the same time becoming thicker, and have evaginated
in the form of the two large optic lobes. Hence the median
portion of the roof is sunk in between the lobes (Fig. 147), and is
much thinner than the walls of the lobes. The dorso-lateral
zones and roof thus form a very distinct division of the mesen-
cephalon, known as the tectum lohi optici. The ventro-lateral
zones and floor have thickened greatly and form the basal divi-
sion of the mesencephalon. The ventricle of the mesencephalon
thus becomes converted into a canal (aqueduct of Sylvius), from
which the cavities of the optic lobes open off.

In the metencephalon likewise there is a sharp distinction
between the development of the dorso-lateral zones and roof,
on the one hand, and the ventro-lateral zones and floor on the
other. From the former the cerebellum develops in the form
of a thickening overhanging the fourth ventricle. This thick-
ening is relatively inconsiderable in the middle line (cf. Figs. 148
and 150). Thus the future hemispheres of the cerebellum are

tooth. Eust., Eustachian tube. Gn. 1, 13, First and thirteenth spinal
granglia. Gon., Gonad. Hem., Hemisphere. Lag., Lagena. Lg., Lung. M.,
Mantle of Hemisphere. Msn., Mesonephros. Olf. L., Olfactory lobe. Olf.
N., Olfactory nerve. P. C, Pericardial cavity. Pz. 5, The fifth post-zyga-
pophysis. R. C. 1, 2, Last two cervical ribs. R. th. 1, 5, First and fifth tho-
racic ribs. S. pc-per., Septum pericardiaco-peritoneale. S'r., Suprarenal.
Symp., Main trunk of the sympathetic. Str., Corpus striatum. V. 1, 10,
20, 30, First, tenth, twentieth and thirtieth vertebral arches. V. C. I., Vena
cava inferior. V. L. L., Ventral ligament of the liver.

252 THE DEVELOPMENT OF THE CHICK

indicated. The surface is still smooth at the eighth day, but
on the tenth and eleventh days folds of the external surface
begin to extend into its substance, without, however, invaginat-
ing its entire thickness. These are the beginnings of the cere-
bellar fissures.

The floor and ventro-lateral zones of the metencephalon enter
into the formation of the pons.

In the roof of the isthmus, or constricted region between
cerebellum and mesencephalon, is found a small commissure
produced by decussation of the fibers of the trochlearis (Fig. 147).

In the wall of the myelencephalon the neuromeres have dis-
appeared. The thin epithelial roof has become more expanded
in the anterior part (Figs. 147 and 148). Floor and sides have
become greatly thickened.

Commissures. The brain commissures existing at eight days
are the anterior, posterior, inferior, and trochlearis (Fig. 149).
In the next four or five days two more appear, viz., the com-
missura pallii anterior (Kupffer), corresponding to the corpus
callosum of mammalia and the commissura habenularis.

The development of the various nuclei and fiber tracts of
the bird's brain is entirely unknown and affords an interesting
topic for research.

IV. The Peripheral Nervous System

The peripheral nervous system comprises the nerves which
span between peripheral organs and the central nervous system.
There are fifty pairs in a chick embryo of eight days, of which
twelve innervate the head, and thirty-eight the trunk, distin-
guished respectively as cranial and spinal nerves. It is con-
venient for purposes of description to consider cranial and spinal
nerves separately, and to take up the spinal nerves first because
they are much more uniform in their mode of development
than the cranial nerves, and also exhibit a more primitive or
typical condition, on the basis of which the development of the
cranial nerves must be, in part, at least, explained.

The Spinal Nerves. Ear-h spinal nerve may be divided into
a somatic portion related primarily to the somatopleure and axis of
the embryo, and a splanchnic portion related primarily to the
splanchnopleure and its derivatives. In each of these again a
motor and sensory component may be distinguished. Thus each

THE NERVOUS SYSTEM

253

y&/./f

'S.S^r.

D

- '/f.

str

l'JeJ./7]^o'.)

W^^

,op.L.

Tr ^

#

B

^//.if^-'

Fig. 1.51. — Six transverse sections through the brain of an 8-day chick in
the planes represented in Fig. 147.
Cbl., Cerebelhim. F. M., Foramen of Monro. Gn. V., Ganghon of the
trigeminus. Isth., Isthmus. It. d., Diverticuhmi of the iter. lat. V.,
Lateral ventricle. Other abbreviations as before (Fig. 147).

254 THE DEVELOPMENT OF THE CHICK

spinal nerve has four components, viz., somatic motor, somatic
sensor}^, splanchnic motor, and splanchnic sensory, the two latter
constituting the so-called sympathetic nervous system. It is
obvious, of course, that the splanchnic components must be
missing in the caudal nerves. The somatic and splanchnic com-
ponents will be considered separately.

Somatic Components. Each spinal nerve arises from two roots,
dorsal and ventral (Fig. 145). The fibers of the former arise from
the bipolar neuroblasts of the spinal ganglia; the fibers of the ven-
tral root, on the other hand, arise from a group of neuroblasts in
the ventral portion of the cord. The roots unite in the interver-
tebral foramen to form the spinal nerve. Typically, each spinal
nerve divides almost immediately into three branches, viz., a dor-
sal branch, a ventral branch, and a splanchnic branch to the sym-
pathetic cord; the last is known as the ramus communicans.

Fig. 145 represents a section passing through the twentieth
spinal nerve of an eight-day chick. The dorsal and ventral roots
unite just beneath the spinal ganglion; fibers are seen entering
the sympathetic ganglion (ramus communicans); the ventral
branch passes laterally a short distance where it is cut off;
beyond this point it can be traced in other sections in the
next posterior intercostal space more than half-way round the
body-wall; that is, as far as the myotome has extended in its
ventral growth. The dorsal branch arises at the root of the
ventral and passes dorsally in contact with the ganglion to
branch in the dorsal musculature and epidermis. This nerve may
be regarded as typical of the spinal nerves generally.

There are thirty-eight spinal nerves in an embryo of eight
days. The first two are represented only by small ventral roots.

The first two spinal ganglia are rudimentary in the embryo and
absent in the adult, hence the ganglion illustrated in Fig. 145 is the
eighteenth of the functional series (see Fig. 149) ; it lies between the
nineteenth and twentieth vertebra?.

The fourteenth, fifteenth, and sixteenth are the principal
nerves of the brachial plexus, and have unusually large ganglia.
The twenty-third to the twenty-ninth are the nerves of the leg
plexus, the thirtieth to the thirty-second innervate the region
of the cloaca and the remainder are caudal. The special mor-
phology of the spinal nerves does not belong in this description.

THE NERVOUS SYSTEM 255

There are one or two vestigial ganglia behind the thirty-eighth nerve,
evidently in process of disappearance at eight days.

The early history of the spinal nerves is as follows: The axis
cylinder processes of the fibers begin to grow^ out from the neuro-
blasts about the third day (cf. p. 235). At this time the myo-
tomes are in almost immediate contact with the ganglia; thus
the fibers have to cross only a very short space before they enter
the myotome. The further growth is associated with the growth
and differentiation of the myotome between which and the
embryonic nerve there is a very intimate relation of such a sort
that the nerve follows the myotome and its derivatives in all
changes of position. Thus nerves do not need to grow long
distances to establish their connections, but these are formed
at a very early period. This accounts for the motor fibers; the
way in which the sensory fibers, that arise from the spinal ganglia,
reach their termination is not known.

Sheath-cells and Cell-chain Hypothesis. No embryonic nerve
consists entirely of axones, but, from the start, each nerve trunk
contains numerous nuclei. The latter belong to cells which have
been given two radically different interpretations, corresponding
to two distinct theories concerning the neuraxone.

(1) The first theory, knowm as the neurone theory, is the one
tacitly followed in the preceding description and may be stated
as follows: the nerve-cell, dendrites and axone, including the
terminal arborization, constitute a single cellular individual or
unit, differentiated from the neuroblast alone. The nuclei in
the embryonic nerves therefore belong to cells that are foreign
to the primary nerve. Their function is to form the various
sheaths of the nerves, viz., the sheaths of the individual axones
and the endo-, peri-, and epineurium. The sheath of Schwann
arises from such cells that envelop the individual fibers at suitable
distances and spread longitudinally until neighboring sheath cells
meet; each such place of meeting constitutes a node of Ranvier.
Until recently it has been universally believed that the sheath
cells arose from the mesenchvme; but recent observations on Am-
phibia and Selachia have shown that they arise from the ganglia
in these forms; their original source is therefore the ectoderm. It
is probable that they have the same origin in the chick, though this
has not been demonstrated by direct observation or experiment.

(2) The second theory is known as the cell-chain hypothesis.

256 THE DEVELOPMENT OF THE CHICK

According to this the axones of peripheral nerves arise as differ-
entiations of the sheath-cells in situ; continuity of the axone is
established by arrangement of these cells in rows, and union
with the neuroblast is essentially secondary. The entire axone
is thus by no means an outgrowth of the neuroblast; at most its
proximal portion is.

Bethe (1903) expresses the idea thus: "Between the cord of
the embryo and the part to be innervated there is formed primarily
a chain of nuclei around which the protoplasm is condensed.
This is fundamentally an extended syncytium in which the nuclei
of the neuroblasts and of the nerve-primordium lie. Within
the denser protoplasm which appears as the body of the nerve-
cells, axones differentiate by condensation, and these extend
from one cell to the next, and so on to the condensations which
are called neuroblasts. The differentiated axones tend more
and more to occupy the center of the embryonic nerve, where
they appear to lie free, though as a matter of fact they are still
embedded in the general plasma which is no longer distinctly
visible on account of its lesser density. Since the axones remain
in firm connection with the neuroblasts, it appears in later stages
as if they were processes of these and had nothing to do with
their original formative cells."

This view is essentially that of Balfour, Beard, and Dohrn;
the neurone hypothesis was first clearly formulated in embryo-
logical terms by His, and has been supported by the investiga-
tions of a considerable number of observers, notably Ramon y
Cajal, Lenhossek and Harrison.

The neurone hypothesis has far stronger embryological sup-
port than the cell-chain hypothesis; moreover, it is the only
possible hypothesis of the development of nerve tracts in the
central system, because cell-chains are entirely lacking here dur-
ing the formation of these tracts. In recent years it has been
demonstrated that isolated neuroblasts in culture media produce
complete axones, sheath cells being entirely absent. Thus the
cell-chain hypothesis has received its final quietus, and is now of
historical interest only. (Burrows 1911, Lewis and Lewis 1911.)
Splanchnic Components (Sympathetic Nervous System). Two
views have been held concerning the origin of the sympathetic
nervous system: (a) that it is of mesenchymal origin, its elements
arising in situ; (b) that it is of ectodermal origin, its elements

THE NERVOUS SYSTEM 257

migrating from the cerebro-spinal ganglia to their definitive
positions. The first view was held by the earlier investigators
and was originally associated with the extinct idea that the spinal
ganglia were mesenchymal in origin; the view has been entirely
abandoned. The second view was partly established with the
discovery that the spinal ganglia are of ectodermal origin, and
that the ganglia of the main sympathetic trunk arise from the
spinal ganglia; but there is some difference of opinion yet in
regard to the peripheral ganglia of the symphathetic system,
and especially the plexuses of Meissner and Auerbach in the walls
of the intestine. However, the preponderance of evidence and
logic favors the view of the ectodermal origin of the entire sym-
pathetic nervous system.

The first clear evidences of the sympathetic nervous system
of the chick are found at about the end of the third or the begin-
ning of the fourth day; at each side of the dorsal surface of the
aorta there is found in cross-section a small group of cells massed
more densely than the mesenchyme and staining more deeply.
Study of a series of sections shows these to be a pair of longi-
tudinal cords of cells beginning in the region of the vagus, where
they lie above the carotids, and extending back to the beginning
of the tail; the cords are strongest in the region of the thorax,
and slightly larger opposite each spinal ganglion. Cells similar
to those composing the cords are found along the course of the
nerves up to the spinal ganglia, and careful study of earlier stages
indicates that the cells composing the cords have migrated from
the spinal ganglia. The two cords constitute the primary sym-
pathetic trunks.

Fig. 152 is a reconstruction of the anterior spinal and sym-
pathetic ganglia of a chick embryo of four days. The primary
sympathetic trunk is represented by a cord of cells enlarged
opposite each ganglion and united to the spinal nerve by a cellu-
lar process, the primordium of the ramus communicans. In the
region of the head the segmental enlargements are lacking.

No other part of the sympathetic nervous system is formed
at this time with the exception of a group of cells situated in the
dorsal mesentery above the yolk-stalk; these are destined to
form the ganglion and intestinal nerves of Remak. They have
not been traced back to the spinal ganglia, but it is probable
that such is their origin.

258 THE DEVELOPMENT OF THE CHICK

In the course of the fourth and fifth days aggregations of
sympathetic gangUon cells begin to appear ventral to the aorta,
and in the mesentery near the intestine. The connection of these
with the primary cord is usually rendered evident by agreement
in structure, and by the presence of intervening strands of cells;
moreover, in point of time they always succeed the primary cord,
so that their origin from it can hardly be doubted.

About the sixth day the secondary or permanent sympathetic
trunk begins to appear as a series of groups of neuroblasts situ-
ated just median to the ventral roots of the spinal nerves. They

r~

Fig. 152. — Reconstruction in the sagittal plane
of the anterior spinal and sympathetic gan-
glia of a chick embryo of 4 days. (After
Neumayer.)
Ceph. S., Cephalic continuation of the sym-
pathetic trunk. S. C, Sympathetic cord. Sg.,
Sympathetic ganghon. sp., Spinal nerve, spg.,
Spinal ganglion. R. C, Ramus communicans.

are thus separated from the spinal ganglia only by the fibers
of the ventral roots between which neuroblasts may be found,
caught apparently in migration from the spinal to the sympa-
thetic ganglion. The number of these secondary sympathetic
ganglia is originally 30, one opposite the main vagus ganglion,
and each spinal ganglion to the twenty-ninth (Fig. 150). Soon
after their origin they acquire three connections by means of
axones, viz., (a) central, with the corresponding spinal nerve-

THE NERVOUS SYSTEM 259

root by means of strong bundles of fibers; (b) peripheral, with
certain parts of the original primary sympathetic cord; (c) longi-
tudinal, the entire series being joined together by two longitudinal
bundles of fibers uniting them in a chain. The central connec-
tions constitute the rami communicantes , and are as numerous as
the sympathetic ganglia themselves; but so close is the approxi-
mation of the sympathetic ganglion to the roots of the spinal
nerves that they are not visible externally, the ganglion appear-
ing to be sessile on the root (Fig. 145); sections, however, show
the fibers. The peripheral connections constitute the various
nerves of the abdominal viscera; these are not metameric;
their number and arrangement is shown in Figure 153.

In the period between the fourth and the eighth da}^ the pri-
mary sympathetic cord becomes resolved into the various ganglia
and nerves constituting the aortic plexus, the splanchnic plexus,
and the various ganglia and nerves of the wall of the intestine.
Remak's ganglion has grown and formed connections with the
splanchnic plexus, and other parts of the primary sympathetic
cord. The details of these various processes are too complex
for full description; they are included in part in Figs. 153 and 154.

Ganglia and Nerves of the Heart. The development of the
cardiac nerves is of special interest on account of its bearing on the
physiological problem of the origin of the heart-beat. The heart
of the chick begins to beat long before any nervous connections
with the central system can have been established; indeed, the
rhythmical pulsation begins at about the stage of 10 somites
when the neural crest is yet undifferentiated, and no neuroblasts
are to be found anywhere. Either, then, the heart-beat is of mus-
cular origin (myogenic), or, if of nervous origin, the nerve-cells
concerned must exist in the wall of the cardiac tube ah initio.

The first trace of nerve-cells is found in the heart of the chick
about the sixth day. These cells are at the distal ends of branches
of the vagus, with which they have grown into the heart. Pre-
vious to this time these neuroblasts are found nearer to the vagus
along the course of the arteries. There can be but little doubt
that they have arisen from the vagus ganglion and that they
reach the heart by migration. Such an origin has been demon-
strated with great probability for all the known nervous elements
of the heart of the chick. (See Wilhelm His, Jr., Die Entwickelung
des Herznervensystems bei Wirbelthieren.)

260

THE DEVELOPMENT OF THE CHICK

CO

CO

-(-3

O) o

o

Si

o

u

o

O ^ r: c^

■■^ 5=: ^ =5

rt c3 t^i X

n T3

IB

Cj

CO

■^ o

+^ fc£__;

i:x

5
o

3 S"^

o M

"tS !>. ^ " 2
• -^ o S 'n '•+J

OQ

fc£

o

I— I

:S - g ^^s

-tJ ^ o >

c -i^ ?- :j s

„. o S ^^

1^ ^ c ^ c

2^ • o c o
^ . o '

-< <J 3 -H ^

2; £

THE NERVOUS SYSTEM

261

If any cardiac nervous elements arise in situ, they certainly
remain undifferentiated until those that have a ganglionic origin
have already entered the heart.

The Cranial Nerves. Tlie nerves of the head exhibit a much
greater degree of heteronomy than the spinal nerves, and, in
spite of much study, knowledge of their embryonic development
is still in a very unsatisfactory condition. The same principles,
however, apply to the development of both cranial and spinal
nerves; the axones of the former like those of the latter arise
either from medullary or ganglionic neuroblasts which are re-
spectively unipolar and bipolar; but the cranial ganglionic and

Fig. 154. — Diagram of the relations of the

parts of the sympathetic nervous system

as seen in the cross-section. (After His,

Jr.)

M., mesentery. Msn., Mesonephros.

Other abbreviations same as Fig. 153.

medullary nerve-nuclei are not similarly segmented, as in the
case of the spinal nerves, and hence the axones are not related
as dorsal and ventral roots of single nerve trunks; nor has the
attempt to interpret the cranial nerves as homologues of dorsal
and ventral roots respectively been successful in the case of the
most important nerves. Moreover, the olfactory and optic nerves
differ from the spinal type even more fundamentally. The olfac-
tory is a sensory nerve that arises apparently from the olfactory

262 THE DEVELOPMENT OF THE CHICK

epithelium, and the optic is really comparable to an intramedul-
lary nerve tract, seeing that its termination lies in a part of the
original wall of the neural tube, viz., the retina.

Groups of medullary neuroblasts giving rise to axones of
motor cranial nerves are located in the brain as follows, according

to His:

Oculo-motor nucleus in the mid-brain.

Trochlearis nucleus in the isthmus.

Motor trigeminus nucleus in the zone of the cerebellum, including

the descending root.
Abducens and facialis nuclei, beyond zone of greatest width

of the fourth ventricle (auditory sac zone).
Glossopharyngeus, vagus, in the region of the calamus scrip-

torius.
Accessorius and hypoglossus, in the region extending to the

cervical flexure.

These constitute the cranial motor nerve nuclei, and are more
or less discontinuous.

The ganglionic nerves or nerve-components of the head arise
from the following primitive embryonic ganglion-complexes:

1. Complex of the trigeminus ganglia.

2. Complex of the acustico-facialis ganglia.

3. Complex of the glossopharyngeus ganglia.

4. Complex of the vagus ganglia.

The early history of these ganglion-complexes has already been
considered; they are called complexes because each forms more
than one definitive ganglion. It is probable also that each con-
tains sympathetic neuroblasts, which may separate out later as dis-
tinct ganglia, thus reseml)ling the spinal sympathetic neuroblasts.

There is no close agreement in the segmentation of the motor
neuroblasts within the brain and that of the ganglion complexes.
For instance, in the region of the trigeminal ganglionic complex,
the motor nuclei of the oculo-motor, trochlearis, and trigeminus
are found, and in the region of the vagus ganglionic complex,
the motor nuclei of vagus, accessorius, and hypoglossus. Thus
the medullary and ganglionic nerves of the head are primitively
separate by virtue of their separate origins. They may remain
entirelv so, as in the case of the olfactory, trochlearis, and abdu-
cens, or they may unite in the most varied manners to form
mixed nerves.

THE NERVOUS SYSTEM 263

The motor nuclei of the oculo-motor, trochlearis, abducens,
and hypoglossus nerves He in the same plane as the motor nuclei
of the spinal nerves, i.e., in the line of prolongation of the ventral
horns of the gray matter. The motor nuclei of the trigeminus,
facialis, glossopharyngeus, vagus, and spinal accessory on the
other hand lie at a more dorsal level, and the roots emerge there-
fore above the level of origin of the others. It will be noted that
these are the nerves of the visceral arches, whereas those cranial
nerves that continue the series of spinal ventral roots innervate
myotomic muscles, like the latter. Similarly the ganglia of the
pharyngeal nerves (V, VII, IX, and X) differ from spinal ganglia
in certain important respects: the latter are derived entirely
from the neural crest, whereas a certain portion of each of the
primary cranial ganglia is derived from the lateral ectoderm of
the head, as noted in the preceding chapter. Thus the pharyn-
geal nerves form embryologically a class by themselves, both
as regards the medullary and also the ganglionic components.

1. The Olfactory Nerve. The embr3'onic origin of the olfactory
nerve has been a subject of much difference of opinion: thus it
has been maintained by a considerable number of w^orkers that
it arises from a group of cells on each side situated between the
fore-brain and olfactory pits; some of these maintained that
these cells arose as an outgrowth from the fore-brain, others
that they came from the epithelium of the olfactory pit, and
yet others that this group of cells, or olfactory ganglion, was
derived from both sources. This group of cells was supposed
by some to include a large number of bipolar neuroblasts, one
process of which grew towards the olfactory epithelium and
the other towards the fore-brain, entering the olfactory lobe
and ending there in terminal arborization. This view is, however,
in conflict with the ascertained fact that the fibers of the fully
formed olfactory nerve are centripetal processes of olfactory
sensory cells situated in the olfactory epithelium.

The most satisfactory account of the origin of the olfactory
nerve in the chick is that of Disse. This author finds two kinds
of cells in the olfactory epithelium of a three-day chick, viz.,
epithelial cells, and germinal cells which become embryonic
nerve-cells or neuroblasts. At this time the olfactory epithelium
is separated from the w^all of the fore-brain by only a very thin
layer of mesenchyme. Early on the fourth day axones arise

264

THE DEVELOPMENT OF THE CHICK

from the central ends of the neuroblasts and grow into the
mesenchyme towards the fore-brain. At the same time groups
of epithelial cells free themselves from the inner face of the
olfactory epithelium, and come to lie between this and the fore-
brain. The axones of the neuroblasts grow between these cells
until they reach the base of the fore-brain over which they spread
out, entering the olfactory lobe about the sixth day (Figs. 155
and 156). In the meantime the peripheral ends of the olfactory
neuroblasts have extended out as broad protoplasmic processes
to the surface of the olfactory epithelium, and thus form the per-
cipient part of the olfactory sense-cells.

Fig. 155. — Olfactory epithelium of a chick embryo of 5
days, prepared by the method of Golgi. (After Disse.)
a, b, and c indicate different forms of neuroblasts in the
olfactory epithelium.

The epithelial cells between fore-brain and olfactory pit, through
which the axones of the olfactory neuroblasts grow, are for the
most part supporting and sheath-cells of the nerve, but they in-
clude a few bipolar neuroblasts (Fig. 156). The latter are to
be considered as olfactory neuroblasts with elongated protoplas-
mic processes.

Rubaschkin finds a ganglion, which he calls ganglion olfactorium
nervi trigemini, situated beneath the olfactory epithelium in a nine-
day chick. The bipolar cells send out processes peripherally which end
in fine branches between the cells of the olfactory mucous membrane,
and centrally, which go by way of the ramus olfactorius nervi
trigemini towards the Gasserian ganglion.

2. The Second Cranial or Optic Nerve. The course of this

THE NERVOUS SYSTEM

265

nerve is entirely intramedullary, the retina being part of the
wall of the embryonic brain; its development will therefore be
considered in connection with the development of the eye.

Fig. 156. — Sagittal section through the head of a chick embryo of 5 days,

showing the floor of fore-brain, olfactory pit, and developing olfactory

nerve between. (After Disse.)

a., Unipolar neuroblasts near the olfactory epithelium, b., Bipolar cell
in the olfactory nerve, c, Unipolar cell near the brain. F. B., Floor of
fore-brain. N'bl., Neuroblast in the olfactory epithelium, olf. Ep., Olfac-
tory epithelium, olf. N., Olfactory nerve, olf. P., Cavity of olfactory pit.

3. The third cranial or oculo-motor nerve arises from a group
of neuroblasts in the ventral zone of the mid-brain near the median
line, and appears external to the wall of the brain at about sixty
hours (about 28-30 somites). At this time it appears as a small
group of axones emerging from the region of the plica encephali

266 THE DEVELOPMENT OF THE CHICK

ventralis, and ending in the mesenchyme a short distance from
its point of origin. At seventy-two hours the root is much
stronger, interpenetrated with mesenchyme and ends between
the optic cup and floor of the brain behind the optic stalk (cf.
Fig. 101). At ninety-six hours the root is broad and fan-shaped,
the nerve itself is comparatively slender, and passes downwards
and backwards behind the optic-stalk where it enters a well-
defined ganglion situated just median to the ophthalmic branch
of the trigeminus; this is the ciliary ganglion; beyond it the
fibers of the oculo-motor turn forward again to enter the region
of the future orbit.

According to Carpenter (1906) the ciliary ganglion arises
from two sources: (a) migrant medullary neuroblasts that pass
out into the root of the oculo-motor, and follow its course to
the definitive situation of the ciliary ganglion, and (b) a much
smaller group of neuroblasts that migrate from the ganglion of
the trigeminus along the ophthalmic branch, and by way of a
ramus communicans to the ciliary ganglion. The adult ciliary
ganglion show\s correspondingly two component parts: (a) a
larger ventral region composed of large bipolar ganglion cells,
and (6) a smaller dorsal region containing small ganglion cells
with many sympathetic characters. It is probable that the
medullary fibers of the oculo-motor nerve are distributed entirely
to the muscles innervated by it, viz., the superior, inferior, and
internal rectus and inferior oblique muscles of the eye. The
fibers arising from the neuroblasts of the ciliary ganglion ter-
minate peripherally in the intrinsic muscles of the eye-ball, and
centrally (in the case of the bipolar cells) in the brain, which
they reach by way of the medullary nerve. The motor branches
leave the trunk of the nerve a short distance centrally to the
ciliary ganglion.

4. The trochlearis or fourth cranial nerve is peculiar inas-
much as it arises from the dorsal surface of the brain in the
region of the isthmus. It arises entirely from medullary neuro-
blasts and innervates the superior oblique muscle of the eye.
Marshall states that it may be readily seen in a five-day embryo;
in an embryo of eight davs it is a slender nerve arising from the
dorsal surface of the isthmus immediately in front of the cere-
bellum ; the fibers of the two sides form a commissure in the roof
of the isthmus (Fig. 148).

THE NERVOUS SYSTEM 267

5. The trigeminus or fifth cranial nerve consists of motor
and sensory portions. The latter arises from the trigeminal
ganglion, the origin of which has already been described. The
ganglionic rudiment appears roughly Y-shaped even at an early
stage (cf. Figs. 105 and 117), the short stem lying against the
wall of the brain and the two branches diverging one in the direc-
tion of the upper surface of the optic cup (ophthalmic branch)
and the other towards the mandibular arch. The original con-
nection of the ganglion with the roof of the neural tube is lost
during the second day and permanent connection is established
during the third day, presumably by growth of axones into the
wall of the brain. The new connection or sensory root of the
trigeminus is attached to the myelencephalon in the region of
greatest width of the fourth ventricle near the ventral portion
of the lateral zone.

During the fourth day the peripheral axones follow the direc-
tion of the ophthalmic and mandibular branches of the ganglion
and grow out farther as the ophthalmic and mandibular nerves;
the former passes forward between the optic vesicle and the wall
of the brain; the latter runs ventrally towards the angle of the
mouth, over which it divides, a smaller maxillary branch entering
the maxillary process of the mandibular arch, and a larger one,
the mandibular nerve, runs into the mandibular arch. (For an
account of the branchial sense organ of the trigeminus, see Chap.

VI.)

A medullary component of the trigeminal nerve arises from
the wall of the brain just median to the ganglionic root during
the fourth day; it runs forward parallel to the ganglionic ophthal-
mic branch, and sends a twig to the ciliary ganglion. Beyond
this point it unites with the ganglionic branch.

A connection of the trigeminus with the olfactory sensory
epithelium is described under the olfactory nerve.

6. The sixth cranial or abducens nerve is stated to arise about
the end of the fourth day. It is a purely motor nerve, and has
no ganglion connected with it; it innervates the external rectus
muscle of the eye. At 122 hours it arises by a number of slender
roots attached to the myelencephalon near the mid- ventral line,
beneath the seventh nerve. Its roots unite into a slender trunk
that runs directly forward beneath the base of the brain to the
region of the orbit. The sixth nerve thus corresponds more

268 THE DEVELOPMENT OF THE CHICK

nearly than any other cranial nerve to a ventral spinal nerve-
root.

7 and 8. The Facial and Auditory Nerves. The ganglia of
these nerves at first form a common mass, the acustico-facialis.
But during the course of the fourth day the anterior and ventral
portion becomes distinctly separated from the remainder and
forms the geniculate ganglion; the remainder then forming the
auditory ganglia (cf. Fig. 102). The acustico-facialis ganglion
complex moves from its original attachment to the dorsal surface
of the brain and acquires a permanent root during the third day,
attached ventrally just in front of the auditory sac.

(a) The seventh cranial or facialis nerve arises during the
fourth day from the geniculate ganglion which is situated just
above the second or hyomandibular branchial cleft. It grows
first into the hyoid arch (posttrematic branch), but towards
the end of the fourth day a small branch arises just above the
cleft and arches over in front of it and runs down the posterior
face of the mandibular arch (pretrematic branch). The origin of
the motor components is not known.

(h) The further history of the auditory nerve is considered
with the development of the ear.

9. The ganglion of the ninth cranial or glossopharyngeal nerve
(ganglion petrosum cf. Fig. 102) arises from the anterior part of
the postotic cranial neural crest as already described. Early on
the fourth day the ganglionic axones enter the base of the brain
just behind the auditory sac and establish the root, which con-
sists of four or five parts on each side. From the ganglion which
is situated at the summit of the third visceral arch a strong
peripheral branch develops on the fourth day, and extends into
the same arch; a smaller anterior branch develops a little later
which passes over the second visceral pouch and enters the
second visceral arch. About the same time an anastomosis is
formed with the ganglion of the vagus.

10. The tenth cranial or vagus (pneumogastric) nerve is very
large and complex. Its ganglion very early shows two divisions,
one near the roots (ganglion jugulare) and the other above the
fourth and fifth visceral arches (ganglion nodosum cf. Fig. 102).
It arises by a large number ot fine rootlets on each side of the
hind-brain behind the glossopharyngeus, and the roots converge in
a fan-like manner into the proximal ganglion; from here a stout

THE NERVOUS SYSTEM 269

nerve passes ventrally and enters the ganglion nodosum situated
above the fourth and fifth visceral arches. Branches pass from
here into the fourth and fifth arches, and the main stem is con-
tinued backward as the pneumogastric nerve s.s. From the hinder
portion of the spreading roots a strong commissure is continued
backward parallel to and near the base of the neural tube as far
as the fifth somite; this is provided with three small ganglion-like
swellings. This condition is found about the end of the fourth
day. Later this commissure unites with the main sympathetic
trunk, and part of the vagus ganglion separates from the remain-
der as the ganglion cervicale primum of the sympathetic trunk.

During the fifth and sixth days the main stem of the vagus
grows farther back and innervates the heart, lungs, and stomach.
Neuroblasts of the sympathetic system accompany the vagus
in its growth, and form the various ganglion cells of the heart,
and other organs innervated by the vagus.

During the fifth and sixth days the ganglion nodosum, which
originally lay at the hind end of the pharynx, is carried down
with the retreat of the heart into the thorax, and on the eighth
day it is situated at the base of the neck in close contact with
the thymus gland.

11. The Eleventh Cranial or Spinal Accessory Nerve. No ob-
servations on the development of this nerve in the chick are
known to me.

12. The twelfth cranial or hypoglossus nerve appears on the
fourth day as two pairs of ventral roots opposite the third and
fourth mesoblastic somites; each root is formed, like the ventral
roots of the spinal nerves, of several bundles that unite in a com-
mon slender trunk; ganglia are lacking, as in the first and second
cervical nerves. The roots of the hypoglossus are a direct con-
tinuation of the series of ventral spinal roots, and as they are
related to somitic muscle plates in the same way as the latter,
there can be no doubt of their serial homology with ventral roots
of spinal nerves. The first four mesoblastic somites are subse-
quently incorporated in the occipital region of the skull, and
thus the hypoglossus nerve becomes a cranial nerve. No nerves
are formed in connection with the first and second mesoblastic
somites. As the occipital region of the skull forms in the region
of the occipital somites, two foramina are left on each side for
exit of the roots of the hypoglossus (Figs. 150 and 244).

270 THE DEVELOPMENT OF THE CHICK

During the fourth and fifth days the nerve grows back above
the roof of the pharynx, then turns ventrally behind the last
visceral pouch and forward in the floor of the pharynx.

According to Chiarugi minute ganglia are formed in the second,
third, and fourth somites: but they soon degenerate (fourth day) without
forming nerves.

Note: The structure called "hypophysis" on p. 249, sometimes called
Rathke's pouch, forms only the anterior lobe or glandular part of the hy-
pophysis of adult anatomy; the posterior lobe of the hypophysis is derived
from the structure called " saccus infundibuli " in this chapter, which is a deri-
vation of the floor of the brain.

CHAPTER IX
ORGANS OF SPECIAL SENSE

I. The Eye

The development of the eye up to the stage of 36 somites has
been already described. We shall now consider the subsequent
changes in the following order: (1) optic cup, (2) vitreous body,
(3) lens, (4) anterior chamber, cornea, iris, etc., (5) choroid and
sclerotic, (6) the conjunctival sac and eyelids, (7) the choroid fis-
sure and the optic nerve.

1. The optic cup at the stage of 36 somites is composed of
two layers, an inner, thicker layer, known as the retinal layer,
and an outer, thinner layer, known as the pigment layer; these
are continuous with one another at the pupil and choroid fissure.
The inner and outer layers come into contact first in the region
of the fundus, and the cavity of the original optic vesicle is gradu-
ally obliterated. The choroid fissure is in the ventral face of
the optic cup; it is very narrow at this time, and opens distally
into the pupil; centrally it ends at the junction of optic stalk
and cup, not being continued on the stalk as it is in mammals (Fig.
157).

The walls of the optic cup may be divided into a lenticular
zone {pars lenticularis or pars cceca) and a retinal zone; the former
includes the zone adjacent to the pupil, not sharply demarcated
at first from the remainder or retinal zone, but later bounded dis-
tinctly by the ora serrata. The retinal zone alone becomes the
sensitive portion of the eye; the lenticular zone develops into the
epithelium of the iris and ciliary processes.

In the lenticular zone the inner and outer layers become actu-
ally fused, but in the retinal zone they may always be separated;
indeed, in most preparations they are separated by an actual
space produced by unequal shrinkage.

The differentiation of the lenticular from the retinal zone
begins about the seventh day, when a marked difference in thick-

271

272

THE DEVELOPMENT OF THE CHICK

ness appears. The transition from the thinner lenticular to the
thicker retinal zone soon becomes rather sudden in the region of
the future ora serrata. About the eighth or ninth day a further
differentiation arises within the lenticular zone, marking off the
regions of the iris and ciliary processes (Fig. 159). The region

ep ^es p r

157 ■ 158

Fig. 157. — Section through the eye of a chick embryo at the

beginning; of the fourth day of incubation. (After Froriep.)

ch. Fis. I., Lip of the choroid fissure. Di., Lateral wall of the
diencephalon. V, \", Distal and proximal walls of the lens, st.,
Optic stalk.

Fig. 158. — Section of the distal portion of the eye of a chick,

second half of the fifth day of incubation. (After Froriep.)

c. ep. int., Internal epithelium of the cornea. Corn, pr., Cornea
propria. Ect., Ectoderm, ep.. Epidermis. ir.,Iris. mes.. Meso-
derm, p., Pigment layer of the optic cup. r., Retinal layer of
the optic cup.

of the iris is a narrow zone bounding the pupil in which the two
la3'ers of the optic cup become blended so that pigment from
the outer layer invades the inner layer; the epithelia are decidedly

ORGANS OF SPECIAL SENSE

273

u.e. /.

C/2.

cj7.

irjs -

ant. (•/?.
Corri.

ITj^

^ — op.n .

■olf.

/i .m

Fig. 159. — Frontal section of the eye of an eight day chick. Shrinking in
the process of preparation has caused a separation between the retinal and
pigment layers,
ant. ch., Anterior chamber of the eye. ch., Choroid coat, cil., Ciliary
processes. Corn., Cornea. 1. e. 1., Lower eyelid, n. m., Nictitating mem-
brane, olf., Olfactory sac. op. n., Optic nerve, o. s., Ora serrata. p.,
Pigment layer of the optic cup. post, ch., Posterior chamber of the eye.
ret.. Retina, scl., Sclerotic coat. scl. C, Sclerotic cartilage, u. e. 1., Upper
eyelid.

thinner than in the ciliary region. The mesenchyme overlying
the iris early becomes condensed to form the stroma of the iris;
the epithelia form the uvea of the developed iris (Fig. 159).
The muscles of the iris (sphincter pupillse) are stated by

274

THE DEVELOPMENT OF THE CHICK

Nussbaum, Szily, and Lewis to arise from epithelial buds of the
pupillary margin and the adjacent portion of the pigment layer
of the iris. The marginal buds (Fig. 160) begin to form during
the seventh day, the more peripheral ones somewhat later; the
former are less numerous and larger than the latter. The
observations are well supported, and appear to leave no doubt
that the specificity of the ectoderm cells of the iris is not fixed.
According to Lewis the wandering pigmented cells of the ante-
rior portion, at least, of the choroid also arise from the pigment
layer of the optic cup.

The ciliary processes begin to form from the ciliary region
of the lenticular zone on the eighth day (Fig. 159) ; the epithelium

^M" Sph.
Sfih. ^-"

ES.

3pM

B.

Fig. 160. — Two sections of the pupillary margin of the eye of a chick of 13
days' incubation. A., X 260. B., 130. (Afte