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The brain of the tiger salamander, Ambystoma tigrinum.
Chicago,Univ. of Chicago Press[1948]
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The tiger salamander, Ambystoma tigrinum, natural size. The figure at the top is a midwestern
adult form, after G. K. Noble ('31, by permission of the McGraw-Hill Book Co.).
Below this is a photograph of a midlarval stage by Professor S. H. Bishop. The two lower
figures show late larval and adult stages of the eastern form, the adult with brilliant yellow
"tiger" stripes. (Courtesy of the American Museum of Natural History.)
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Amby stoma tigrinum
Professor Emeritus of Neurology
The University of Chicago
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The University of Chicago Press, Chicago 37
Cambridge University Press, London, N.W. 1, England
W. J. Gage & Co., Limited, Toronto '2B, Canada
Copyright 19^8 by The University of Chicago. All rights reserved
Published 191,8. Composed and printed by The University
OF Chicago Press, Chicago, Illinois, U.S.A.
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THIS work reports the results of a search, extending over fifty
years, for the fundamental plan of the vertebrate nervous system
as revealed in generalized form in the amphibians. In these small
brains we find a simplified arrangement of nerve cells and fibers
with a pattern of structural organization, the main features of which
are common to all vertebrates. From this primitive and relatively
unspecialized web of tissue it is possible to follow the successive
steps in progressive elaboration as the series of animals from salamanders
to men is passed in review.
This is a record of personal observation, not a compilation of the
literature. It is presented in two parts, which differ in content and
method of treatment of the data.
The first part gives a general over-all view of the structure without
details, followed by physiological interpretation and discussion of
some general principles of embryologic and phylogenetic morphogenesis.
This part, with the accompanying illustrations, can be
read independently of the histological details recorded in the second
The second part presents the evidence upon which conclusions are
based, drawn from my own previously published descriptions, to
which references are given, together with considerable new material.
This part is designed for specialists in comparative neurology and as a
guide for physiological experiments. The second part supplements the
first, to which the reader must make frequent reference.
Grateful acknowledgment is made to many colleagues for generous
assistance and criticism, and particularly to Doctors Elizabeth C.
Crosby, Davenport Hooker, Olof Larsell, Gerhardt von Bonin,
Ernst Scharrer, and W. T. Dempster. In the preparation of the manuscript
invaluable help was given by Miss Anna Seaburg.
I am indebted to Dr. Paul G. Roofe for permission to copy one of
his pictures, shown here as figure 86A. The American Museum of
Natural History, New York, generously furnished the two photographs,
taken from life, shown at the bottom of the Frontispiece.
These are copyrighted by the Museum. One of them has been previously
published by the Macmillan Company in Hegner's Parade
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of the Animal Kingdom (p. 289). The photograph of the midlarval
stage was kindly suppHed by Professor Sherman C. Bishop of the
University of Rochester. The upper figure is from G. K. Noble's
Biology of the Amphibia, courtesy of the McGraw-Hill Book Company
(copyrighted, 1931). Figures 1, 2C, and 86-113 are reproductions
of figures previously published by the author in the Journal of
Comparative Neurology and used here by courtesy of the Wistar Institute
of Anatomy and Biology, publishers of that Journal. The
other figures are originals prepared for this work.
Money for the prosecution of the work and for financing its publication
was liberally supplied by the Dr. Wallace C. and Clara A.
Abbott Memorial Fund of the University of Chicago.
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I. Salamanders and Their Brains JJ
The salamanders, 3. — The scope of this inquiry, 4. — The plan of
this book, 6.— Sources and material, 10.— Development of the brain,
11. — The evolution of brains, 13
II. The Form and Subdivisions of the Brain 18
Gross structure, 18.— Ventricles, "24.— Meninges, chorioid plexuses,
and blood vessels, 'id
III. Histological Structure '28
General histology, 38.— The neuropil, '29.— The ventrolateral
peduncular neuropil, 3,3
IV. Regional Analysis 4<>
The subdivisions, spinal cord to pallium, 41.— The commissures, ;5;5.
^Conclusion, 56
V. Functional Analysis, Central and Peripheral 57
The longitudinal zones, 57. — The sensory zone, 58. — The motor
zone, 60. — The intermediate zone, 64.— The functional systems, 65
VI. Physiological Interpretations '^^
Apparatus of analysis and synthesis, 70. — The stimulus-response
formula, 7^2. — Reflex and inhibition, 73.— Principles of localization
of function, 8'2
Vll. The Origin and Significance of Cerebral Cortex .... 91
The problem, 91. — Morphogenesis of the cerebral hemispheres,
9*2. — The cortex, 98. — Physiology and psychology, 106
VIII. General Principles of Morphogenesis 109
Morphogenic agencies, 109. — Morphological landmarks, 116. — The
future of morphology, 120
IX, Spinal Cord and Bulbo-spinal Junction 1'25
The spinal cord and its nerves, 125. — The bulbo-spinal junction,
X. Cranial Nerves l-^l
Development, 131. — Survey of the functional systems, 132
XI. Medulla Oblongata ^^'^
Sensory zone, 153. — Intermediate zone, 156. — Motor zone, 157. —
Fiber tracts of the medulla oblongata, 158.— The lemniscus
sy.stems, 162
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XII. Cerebellum ^'^
Brachium conjunctivum, 176.— The cerebellar commissures, 177.—
Proprioceptive functions of the cerebellum, 178
XIII. Isthmus 1'^^
Development, 179.— Sensory zone, 181.— Intermediate zone, 182.
—Motor zone, 182.— White substance, 186.— Isthmic neuropil, 187.
— Physiological interpretation, 189
XIV. Interpeduncular Nucleus l^^
Comparative anatomy, 191.— Histological structure, 193.—
Afferent connections, 197.— Efferent connections, 201.— Interpretation,
202. — Conclusion, 210
XV. Midbrain ^^'^
Development, 212.— Sensory zone, 214.— Intermediate zone, 215.
— Motor zone, 216
XVI. Optic and Visual-motor Systems 219
Optic nerve and tracts, 219.— Tectum opticum, 222.— Tectooculomotor
connections, 226.— Visual functions, 227
XVII. Diencephalon ^^^
General features, 230.— Development, 231.— Epithalamus, 234.—
Dorsal thalamus, 236.— Ventral thalamus.— 239.— Hypothalamus,
XVIII. The Habenula and Its Connections 247
The di-telencephalic junction, 247.— Fornix, 254.— Stria terminalis,
255.— Stria medullaris thalami, 256.— Fasciculus retroflexus, 261
XIX. The Cerebral Hemispheres 265
Subdivisions of the hemisphere, 265.— The olfactory system, 266
XX. The Systems of Fibers 270
The basal forebrain bundles, 271.— The tegmental fascicles, 275.—
Fasciculus tegmentalis profundus, 286
XXI. The Commissures ^^^
General considerations, 289.— The dorsal commissures, 292.— The
ventral commissures, 294
Abbreviations for All Figures ^^^
Index ^99
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SALAMANDERS are shy little animals, rarely seen and still more
rarely heard. If it were not so, there would be no salamanders at
all, for they are defenseless creatures, depending on concealment for
survival. And yet the tiger salamander, to whom this book is dedicated,
is appropriately named, for within the obscurity ol its contracted
world it is a predaceous and voracious terror to all humbler
This salamander and closely allied species have been found to be
so well adapted for a wide range of studies upon the fundamental
features of growth and differentiation of animal bodies that during
the last fifty years there has been more investigation of the structure,
development, and general physiology of salamanders than has been
devoted to any other group of animals except mankind. The reason
for this is that experimental studies can be made with these amphibians
that are impossible or much more difficult in the case of
other animals. This is our justification for the expenditure of so much
hard work and money upon the study of the nervous system of these
insignificant little creatures.
The genus Amby stoma is widely distributed throughout North
America and the tiger salamander, A. tigrinum, is represented by
several subspecies. The individuals vary greatly in size and color,
and the subspecies have different geographical distribution, with
some overlap of range (Bishop, '43). The subspecies, A. tigrinum
tigrinum (Green), ranges from New York southward to Florida and
westward to Minnesota afid Texas. It has a dark-brown body crossed
by bright-yellow stripes, as shown in the lower figure of the Frontispiece.
The species probably was named for these tiger-like markings,
not for its tigerish ferocity. The upper figure of the Frontispiece is an
adult of a western form, with less conspicuous markings. Other subspecies
range as far to the northwest as Oregon and British Columbia.
Several other species of Ambystoma are found in the same areas as
A. tigrinum.
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Zoological names. — The approved names of the genus and larger groups to which
reference is here made, as given in a recent official list (Pearse, '36), are as follows:
Salienta, to replace Anura
Caudata, to replace Urodela
Ambystoma, to replace Amblystoma
Amby stoma (or Siredon) maculatum has priority over A. punctatum. The names,
Anura, Urodela, and Amblystoma, are used throughout this text because they are
so commonly found in current literature that they may be regarded as vernacular
From the dawn of interest in the minute structure of the human
brain, it was recognized that the simpler brains of lower vertebrates
present the fundamental features of the human brain without the
numberless complications which obscure these fundamentals in
higher animals. This idea motivated much research by the pioneers
in neuroanatomy, and it was pursued systematically by L. Edinger,
H. Obersteiner, Ramon y Cajal, C. L. Herrick, J. B. Johnston,
Ariens Kappers, and many others. In 1895, van Gehuchten wrote
that he was engaged upon a monograph on the nervous system of the
trout, "impressed by the idea that complete information about the
internal organization of the central nervous system of a lower vertebrate
would be of great assistance as our guide through the complicated
structure of the central nervous system of mammals and of
man." The few chapters of this monograph which appeared before
his untimely death intensify our regret that he was not permitted to
complete this work. Van Gehuchten's ideal has been my own inspiration.
Our primary interest in this inquiry is in the origins of the structural
features and physiological capacities of the human brain and
the general principles in accordance with which these have been developed
in the course of vertebrate evolution. This is a large undertaking.
What, then, is the most promising approach to it.'^ My
original plan was, first, to review all that has been recorded about the
anatomy and physiology of the nervous systems of backboned animals,
to arrange these animals in the order of their probable diverse
specialization from simple to complex in the evolutionary sequence,
then to select from the series the most instructive types and subject
them to intensive study, in the expectation that the principles underlying
these morphological changes would emerge.
So ambitious a plan, however, is far too big to be encompassed
within the span of one man's lifetime. The fact-finding research is
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extremely laborious and exacting; and, during the fifty years which
have elapsed since my project was formulated, the descriptive literature
has increased to enormous volume. This literature proves to be
peculiarly refractory to analysis and interpretation. Until recently
this vast accumulation of factual knowledge has contributed disappointingly
little to the resolution of the fundamental problems of
human neurology. Nevertheless, the method is sound, and this slow
growth is now coming to fruition, thanks to the conjoint labors of
specialists in many fields of science. What no individual can hope to
do alone can be done and has been done in co-operative federation,
as illustrated, for instance, by the Kappers, Huber, and Crosby
team and their many collaborators.
Traditionally, comparative neurology has been regarded as a subdivision
of comparative anatomy, and so it is. But it is more than
this. The most refined methods of anatomical analysis cannot reveal
the things that are of greatest significance for an understanding of the
nervous system. Our primary interest is in the behavior of the living
body, and we study brains because these organs are the chief instruments
which regulate behavior. As long as anatomy was cultivated
as a segregated discipline, its findings were colorless and too often
Now that this isolationism has given way to genuine collaboration
among specialists in all related fields — physiology, biochemistry, biophysics,
clinical practice, neuropathology, psychology, among others
— we witness today a renaissance of the science of neurology. The
results of the exacting analytic investigations of the specialists can
now be synthesized and given meaning. The task of comparative
anatomy in this integrated program of research is fundamental and
essential. The experimentalist must know exactly what he has done
to the living fabric before he can interpret his experiment. In the past
it too often happened that a physiologist would stab into a living
frog, take his kymograph records, and then throw the carcass into
the waste-jar. This is no longer regarded as good physiology. Without
the guidance of accurate anatomical knowledge, sound physiology is
impossible; and, without skilful physiological experimentation, the
anatomical facts are just facts and nothing more.
Early in my program the amphibians were selected as the most
favorable animals with which to begin a survey of the comparative
anatomy of the nervous system. Time has proved the wisdom of this
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choice, and the study of these animals has been so fruitful that by
far the larger part of my research has been devoted to them.
In this work it was my good fortune to be associated with the late
G. E. Coghill, whose distinguished career pointed the way to an
original approach to the problems of the origins and growth of the
nervous organs and their functions. The record of phylogenetic history
spans millions of years and is much defaced by time; but the
record of the embryonic development of the individual is measured
in days and hours, and every detail of it can be watched from moment
to moment. The internal operations of the growing body are not
open to casual inspection, but Coghill showed us that the sequence
of these changes can be followed.
He selected the salamanders for his studies for very good reasons,
the same reasons that led me to take these animals as my own point
of departure in a program of comparative neurology. My intimate
association with Coghill lasted as long as he lived, and the profound
influence which his work has had upon the course of biological and
psychological events in our generation has motivated the preparation
of a book devoted to his career ('48). This influence, though
perhaps unrecognized at the time, was doubtless largely responsible
for my persistent efforts to analyze the texture of the amphibian
nervous system, for his studies of the growth of patterns of behavior
and their instrumentation in young stages of salamanders brought to
light some prmciples which evidently are applicable in phylogenetic
development also.
While Coghill's studies on the development of salamanders were in
process, we were impressed by the importance of learning just how
these processes of growth eventuate in the adult body. This was my
job, and so we worked hand in hand, decade after decade, for forty
years. Progress was slow, but our two programs fitted together so
helpfully that my original plan for a comprehensive study of the
comparative anatomy of the nervous system was abandoned in favor
of more intensive study of salamanders.
The preceding details of personal biography are relevant here because
they explain the motivation and plan of this book. The significant
facts now known about the internal structure of the brain of
the tiger salamander in late larval and adult stages are here assembled.
The observation's on this and allied species previously re[
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corded by the writer and many others are widely scattered, often in
fragmentary form, and with confusing diversity in nomenclature and
interpretation. As observations have accumulated, gaps in knowledge
have been filled, early errors have been corrected, the nomenclature
has been systematized, and now, with the addition of considerable
new observation here reported, the structure may be viewed as a
whole and interpreted in relation with the action system of the living
animal. Many of my observations during the last fifty years confirm
those of others; and, since references to these are given in the papers
cited, this account is not encumbered with them except where they
supplement my own experience or deal with questions still in controversy.
I here describe what I myself have seen, with exceptions
explicitly noted. This explains the disproportionate number of references
in the text to my own papers.
Two genera of urodeles have been studied intensively to find out
what is the instrumentation of their simple patterns of behavior. All
observations on the brain of the more generalized mudpuppy,
Necturus, were assembled in a monograph ('336) and several followmg
papers. The present work is a similar report upon the brain of the
somewhat more specialized tiger salamander. The original plan was
to follow this with an examination of the brain of the frog, for which
abundant material was assembled and preliminary surveys were
made; but this research, which is urgently needed, must be done by
In this book the anatomical descriptions are arranged in such a
way as to facilitate interpretation in terms of probable physiological
operation. Though the amount of experimental evidence about the
functions of the internal parts of the amphibian brain is scanty, there
is, fortunately, a wealth of such observation about the brains of other
animals; and where a particular structural pattern is known to be
colligated with a characteristic pattern of action, the structure may
be taken as an indicator of the function. The reliability of this method
depends upon the adequacy of our knowledge of both the function
and the structure. The present task, then, is an assembly of the
anatomical evidence upon which the interpretations are based.
The first part of this work is written to give biologists and psychologists
an outline of the plan of organization of a generalized
vertebrate brain and some insight into the physiological principles
exemplified in its action. These eight chapters, with the accompanying
illustrations, can be read independently of the rest of the book.
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Part II is written for specialists in comparative neurology. It
covers the same ground as the first part, reviewing each of the conventional
subdivisions of the brain, giving details of the evidence
upon which conclusions are based, with references to sources and
much new material. This involves some repetition, which is unavoidable
because all these structures are interconnected and in action
they co-operate in various ways. Many structures must be described
in several contexts and, accordingly, the Index has been prepared
with care so as to enable the reader to assemble all references to every
The most important new observations reported in Part II relate to
the structure and connections of the isthmus (chap, xiii), interpeduncular
nucleus (chap, xiv), and habenula, including analysis of
the stria medullaris thalami and fasciculus retroflexus (chap, xviii).
In chapter xx a few of the more important systems of fibers are described,
including further analysis of the tegmental fascicles as enumerated
in the paper of 1936 and references to other lists in the literature.
The composition of the commissures of the brain is summarized
in chapter xxi. The lemniscus systems are assembled in chapter xi,
and other tracts are described in connection with the structures with
which they are related.
Since most neurologists are not expert in the comparative field,
where the nomenclature is technical and frequently unintelligible
except to specialists, the attempt is made in Part I to present the
salient features with a minimum of confusing detail and, so far as
practicable, in terms of familiar mammalian structure. This is not an
easy thing to do, and no clear and simple picture can be drawn, for
the texture of even so lowly organized a brain is bafflingly complicated
and many of these structures have no counterparts in the human
body. Homologies implied by similar names are rarely exact,
and in many of these cases the amphibian structure is regarded as the
undifferentiated primordium from which the mammalian has been
derived. This is emphasized here because homologies are usually
defined in structural terms and because organs which are phylogenetically
related are regarded as more or less exactly homologous,
regardless of radical changes in their functions. Thus the "dorsal
island" in the acousticolateral area of the medulla oblongata of
Necturus is regarded as the primordium of the dorsal cochlear nucleus
of mammals, despite the fact that Necturus has no recognizable
rudiment of a cochlea or cochlear nerve. This is because, when the
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cochlear rudiment and its nerve appear in the frog, the tissue of the
"dorsal island" receives the cochlear nerve with radical change in the
functions performed (p. 138).
The histological texture of these brains is so different from that of
mammalian brains that the development of an intelligible nomenclature
presents almost insuperable difficulty — a difficulty exacerbated
by the fact that in the early stages of the inquiry it was necessary to
apply descriptive terms to visible structures before their relationships
were known. With increase of knowledge, errors were corrected,
and unsuitable names were discarded; but terms already in use are
still employed so far as possible, even though they are in some cases
cumbersome and now known to be inappropriate. In all these descriptions
I have consistently used the word "fissure" to designate visible
furrows on the external surface of the brain and "sulcus" for those on
ventricular surfaces. Attention is called to the list of abbreviations
(p. 391) and to previous lists there cited where synonyms are given.
In all my published figures of brains of urodeles the intent has been
to use the same abbreviations for comparable structures. This intention
has been approximately realized, but there are some inconsistencies,
in most of which the differences express a change in emphasis
rather than a correction of errors of observation.
Many well-defined tracts of fibers seen in fishes and higher animals
are here represented in mixed collections of fibers of diverse sorts,
here termed "fasciculi," or they may be dispersed within a mixed
neuropil. The practice here is to define as a "tract" all fibers of like
origin or termination, whether or not they are segregated in separate
bundles. The customary self-explanatory binomial terminology is
used wherever practicable — a compound word with origin and termination
separated by a hyphen. But, since a single fiber of a tract
may have collateral connections along its entire length, the fully
descriptive name may become unduly cumbersome ('41a, p. 491).
Thus, in accordance with strict application of the binomial terminology,
tractus strio-tegmentalis would become tractus striothalamicus
et peduncularis et tegmentalis dorsalis, isthmi et trigemini.
The chemists seem to be able to manipulate similar enormities
even without benefit of hyphens or spaces, but not many anatomists
are so hardy. Few of the named tracts are sharply delimited, and all
of them are mixtures of fibers with different connections. Any
analysis is necessarily somewhat arbitrary.
Simple action systems of total-pattern type, wherever found
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(cyclostomes, primitive ganoid fishes, urodeles), are correlated with
a histological texture of the brain which is characteristic and probably
primitive (chap. iii).
The external configuration of the urodele brain also is generalized,
much as in a human embryo of about 6 weeks. In the next chapter
special attention is directed to this comparison to assist the reader in
identifying familiar parts of the human brain as they are seen in the
simplified amphibian arrangement.
In our comparison of the amphibian brain with the human, two
features are given especial emphasis, both of which are correlated
with differences in the mode of life of the animals in question, that is,
with the contrast between the amphibian simplicity of behavior with
stereotyped total patterns of action predominating and the human
complexity of movement in unpredictable patterns. The correlated
structural differences are, first, in Amblystoma the more generalized
histological texture to which reference has just been made, and notably
the apparent paucity of provision for well-defined localization
of function in the brain; and, second, the preponderant influence of
motor patterns rather than sensory patterns in shaping the course of
differentiation from fishlike to quadrupedal methods of locomotion
and somatic behavior in general.
The material studied comprises gross dissections and serial sections
of about five hundred specimens of Amblystoma from early embryonic
to adult stages. About half these brains were prepared by the
Golgi method and the remainder by various other histological procedures.
Most of these are A. tigrinum, some are A. maculatum
(punctatum), and a few are A. jeffersonianum. In early developmental
stages some specific differences have been noted in the embryological
papers of 1937-41, but no systematic comparative study
has been made. The late larval and adult brains under consideration
in this book are of A. tigrinum. In former papers there are comments
on this material and the methods of preparation ('25, p. 436; '35a,
p. 240; '42, p. 193).
In the study of these sections the cytological methods of Nissl and
others are less revealing than in more highly differentiated brains
because of the unspecialized structure of the nervous elements. Some
modifications of the method of Weigert which decolorize the tissue
sufficiently to show the myelinated fibers and also the arrangement
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of cell bodies prove to be most useful for general orientation. Other
details can then be filled in by study of reduced silver preparations
and especially of Golgi sections. A favorable series of transverse
Weigert sections (no. IIC; see p. 3'21) has been chosen as a type or
standard of reference, and the median section as reconstructed from
this specimen (fig. 2C) has been used as the basis for many diagrams
of internal structure. For reference to published figures of this brain
and other details concerning it see page 321. Figures 2A and B are
similar diagrams of the median section of the specimen from which
figures 25-36 were drawn. The topography shown in these median
sections is the basis for the descriptive terms used throughout this text.
Except for scattered references to details, the only systematic
descriptions of the brain of Amblystoma are in my papers, Bindewald's
('14) on the forebrain, and Larsell's ('20, '32) on the cerebellum.
Mention should also be made of Roofe's account ('35) of the
endocranial blood vessels and Dempster's paper ('30) on the endolymphatic
Kingsbury's admirable paper on Necturus in 1895 may be taken as
a point of departure for all further investigation of the brains of
urodeles, including my monograph of 1933 and several preceding and
following papers. Some of the more important descriptions of the
brains of other urodeles are cited in the appended bibliography,
notably the following: Salamandra (Kuhlenbeck, '21; Kreht, '30),
Proteus (Kreht, '31; Benedetti, '33), Cryptobranchus (Benzon, '26),
Gymnophiona (Kuhlenbeck, '22), Siren (Rothig, '11, '24, '27), and
several other urodeles in Rothig's later papers, Hynobius, Spelerpes,
Diemyctylus (Triturus), Cryptobranchus, Necturus.
For the Anura the excellent description of the frog by E. Gaupp in
1899 laid a secure foundation for all subsequent work, and the time is
now ripe for a systematic restudy of this brain with the better methods
now available and the correlation of the histological structure
with physiological experiments specifically designed to reveal the
action of this structure. Aronson and Noble ('45) have published an
excellent contribution in this field.
No comprehensive description of the development of the brain of
Amblystoma has been published. The difficulties met in staging
specimens by criteria defined by Harrison, Coghill, and others I
have discussed elsewhere ('48, chap. x). Griggs ('10) described with
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excellent illustrations the early stages of the neural plate and neural
tube. Baker ('27) illustrated dorsal and ventral views of the open
neural plate, and Baker and Graves ('32) described six models of
the brain of A. jeffersonianum from 3 to 17 mm. in length. Burr
('22) described briefly the early development of the cerebral hemispheres.
Successive stages of the brain of A. punctatum have been illustrated
by Coghill and others (some of which I have cited, '37, p. 391,
and '38, p. 208), and at the Wistar Institute there are other models
of the brains of physiologically tested specimens. Coghill's papers
include a wealth of observation on the development of the mechanisms
of the action system, and these were summarized in his London
lectures, published in 1929. His reports were supplemented by a series
of papers which I published from 1937 to 1941, but these fragmentary
observations (of the younger stages particularly) were based on inadequate
material and are useful only as preliminary orientation for
a more systematic investigation. In Coghill's papers there are accurate
projections of all mitotic figures and neuroblasts of the central
nervous system in nonmotile, early flexure, coil, and early swimming
stages and the arrangement of developing nerve fibers of the brain in
the last-mentioned stage (Coghill, '30, Paper IX, fig. 4). On the basis
of these data he divided the embryonic brain in front of the isthmus
into sixteen regions, each of which is a center of active and characteristic
differentiation. These regions are readily identified in our
reduced silver preparations of these and later stages. Using a modification
of this analysis, I have distinguished and numbered twentytwo
such regions in the cerebrum and cerebellum ('37, p. 392), and
the development of each of these can be followed through to the
adult stage. In my papers of 1937-39 some salient features of these
changes are recorded; but this account is incomplete, and more
thorough study is urgently needed. In the present work some details
only of this development are given in various contexts as listed in the
Index under "Embryology."
The most detailed description of the development of the urodele
brain is the paper by Sumi ('26) on Hynobius. Soderberg ('22) gave a
brief description of the development of the forebrain of Triturus
(Triton) and a more detailed account of that of the frog, and Rudebeck
('45) has added important observations.
The successive changes in the superficial form of the brain can be
interpreted only in the light of the internal processes of growth and
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differentiation. The need for a comprehensive study of the development
of the histological structure of the brain of Amblystoma, including
the differentiation of the nervous elements and their fibrous
connections, is especially urgent in view of the very large number of
experimental studies on developmental mechanics which have been
in progress for many years and will probably continue for years to
come. Amblystoma has proved to be an especially favorable subject
for these studies, and in many of them a satisfactory interpretation
of the findings cannot be achieved without more complete knowledge
than we now possess of the development of both the nervous tissues
and other bodily organs.
The nervous systems of all vertebrates have a common structural
plan, which is seen most clearly in early embryonic stages and in the
adults of some primitive species. But when the vertebrate phylum is
viewed as a whole, the nervous apparatus shows a wider range of
adaptive structural modifications of this common plan than is exhibited
by any other system of organs of the body. In order to understand
the significance of this remarkable plasticity and the processes
by which these diverse patterns of nervous organization have been
elaborated during the evolutionary history of the vertebrates, it is
necessary to find out what were the outstanding features of the
nervous system of the primitive ancestral form from which all higher
species have been derived.
Since the immediate ancestors of the vertebrate phylum have been
extinct for millions of years and have left no fossil remains, our only
recourse in this search is to examine the most generalized living
species, compare them one with another and with embryonic stages,
and so discover their common characteristics. This has been done,
and we are now able to determine with a high degree of probability
the primitive pattern of the vertebrate nervous system.
The most generalized living vertebrates (lampreys and hagfish)
have brains which most closely resemble that of the hypothetical
primordial vertebrate ancestor. The brains of the various groups of
fishes show an amazing variety of deviations from the generalized
pattern. The paleontological record shows that the first amphibians
were derived from one of the less specialized groups of fishes; and
there is evidence that the existing salamanders and their allies have
preserved until now a type of brain structure which closely resembles
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that of the most primitive amphibians and of the generahzed fishes
ancestral to them.
The internal texture of the brains of the generalized amphibians
which are described in this work closely resembles that of the most
primitive extant fishes; but the brain as a whole is organized on a
higher plane, so that it can more readily be compared with those of
reptiles, lower mammals, and man. For this reason the salamanders
occupy a strategic position in the phylogenetic series. This examination
has brought to light incipient stages of many complicated human
structures and some guiding principles of both morphogenesis
and physiological action that are instructive.
When the first amphibians emerged from the water, they had all
the land to themselves ; there were no living enemies there except one
another. During aeons of this internecine warfare they carried protective
armor; but in later times, during the Age of Reptiles, these
more efficient fighters exterminated the clumsy armored amphibians.
The more active frogs and toads survived, and so also did the sluggish
salamanders and their allies, but only by retiring to concealment
in sheltered places.
In Devonian times, probably about three hundred million years
ago, various species of fishes made excursions to the land and acquired
structures adapted for temporary sojourn out of water. Some
of the primitive crossopterygian fishes went further and, after a fishlike
larval period, experienced a metamorphosis into air-breathing
tetrapods. They became amphibians. These were fresh-water species,
and the immediate cause of this evolutionary change was extensive
continental desiccation during the Devonian period. While their
streams and pools were drying up, those fishes which had accessory
organs of respiration in addition to the gills of typical fishes, were
able to survive and, through further transformations, become airbreathing
land animals. An excellent summary of the paleontological
evidence upon which the history of the evolution of fishes has been
reconstructed has been published by Romer ('46).
Two prominent features of this revolutionary change involved the
organs of respiration and locomotion, with corresponding changes in
the nervous apparatus of control. These systems of organs are typical
representatives of the two major subdivisions of all vertebrate bodies
and their functions — the visceral and the somatic. The visceral functions
and the visceral nervous system will receive scant consideration
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in this work, for the material at our disposal is not favorable for the
study of these tissues. Here we are concerned primarily with the
nervous apparatus of overt behavior, that is, of the somatic adjustments.
The most important change in these somatic adjustments during
the critical evolutionary period under consideration is the transition
from swimming to walking. The fossil record of the transformation of
fins into legs is incomplete, but it is adequate to show the salient
features of the transformation of crossopterygian fins into amphibian
legs (Romer, '46). In the individual development of every
salamander and every frog the internal changes in the organization
of the nervous system during the transition from swimming to walking
can be clearly seen. And these changes are very significant in our
present inquiry because they illustrate some general principles of
morphogenesis of the brain more clearly than do any other available
In fishes, swimming is a mass movement requiring the co-ordinated
action of most of their muscles in unison, notably the musculature of
the trunk and tail. The paired fins are rudders, not organs of propulsion.
The young salamander larva has no paired limbs but swims
vigorously. This is a typical total pattern of action as defined by
Coghill. The adult salamander after metamorphosis may swim in the
water like the larva; and he can also walk on land with radically different
equipment. Some fishes can crawl out on land, but the modified
fins are clumsy and ineflBcient makeshifts compared with the
amphibian's mobile legs.
Quadrupedal locomotion is a very complicated activity compared
with the simple mass movement of swimming. The action of the four
appendages and of every segment of each of them must be harmoniously
co-ordinated, with accurate timing of the contraction of many
small muscles. These local activities are "partial patterns" of behavior,
in Coghill's sense. From the physiological standpoint there is
great advance, in that the primitive total pattern is supplemented,
and in higher animals largely replaced, by a complicated system of
co-ordinated partial patterns. This is emphasized here because it provides
the key to an understanding of many of the differences between
the nervous systems of fishes, salamanders, and mammals. Motility,
and particularly locomotion, have played a major role in vertebrate
evolution, as dramatically told by Gregory ('43). This outline has
been filled in by Howell's ('45) interesting comparative survey of the
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mechanisms of locomotion, and I have elsewhere discussed ('48) Coghill's
contributions to this theme.
In the history of vertebrate evolution there were four critical periods:
(1) the emergence of the vertebrate pattern of the nervous
system from invertebrate ancestry; (2) the transition from aquatic
to terrestrial life; (3) the differentiation within the cerebral hemispheres
of primitive cerebral cortex; (4) the culmination of cortical
development in mankind, with elaboration of the apparatus requisite
for language and other symbolic (semantic) instrumentation of the
mental life.
1 . The extinct ancestors of the vertebrates in early Silurian times
were probably soft and squashy creatures, not preserved as fossils.
Some of their aberrant descendants may be recognized among the
Enteropneusta, Tunicata, and Amphioxi ; but the first craniate vertebrates
preserved as fossils were highly specialized, heavily armored
ostracoderms, now all extinct.
2. The salient features of the second critical period have been mentioned,
and here the surviving amphibians recapitulate in ontogeny
many instructive features of the ancestral history.
3. Amphibians have no cerebral cortex, that is, superficial laminated
gray matter, in the cerebral hemispheres. This first takes
definitive form in the reptiles, though prodromal stages of this differentiation
can be seen in fishes and amphibians, a theme to which
we shall return in chapter vii.
4. The fourth critical period, like the first, does not lie within the
scope of this work, though study of the second and third periods
brings to light some principles of morphogenesis which may help us
to understand the more recondite problems involved in human cortical
It is probable that none of the existing Amphibia are primitive in
the sense of survival of the original transitional forms and that the
urodeles are not only aberrant but in some cases retrograde (Noble,
'31; Evans, '44); yet the organization of their nervous systems is
generalized along very primitive lines, and these brains seem to me
to be more instructive as types ancestral to mammals than any others
that might be chosen. They lack the highly divergent specializations
seen in most of the fishes; and, in both external form and internal
architecture, comparison with the mammalian pattern can be made
with more ease and security. So far as structural differentiation has
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advanced, it is in directions that point clearly toward the mammalian
Amphibian eggs and larvae are readily accessible to observation
and experiment; they are easily reared; they tolerate experimental
operations unusually well; and, in addition, the amphibian neuromuscular
system begins to respond to stimulation at a very early age,
so that successive stages in maturation of the mechanism are documented
by changes in visible overt movement. The adult structure is
instructive; and, when the embryological development of this structure
is compared with that of higher brains and with the sequence of
maturation of patterns of behavior, basic principles of nervous organization
are revealed that can be secured in no other way. In the
absence of differentiated cerebral cortex, the intrinsic structure of the
stem is revealed. Experimental decortication of mammals yields
valuable information, but study of such mutilations cannot tell us all
that we need to know about the normal operations of the brain stem
and the reciprocal relationships between the stem and the cortex.
In brief, the brains of urodele amphibians have advanced to a
grade of organization typical for all gnathostome vertebrates, Amblystoma
being intermediate between the lowest and the highest species
of Amphibia. This brain may be used as a pattern or template, that
is, as a standard of reference in the study of all other vertebrate
brains, both lower and higher in the scale.
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REFERENCE to figures 1-5, 85, and 86 shows that the larger
; subdivisions of the human brain are readily identified in Amblystoma,
though with remarkable differences in shape and relative
size. When this comparison is carried to further detail, the sculpturing
of the ventricular walls shown in the median section is especially
instructive. It is again emphasized that the application of mammalian
names to the structures here revealed rarely implies exact
homology; these areas are to be regarded as primordia from which
the designated mammalian structures have been differentiated. The
relationships here implied have been established by several independent
lines of evidence: (1) The relative positions and fibrous connections
of cellular masses and the terminal connections of tracts.
In so far as these arrangements conform with the mammalian pattern,
they may be regarded as homologous. (2) Embryological evidence.
The early neural tubes of amphibians and mammals are similar,
and subsequent development of both has been recorded. On the
basis of Coghill's observations of rates of proliferation and differentiation
in prefunctional stages, the writer ('37) gave arbitrary numbers
to recognizable sectors of the neural tube in early functional
stages, and the subsequent development of each of these is, in broad
lines, similar to that of corresponding mammalian parts. (3) The
relationships of svipposed primordia of mammalian structures may be
tested by the comparative method. In an arrangement of animal
types which approximates the phylogenetic sequence from the most
generalized amphibians to man, there are many instances of progressive
differentiation of amphibian primordia by successive increments
up to the definitive human form.
Many pictures of the brains of adult and larval Amblystoma and
other urodeles have been published, some of which I have cited
('35a, p. 239). The most accurate pictures of the brain of adult A.
tigrinum are those of Roofe ('35), showing dorsal, ventral, and lateral
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aspects and the distribution of endocranial arteries and veins. The
outHnes of the brain were drawn from specimens dissected after
preservation for 6 weeks in 10 per cent formahn. One of these is
shown here (fig. 86 A). Figure IB is drawn from a dissection made by
the late Dr. P. S. McKibben, showing the sculpturing of the ventricular
surfaces. Figures lA and 85 are drawn from a wax model in
which there is some distortion of the natural proportions. Not all the
differences seen in these pictures and in the proportions of sections
figured are artifact, for the natural variability of urodele brains is
surprisingly large (Neimanis, '31). Brains of larval stages have been
illustrated by many authors and in my embryological papers of
The somewhat simpler brain of the mudpuppy, Necturus, has
been described in a series of papers as completely as available material
permits, and comparison with the more differentiated structure
of Ambly stoma is instructive. The sketches shown in figures 86B and
C illustrate the differences between the form of this forebrain and
that of Amblystoma. The monograph of 1933 contains a series of
diagrams ('33&, figs. 6-16) of the internal connections of the brain of
Necturus similar to those of Amblystoma shown here (figs. 7-24).
In 1910 I described the general features of the forebrain of A.
tigrinum, with a series of drawings of transverse Weigert sections,
no. lie, which has subsequently been used as the type specimen.
Though this paper contains some errors and some morphological
interpretations which I now regard as outmoded ('33a), most of the
factual description has stood the test of time, and additional details
and reports on other parts of the brain have been published in a
series of papers.
The most conspicuous external fissures of the brain of Amblystoma
are: (1) the longitudinal fissure separating the cerebral hemispheres;
(2) the deep stem-hemisphere fissure; (3) a wide dorsal groove separating
the epithalamus from the roof (tectum) of the midbrain; (4)
the ventral cerebral flexure or plica encephali ventralis, which is a
sharp bend of the floor of the midbrain, where it turns downward and
backward into the "free part" of the hypothalamus; and (5) the
fissura isthmi, extending downward and forward from the anterior
medullary velum between midbrain and isthmus. The middle part of
the fissura isthmi is at the anterior border of the auricle, which is more
prominent in the larva than in the adult ('14a, figs. 1-3). Here in the
adult it lies near the posterior border of the internal isthmic tissue,
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some distance posteriorly of the ventricular sulcus isthmi; but, like
the latter, it really marks the anterior border of the isthmus, as will
appear in the description of the development of the isthmic sulcus
(p. 179).
The obvious superficial eminences on the dorsal aspect of the brain
are the small cerebellum, the dorsal convexity of the roof of the
midbrain (tectum mesencephali) , the habenular nuclei of the epithalamus,
and the two cerebral hemispheres. Posteriorly of the
habenulae in the early larvae is the membranous pineal evagination,
which in the adult is a closed epithelial vesicle detached from the
brain except for the few fibers of the parietal nerve. The lateral aspect
of the thalamus, midbrain, and isthmus is a nearly smooth convexity,
posteriorly of which is the high auricle, composed of tissue which is
transitional between the body of the cerebellum and the acousticolateral
area of the medulla oblongata. This auricle contains the primordia
of the vestibular part of the cerebellar cortex (flocculonodular
lobe of Larsell), and most of its tissue is incorporated within the
cerebellum in mammals. On the ventral aspect there is a low eminence
in front of the optic chiasma, which marks the position of the
very large preoptic nucleus, and a similar eminence behind the
chiasma formed by the ventral part of the hypothalamus. The latter
is in the position of the human tuber cinereum but is not exactly
comparable with it. Most of the hypothalamus is thrust backward
under the ventral cerebral flexure as the pars libera hypothalami.
The large pars glandularis of the hypophysis envelops the posterior
end of the infundibulum and extends spinal ward from it, not anteriorly
as in man.
The primary subdivisions of the human brain as defined from the
embryological studies of Wilhelm His are readily identified in adult
Amblystoma, as shown in the median section (fig. 2A).
At the anterior end of each cerebral hemisphere is the very large
olfactory bulb, the internal structure of which shows some interesting
primitive features (p. 54; '246). The bulbar formation extends backward
on the lateral side for about half the length of the hemisphere,
but on the medial side only as far as the anterior end of the lateral
ventricle (figs. 3, 4). Bordering the bulb is an undifferentiated anterior
olfactory nucleus, and posteriorly of this the walls of the lateral
ventricle show early stages of the differentiation of the major subdivisions
of the mammalian hemisphere — in the ventrolateral wall a
strio-amygdaloid complex, ventromedially the septum, and dorsally
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the pars pallialis. In the pallial part no laminated cortical gray is
differentiated, but there are well-defined pallial fields: dorsomedially,
the primordial hippocampus; dorsolaterally, the primordial piriform
lobe; and between these a primordium pallii dorsalis of uncertain
The boundaries of the diencephalon, as here defined and shown in
figure 2A, are: anteriorly, the stem-hemisphere fissure and the posterior
border of the anterior commissure ridge and, posteriorly, the
anterior face of the posterior commissure and the underlying commissural
eminence and, more ventrally, the sulcus, s, which marks
the anterior border of the cerebral peduncle. The inclusion of the
preoptic nucleus is in controversy; but, whether or not this inclusion
is justifiable morphologically, its relationships with the hypothalamus
are so intimate that it is practically convenient to consider these
parts together. The four primary subdivisions of the diencephalon as
I defined them in 1910 are: (1) the dorsal epithalamus, containing on
each side the habenula and pars intercalaris, the latter including the
pretectal nucleus; (2) pars dorsalis thalami, which is the primordium
of the sensory nuclei of the mammalian thalamus; (3) pars ventralis
thalami, the motor zone of the thalamus, or subthalamus; (4) hypothalamus.
The mammalian homologies of these areas are clear,
though their relative sizes and fibrous connections exhibit remarkable
The posterior boundary of the mesencephalon is marked by the
external fissura isthmi, the ventricular sulcus isthmi (fig. 2B,,
and ventrally in the floor plate a pit, the fovea isthmi [f.i.). These
are all more prominent in the larva than in the adult. This sector
includes the posterior commissure, the tectum mesencephali (primordial
corpora quadrigemina) , the underlying dorsal tegmentum
(subtectal area), and the area surrounding the tuberculum posterius
at the ventral cerebral flexure, termed the "nucleus of the tuberculum
posterius." On embryological grounds and for convenience of description,
this ventral area, which is bounded by the variable ventricular
sulcus s, is here called the "peduncle" in a restricted sense ('36, p.
298; '396, p. 582). This is a primordial mesencephalic structure which
is not the equivalent of the peduncle of human neurology. Amblystoma
has nothing comparable with the human basis pedunculi, and
its "peduncle" is incorporated within the tegmentum of the human
brain. The III cranial nerve arises within the "peduncle" and
emerges near the fovea isthmi. The nucleus of the IV nerve is in the
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isthmus. In the human brain there are no definite structures comparable
to the amphibian dorsal and isthmic tegmentum.
The isthmus is much more clearly defined than in adult higher
brains, it is relatively larger, and its physiological importance is correspondingly
greater, as will appear later. It is bounded anteriorly
by the sharp isthmic sulcus and posteriorly by the cerebellum,
auricle, and trigeminal tegmentum. The so-called "pons" sector of
the human brain stem is named from its most conspicuous component,
but this name is meaningless in comparative anatomy. In man
it is the pons and the sector of the stem embraced by it; but in no
two species of mammals is the part embraced by the pons equivalent;
and below the mammals the pons disappears entirely. The medulla
oblongata, on the other hand, is a stable structure, extending from
the isthmus to the spinal cord, and for it the shorter name "bulb" is
sometimes used, especially in compounds.
I outlined the development and morphological significance of the
urodele cerebellum ('14, '24), and this was followed by detailed descriptions
of the development and adult structure of this region of
Amblystoma by Larsell ('20, '32), whose observations I have subsequently
confirmed, including his fundamental distinction between
its general and its vestibular components.
Some features of the larval medulla oblongata and related nerves
have been described ('14a, '396) and, more recently ('446), additional
details of the adult, particularly the structures at the bulbospinal
junction. Much remains to be done to clarify the organization
of the medulla oblongata and spinal cord.
The cranial nerves and their analysis into functional components
(chap, v) were described by Coghill ('02). The embryological development
of these components also has been extensively studied (chap.
x). The arrangement and composition of these nerves are fundamentally
similar to those of man, with a few notable exceptions. The
internal ear lacks the cochlea, which is represented by a very primitive
rudiment; a cochlear nerve, accordingly, is not separately differentiated.
There is an elaborate system of cutaneous organs of the
lateral lines, whose functions are not as yet adequately known. These
are supplied by very large nerves commonly assigned to the VII and
X pairs, though it would be more appropriate to regard them as
accessory VIII nerves, for all these nerve roots enter a wide zone at
the dorsolateral margin of the medulla oblongata known as the "area
acusticolateralis." There is no separate XI cranial nerve, this being
[Begin Page: Page 23]
represented by an accessorius branch of the vagus. The XII nerve is
represented by branches of the first and second spinal nerves. The
first spinal nerve in some specimens has a small ganglion ; the second
nerve always has a large dorsal root and ganglion. In this connection
a passage in the comprehensive work on the anatomy of Salamandra
by Francis ('34, p. 134) is worthy of mention: "After making due
allowance for the absence of a lateralis component in the adult
salamander, the correspondence between the cranial nerves of this
animal and those of Ambly stoma is very close indeed."
The configuration and mutual relations of the gross structures just
surveyed can be seen only in sections, of which many, cut in various
planes, have been illustrated in the literature. Only a few selected
examples are included in the present work, with references in subsequent
chapters to many others. For general orientation the following
figures may be consulted : a series of selected transverse sections from
the spinal cord to the olfactory bulb (figs. 87-100); a series of horizontal
sections through the middle part of the brain stem (figs.
25-36); a few sagittal sections (figs. 101-4). Figures 6-24 show the
chief fibrous connections of each well-defined region of the brain
The diencephalon, mesencephalon, and isthmus have the form of
three irregular pyramids oppositely oriented (fig. 2A). The broad
base of the diencephalon extends from the anterior commissure to the
hypophysis, and the apex is at the epiphysis. The tectum forms the
base of the mesencephalic pyramid, and the apex is at the ventral tip
of the tuberculum posterius, which borders the ventral cerebral
flexure. The base of the pyramidal isthmus is formed by the massive
tegmentum isthmi of each side and the median interpeduncular
nucleus in the floor plate. It narrows dorsally into the anterior medullary
velum between the tectum and the cerebellum.
The middle sectors of the brain stem — diencephalon, mesencephalon,
and isthmus — contain the primordial regulatory and integrating
apparatus controlling the fundamental sensori-motor systems
of adjustment. The most important peripheral connections are
with the eyes, and these in most vertebrates play the dominant role
in maintaining successful adjustment with environment. From this
topographical feature it naturally followed that, during the course of
phylogenetic differentiation of the brain, the chief centers of adjustment
of the other exteroceptive systems were elaborated in close
juxtaposition with the visual field in the midbrain and thalamus.
[Begin Page: Page 24]
Here they are interpolated between the primary sensory and motor
apparatus of the medulla oblongata and spinal cord below and the
great olfactory field and suprasegmental apparatus of the cerebral
hemispheres above.
In all lower vertebrates the roof of the midbrain, the tectum, is the
supreme center of regulation of motor responses to the exteroceptive
systems of sense organs. The hypothalamus is similarly elaborated for
regulation of olfacto- visceral adjustments. The patterning of motor
responses for both these groups of receptors is effected in the cerebral
peduncle and tegmentum. In the region of the isthmus, between the
tectum and the primary vestibular area of the medulla oblongata and
above the tegmentum, the cerebellum was elaborated as the supreme
adjustor of all proprioceptive systems.
At the rostral end of the brain, within and above the specific
olfactory area of the cerebral hemisphere, there gradually emerged a
synthetic apparatus of control, adapted to integrate the activities of
all the other parts of the nervous system and to enlarge capacity to
modify performance as a result of individual experience. In the lowest
vertebrates this "suprasensory" and "supra-associational" apparatus,
as Coghill termed it, is not concentrated in the cerebral
hemispheres, but it is dispersed, chiefly in the form of diflfuse neuropil.
In the amphibian cerebral hemispheres this integrating apparatus is
more highly elaborated than elsewhere, with some local differentiation
of structure. The hemispheres are larger than in fishes, and the
primordia of their chief mammalian subdivisions can be recognized.
A dorsal pallial part is distinguishable from a basal or stem part of
the hemisphere, though the distinctive characteristics of the pallium
are only incipient. There is no cerebral cortex, and, accordingly, the
mammalian cortical dependencies in the thalamus, midbrain, and
cerebellum have not yet appeared. The primordial thalamus is concerned
chiefly with adjustments within the brain stem, though
precursors of the thalamic radiations to the hemispheres are present.
The lateral ventricles of the cerebral hemispheres have the typical
form except at the interventricular foramen, where the amphibian
arrangement is peculiar. The anterior and hippocampal commissures
do not cross as usual in or above the lamina terminalis, but in a more
posterior high commissural ridge ; and between these structures there
is a wide precommissural recess, into which the interventricular
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foramina open. This results in some radical differences from reptilian
and mammalian arrangements of the related fiber tracts and membranous
parts, as elsewhere described (p. 291; '35). The third ventricle
is expanded dorsally into the complicated membranous paraphysis
and dorsal sac. Ventrally, the great elongation of the preoptic
nucleus gives rise to a large preoptic recess between the anterior commissure
ridge and the chiasma ridge, and in front of the latter there is
a lateral optic recess (fig. 96), which in early larval stages extends
outward as far as the eyeball, as a patent lumen of the optic nerve
('41), an arrangement which persists in the intracranial part of the
nerve of adult Necturus ('41a). In the hypothalamus the ventricle is
dilated laterally ('35a, p. 253; '36, figs. 10-14), and posteriorly it is a
wide infundibulum with membranous roof and thin but nervous floor
and posterior wall. The latter is the pars nervosa of the hypophysis
and is partly enveloped by the pars glandularis (figs. 2, 101; '35a, p.
254; '42, p. 212 and figs. 56-65; Roofe, '37). The aqueduct of the
midbrain is greatly expanded dorsoventrally. Its ventral part is contracted
laterally by the thick peduncles and tegmentum, and the
dorsal part is dilated as an optocoele. The sulcus lateralis mesencephali
marks its widest extent, and tectal structure reaches far below this
sulcus. The fourth ventricle is of typical form except anteriorly,
where the wide lateral recess with membranous roof extends outward
and forward to cover the whole dorsolateral aspect of the auricular
lobe (figs. 90, 91 ; '24, p. 627). The rhombencephalic chorioid plexus is
elaborately developed in interesting relation with the peculiar endolymphatic
organs of this animal ('35, p. 310). The ventricular systems
of adult Triturus (Diemyctylus) and of larval and adult stages
of Hynobius have been described and illustrated with wax models
bySumi('26, '26a).
The ventricular surface of both larvae and adults is clothed with
very long cilia. These are not preserved in ordinary preparations and
in our material are seen only in Golgi sections, where their impregnation
is erratic and local ('42, p. 196). They are most frequently seen
in the infundibulum and optocoele under the tectum. In the vicinity
of the posterior commissure the ciliated ependyma is thickened (subcommissural
organ of Dendy), and to it the fiber of Reissner is attached
('42, p. 197). This thick, nonnervous fiber extends backward
through the ventricle to the lower end of the spinal cord and, like the
cilia, is apparently an outgrowth from the internal ependymal membrane.
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The meninges of Amblystoma were described in 1935. This account
shoukl be compared with that of Salamandra pubhshed in 1934 by
Francis, whose description was based on the investigation of Miss
Helen O'NeiU ('98), done under the direction of Wiedersheim and
Gaupp. In Amblystoma the meninges are intermediate between the
meninx primitiva of the lower fishes and those of the frog. Over the
spinal cord and most parts of the brain a firm and well-defined
pachymeninx, or dura, closely invests the underlying undifferentiated
pia-arachnoid. The meninges of the frog have been described by
others, and recently Palay ('44) has investigated their histological
structure in the toad. The most interesting feature of these amphibian
membranes is their intimate relation with the enormous
endolymphatic organ described by Dempster ('30) and the associated
blood vessels.
The vascular supply of these brains is peculiar in several respects.
The distribution of arteries and veins has been described by Roofe
('35, '38), and I have added some details from the adult ('35) and the
larva {'Md). The endocranial veins form a double portal system of
sinusoids of vast extent and unknown significance. Between the
cerebral hemispheres and the epithalamus the nodus vasculosus
(Gaupp) is permeated by a complicated rete of sinusoids, which receives
venous blood from the entire prosencephalon— chorioid
plexuses, brain wall, and meninges. The efferent discharge from this
rete is by the two oblique sinuses, which pass backward across the
midbrain to enter a similar rete of wide, anastomosing smusoids
spread over the chorioid plexus of the fourth ventricle and the
lobules of the endolymphatic organs. This rete also receives the vems
from all posterior parts of the brain, meninges, and chorioid plexus.
The common discharge for all this endocranial venous blood is by a
large sinus, which emerges from the cranium through the jugular
foramen and joins the jugular vein. These membranous structures
are readily observable in the living animal without serious disturbance
of normal conditions, and they provide unique opportunities or
experimental study of some fundamental problems of vascular
^\\' wSomted out by Craigie ('38, '38a, '39, '45) that within the
substance of this brain the penetrating blood vessels are arranged in
two ways-a capillary net of usual type and simple loops, which
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enter from the meningeal arterial network. Our preparations confirm
this observation and also the fact that the vascular pattern varies in
different parts of the brain. Both isolated loops and the capillary net
may be seen in the same field, as in the dorsal thalamus (fig. 44), or
one of these patterns may prevail, with few, if any, instances of the
other. In the tectum and dorsal tegmentum of the midbrain, for instance,
the tissue is vascularized by simple loops with only occasional
anastomosis (fig. 48), while in the underlying peduncle and isthmic
tegmentum the vascular network prevails, with occasional simple
loops. In the meninges and chorioid plexuses only the network has
been observed.
The telencephalic and diencephalic chorioid plexuses have an
abundant arterial blood supply through the medial hemispheral
artery; but the elaborately ramified tubules of the paraphysis seem
to have no arterial supply or capillary net, the accompanying vessels
being exclusively venous sinusoids ('35, p. 342). The same seems to
be true of the endolymphatic sacs ('34c?, p. 543). The chorioid plexus
of the fourth ventricle has abundant arterial blood supply. In all
plexuses the capillaries unite into venules, which discharge into wide
sinusoids, which ramify throughout the plexus and have very thin
walls. All arterioles of the chorioid plexuses are richly innervated,
but it has not been possible to get satisfactory evidence of the sources
of these nerve fibers ('36, p. 343; '42, p. 255; Necturus, '336, p. 15).
The enormous development of the chorioid plexuses and associated
endolymphatic organ of urodeles is apparently correlated with the
sluggish mode of life and relatively poor provision for aeration of the
blood. In the more active anurans the plexuses are smaller; but in the
sluggish mudfishes, including the lungfishes, with habits similar to
those of urodeles, we again find exaggerated development of these
plexuses. Existing species in the border zone between aquatic and
aerial respiration are all slow-moving and relatively inactive. The
enlarged plexuses and sinusoids give vastly increased surfaces for
passage of blood gases into the cerebrospinal fluid; and, correlated
with this, the brain wall is thin everywhere, to facilitate transfer of
metabolites between brain tissue and cerebrospinal fluid. Massive
thickenings of the brain wall occur in many fishes and in amniote
vertebrates, but not in mudfishes and urodeles.
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IN AMPHIBIAN brains the histological texture is generalized,
exhibiting some embryonic features; and it is at so primitive a
level of organization as to make comparison with mammals difficult.
Most of the nerve cells are small, with scanty and relatively undifferentiated
cytoplasm. There are some notable exceptions, such as
the two giant Mauthner's cells of the medulla oblongata and related
elements of the nucleus motorius tegmenti. With the exceptions just
noted, Nissl bodies are absent or small and dispersed.
Almost all bodies of the neurons are crowded close to the ventricle
in a dense central gray layer, with thick dendrites directed outward
to arborize in the overlying white substance (figs. 9, 99). The axon
usually arises from the base of the dendritic arborization, rarely from
its tip, and sometimes from the cell body; it may be short and much
branched or very long, with or without collateral branches. The
ramifications of the short axons and of collaterals and terminals of
the longer fibers interweave with dendritic arborizations to form a
more or less dense neuropil, which permeates the entire substance of
the brain and is a synaptic field. Some of the nerve fibers are
myelinated, more in the peripheral nerves, spinal cord, and medulla
oblongata than in higher levels of the brain. Both myelinated and
unmyelinated fibers may be assembled in definite tracts, or they may
be so dispersed in the neuropil as to make analysis difficult. The arrangement
of recognizable tracts conforms with that of higher brains,
so that homologies with human tracts are in most cases clear. These
tracts and the gray areas with which they are connected provide the
most useful landmarks in the analysis of this enigmatic tissue.
In the gray substance there are few sharply defined nuclei like
those of mammals, but the precursors of many of these can be recognized
as local specializations of the elements or by the connections of
the related nerve fibers. In most cases the cells of these primordial
nuclei have long dendrites, which arborize widely into surrounding
fields (figs. 9, 24, 61, 66), so that the functional specificity of the
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nucleus is, at best, incomplete. This arrangement facilitates mass
movements of "total-pattern" type, but local differentiations serving
"partial patterns" of action (Coghill) are incipient. Localized reflex
arcs are recognizable, though in most cases these are pathways of
preferential discharge within a more dispersed system of conductors
(chap. vi).
Tissue differentiation is more advanced in the white substance
than in the gray. The most important and diversely specialized
synaptic fields are in the alba, and this local specialization is correlated
with differences in the physiological properties of the nervous
elements represented. This means, as I see it, that functional factors
must be taken into account in both ontogenetic and phylogenetic
differentiation and that in the long view the problems of morphogenesis
are essentially physiological, that is, they resolve into questions of
adaptation of organism to environment (chap. viii). This is the reason
why in this work the histological analysis is made in terms of physiological
criteria, even though these criteria are, in the main, based on
indirect evidence, namely, the linkage of structures in functional
systems of conductors.
The nonnervous components of this tissue comprise the blood vessels,
ependyma, and a small number of cells of uncertain relationships
which are regarded as undifferentiated free glial cells or transitional
elements ('34, p. 94; '336, p. 17). The ependymal elements everywhere
span the entire thickness of the brain wall with much free
arborization. They assume various forms in different regions, and
their arrangement suggests that they are not merely passive supporting
structures, though if they have other specific functions these are
still to be discovered. For illustrations see figures 63, 64, 70, 79, and
More detailed descriptions of the histological structure of urodele
brains may be found in earlier papers ('14a, p. 381; '17, pp. 232,
279 ff.; '335, pp. 16, 268; '33c; '33cf; '34; '34a,- '346; '42, p. 195; '44a).
In the olfactory bulbs of Necturus ('31) and Amblystoma ('246) we
find an interesting series of transitional cells between apparently
primitive nonpolarized elements and typical neurons, as described
on page 54.
In the generalized brains here under consideration the neuropil is
so abundant and so widely spread that it evidently plays a major
role in all central adjustments, thus meriting detailed description.
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Only the coarser features of this tissue are open to inspection with
presently available histological technique. In my experience its texture
is best revealed by Golgi preparations, and very many of them,
for the erratic incidence of these impregnations may select in different
specimens now one, now another, of the component tissues —
blood vessels, ependyma, dendrites, or axons. In each area of neuropil
these components are independent variables, and in most of these
areas axons from many sources are so intricately interwoven that the
tissue can be resolved only where fortunate elective impregnations
pick out one or another of the several systems of fibers in different
specimens. It is difficult to picture the neuropil either photographically
or with the pen, and the crude drawings in this book and in the
literature give inadequate representations of the intricacy and delicacy
of its texture.
A survey of the neuropil of adult Amblystoma as a whole has led
me to subdivide it for descriptive purposes and somewhat arbitrarily
into four layers ('42, p. 202). From within outward, these are as
1. The periventricular neuropil pervades the central gray so that
every cell body is enmeshed within a fabric of interwoven slender
axons (figs. 106, 107). This persists in some parts of the mammalian
brain as subependymal and periventricular systems of fibers.
2. The deep neuropil of the alba at the boundary between gray and
white substance knits the periventricular and intermediate neuropil
together, and it also contains many long fibers coursing parallel with
the surface of the gray. The latter are chiefly efferent fibers directed
toward lower motor fields (fig. 93, layer 5; '42, figs. 18-21, 24, 29-45,
3. The intermediate neuropil in the middle depth of the alba contains
the largest and most complicated fields of this tissue. It is very
unevenly developed, in some places scarcely recognizable and in
others of wide extent and thickness. Its characteristics are especially
well seen in the corpus striatum (figs. 98, 99, 108, 109), thalamus
('396, fig. 81; '42, figs. 71, 81), and tectum opticum (figs. 93, layer 2,
101; '42, figs. 26, 30, 32, 79-83). Many of the long tracts lie within
this layer and have been differentiated from it. Most of the specific
nuclei of higher animals, including the outer gray layers of the
tectum, have been formed by migration of neuroblasts from the central
gray outward into this layer. Here we find much of the ap[
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paratus of local reflexes and their organization into the larger, innate
patterns of behavior.
4. The superficial neuropil is a subpial sheet of dendritic and axonal
terminals, in some places absent, in others very elaborately organized.
Here are some of the most highly specialized mechanisms of
correlation in the amphibian brain, from which specific nuclei of
higher brains have been developed. Notable examples are seen in the
interpeduncular neuropil (chap, xiv) and the ventrolateral neuropil
of the cerebral peduncle described in the next section. This neuropil
seems to be a more sensitive medium for strictly individual adjustments
(conditioning) than the deeper neuropil, but of this there is no
experimental evidence. This hypothesis is supported by the fact that
in higher animals cerebral cortex develops within this layer and
apparently by neurobiotactic influence emanating from it.
In the first synapses observed in embryogenesis numerous axonic
terminals converge to activate a single final common path (Coghill,
'29, p. 13), This is the first step in the elaboration of neuropil. As
differentiation advances, neurons are segregated to serve the several
modalities of sense and the several systems of synergic muscles, and
these systems are interconnected by central correlating elements. In
no case are these connections made by an isolated «hain of neurons in
one-to-one contact between receptor and effector. The central terminals
of afferent fibers from different sense organs are widely spread
and intermingled. Dendrites of the correlating cells branch widely in
this common receptive field, and the axons of some of them again
branch widely in a motor field, thus activating neurons of the several
motor systems. This arrangement is perfectly adapted to evoke mass
movement of the entire musculature from any kind of sensory stimulation,
and this is, indeed, the only activity observed in early
embryonic stages.
It is the rare exception rather than the rule for a peripheral sensory
fiber to effect functional connection directly with a peripheral motor
neuron. One or more correlating elements are interpolated; and, as
differentiation advances, the number of these correlating neurons is
enormously increased in both sensory and motor zones and also in
the intervening intermediate zone. The axons of these intrinsic elements
ramify widely in all directions, and, as a rule, they or collaterals
from them interweave to form the closely knit fabric which
pervades both gray and white substance everywhere. This is the
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axonic neuropil, within the meshes of which dendrites of neurons
ramify widely. These axons are unmyelinated, and every contact
with a dendrite or a cell body is a synaptic junction. Eveiy axon contacts
many dendrites, and every dendrite has contact with many
axons, and these may come from near or from very remote parts.
All neuropil is a synaptic field, and, since in these amphibian brains
it is an almost continuous fabric spread throughout the bram, its
action is fundamentally integrative. But it is more than this. It is
germinative tissue, the matrix from which much specialized structure
of higher brains has been differentiated. It is activated locally or
diffusely by every nervous impulse that passes through the substance
of the brain, and these impulses may irradiate for longer or shorter
distances in directions determined by the trend of the nerve fibers of
which it is composed. This web of conductors is relatively undifferentiated,
but it is by no means homogeneous or equipotential, for each
area of neuropil has characteristic structure and its own pattern of
peripheral and central connections. Many of these fibers, which take
long courses, may connect particular areas of gray substance either
in dispersed arrangement or assembled as recognizable tracts. In
fact, we find all gradations between an almost homogeneous web of
neuropil and long well-fasciculated tracts of unmyelinated or myelinated
fibers. Many of these long fibers have collateral connections
throughout their length; others are well-insulated conductors between
origin and termination.
The web of neuropil shows remarkable diversity in different regions.
In some places it is greatly reduced, as, for instance, in the
ventral funiculi, where the alba is densely filled with myelinated
fibers; in other places there are local concentrations of dendrites and
finest axons so dense that in ordinary haematoxylin or carmine preparations
they appear as darker fields, the Punksuhstanz of the early
histologists and the glomeruli of the olfactory bulb and interpeduncular
nucleus (chap. xiv). When some of these fields are analyzed,
it is found that their fibrous connections conform with those of
specific "nuclei" of higher brains. In Ambly stoma such a field is not a
"nucleus," for it contains no cell bodies; but examination of the corresponding
area in anurans and reptiles may show all stages in the
differentiation of a true nucleus by migration of cell bodies from the
central gray outward into the alba ('27, p. 232). Such a series of
phylogenetic changes can be readily followed in the corpus striatum,
the geniculate bodies, the interpeduncular nucleus, and many other
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places and particularly in the tectum opticum and the pallial fields
of the cerebral hemispheres.
In phylogeny the long, well-organized tracts seem to have been
formed by a concentration of the fibers of the neuropil. The diffuse
neuropil is probably the primordial form, going back to the earliest
evolutionary stages of nervous differentiation (coelenterates) . Local
reflex arcs and specific associational tracts have been gradually differentiated
within it, that is, integration precedes local specialization,
the total pattern antedates the partial patterns. In ontogeny,
especially of higher animals, this history may not be recapitulated,
and tracts serving local reflexes may appear very early; but in
Amblystoma, even in the adult stage, there are few tracts which are
compactly fasciculated and free from functional connection with the
surrounding neuropil. Most of the long, well-fasciculated tracts have
some myelinated fibers that seem to have functional connections
only at their ends; but these are accompanied by others, which are
without myelin and are provided with numberless collaterals tied
into the enveloping neuropil. There is, accordingly, a seepage of
nervous influence along the entire length of these tracts.
From the primordial diffuse neuropil, differentiation advanced in
two divergent directions. One of these, as just pointed out, led to the
elaboration of the stable architectural framework of nuclei and tracts,
the description of which comprises the larger part of current neuroanatomy.
This IS the heritable structure, which determines the basic
patterns of those components of behavior which are common to all
members of the species. The second derivative of the primordial
neuropil is the apparatus of individually modifiable behavior — conditioning,
learning, and ultimately the highly specialized associational
tissues of the cerebral cortex. In both phylogeny and ontogeny,
differentiation of the first type precedes that of the second. Primitive
animals and younger developmental stages exhibit more stable and
predictable patterns of behavior; and the more labile patterns are
acquired later. In Amblystoma both these types of differentiation are
at low levels, but they are sufficiently advanced to be clearly recognizable.
Tissue differentiation is further advanced in the white substance
than in the underlying gray.
During the course of this progressive specialization of tissue, the
primordial integrative function of the neuropil is preserved and
elaborated. The mechanism employed is seen in its most generalized
form in the deep periventricular neuropil, layer 1 of the preceding
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analysis. This is a close-meshed web of finest axons, within which all
cell bodies are imbedded. It is everywhere present, providing continuous
activation (or potential activation) of every neuron, summation,
reinforcement, or inhibition of whatever activities may be going
on in the more superficial layers and affecting the general excitatory
state of the whole central nervous system. It receives fibers from all
sensory and motor fields and seems to be the basic apparatus of integration.
In man this type of tissue survives in the periventricular
gray of the diencephalon, and, as suggested by Wallenberg ('31), it
probably plays an important part in determining the disposition and
temperament of the individual ('34rt, pp. 241, 245). This unspecialized
tissue may serve the most general totalizing function. From it
there have been derived the complicated mechanisms for synthesizing
the separate experiences and organizing them in adaptive patterns
— a process of differentiation which culminates in the human
cerebral cortex. The relations of neuropil to reflex arcs are discussed
in chapter vi.
The relative abundance of myelinated fibers is a rough indicator of
the relation between stable and labile types of performance. Thus
the myelinated white substance is relatively greater in the spinal
cord than in the brain, and the ratio of myelinated to unmyelinated
tissue diminishes as we pass forward in the brain, as is well illustrated
by a published series of Weigert sections drawn from a single specimen
(no. IIC) from the olfactory bulb to the spinal cord ('10, figs.
8-21; '25, figs. 2-9; '44&, figs. 1-6). This is because the myelinated
fibers, most of which are long conductors of through traffic, tend to
be compactly arranged, with relatively scanty collateral connections
with the neuropil.
In the gray substance there is a similar increment m relative
amount of neuropil as we pass forward from spinal cord to hemispheres,
the higher levels being specialized for correlation, association,
conditioning, and integration and the lower levels for stabilized
total activities and reflexes. In the phylogenetic series this principle
takes a form which can be quantitatively expressed as Economo's
coefiicient of the ratio between total gray substance and the mass of
the nerve cells contained within it. The lower the animal species in
the scale, the greater is the mass of the cells compared with the gray
substance. This law may be expressed in the converse form: Higher
animals have a larger proportion of neuropil in the gray substance,
thus giving them capacity for conditioning and other individually
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acquired patterns of behavior (Economo, '26, '29). No mathematical
precision should be claimed for these laws, but they do express the
general trend of our experience. For additional data and critical
comment see von Bonin on page 64 of the monograph by Bucy and
others ('44).
The properties of amphibian neuropil have been discussed in several
places, in addition to the summary already cited ('42, p. 199).
In one of these papers ('33c?) the geniculate neuropil of Necturus was
described, and later ('42, p. 280) the quite different arrangement of
Anibly stoma (compare the corresponding structure of the frog, '25),
together with a full account of the neuropil of the optic tectum and
its connections (here, again, comparison with the more differentiated
structure of the frog is instructive). In connection with a general
survey of the neuropil of Necturus, its peculiar relations in the pallial
part of the hemisphere were discussed in four papers ('336, p. 176;
'336?, '34, '34a). Amblystoma is similar ('27), though the details have
not been fully explored. In the pallial field the four layers of neuropil
tend to merge into a single apparatus of association. This is corticogenetic
tissue within which the earliest phases of incipient differentiation
of laminated cortex can be recognized in the hippocampal area,
as described in chapter vii.
Some samples of the appearance of elective Golgi impregnations of
amphibian neuropil are shown in the accompanying illustrations, and
many others are in the literature. The related morphological and
physiological problems can best be presented in the form of illustrative
examples, one of which is the striatal neuropil (chap, vii), another
the interpeduncular neuropil described in chapter xiv, and still
another in the superficial ventrolateral neuropil of the peduncle,
the area ventrolateralis pedunculi, which will next be described.
The "peduncle" in the restricted sense as here defined, together with the adjoining
tegmentum, is the chief central motor pool of the skeletal muscles. Efferent fibers
from it are among the first to appear in the upper brain stem in embryogenesis,
descending in the primary motor path, which is the precursor of the fasciculus
longitudinalis medialis, and activating the musculature of the trunk. A second
efferent path, which appears very early, goes out directly to the periphery through
the oculomotor nerve. The first sensory influence to act upon this pool comes from
the optic tectum through the posterior commissure in the S-reaction stage. In subsequent
stages it is entered by fibers from many other sources, including the basal
optic tract (fig. 14) and the olfacto-peduncular and strio-peduncular tracts (fig. 6).
In the adult animal, motor impulses issuing from this pool are probably concerned
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primarily with synergic activation of large masses of muscle, notably those concerned
with locomotion and conjugate movements of the eyes. Control of the
movements directly involved in seizing and swallowing food is believed to be
chiefly in the isthmic tegmentum, and this apparatus matures later n ontogeny.
The chief synaptic connections of the great motor pool of the peduncle are in the
intermediate, deep, and periventricular layers of neuropil. External to these is a
ventrolateral band of dense neuropil extending from the root of the III nerve forward
along the entire length of the peduncle. In former papers this has been termed
"area lateralis tegmenti" and "nucleus ectomamillaris," but both these names now
seem to me inappropriate ('4'-2, p. 233). This band receives at the anterior end all
the terminals of the large basal optic tract (figs. U, 94) and, at the posterior end,
terminals of the secondary and tertiary ascending ^'isceral sensory and gustatory
tracts (figs. 8, 23). The terminals of these two systems of fibers are intimately interlaced,
and among them are dendritic arborizations of tlie underlying cells of the
peduncle into which optic, olfactory, and visceral systems of nervous impulses converge
and through which the combined effect is transmitted in the outgoing motor
pathways. These seem to be the primary components of this neuropil, and to them
are added axonic terminals from a wide variety of sources, the most notal)le of which
are sketched in figure '23 (compare Necturus, '34, p. 103 and fig. 4).
The peduncular dendrites, which arborize within this neuropil, include some
from the nucleus of the oculomotor nerve (fig. 24; '42, p. 275), so that here fibers of
the basal optic tract coming directly from the retina may synapse with peripheral
motor neurons — one of the rare examples of a two-neuron arc witli only one synapse
between the peripheral receptor and the effector, though even here there are at
least two additional synapses in this arc within the retina. Other peduncular
neurons may transmit retinal excitations downward through the ventral tegmental
fascicles to all lower motor fields.
At its anterior end this neuropil is connected by fibers conducting in both directions
with the dorsal (mamillary) part of tlie hypothalamus, as in Necturus
('346, fig. 3), and also with its ventral (infundibular) part (fig. 23; "42, pp. 226, 227).
This is an extension of the visceral-gustatory tract into the hypothalamus, and it
may be that some of the visceral fibers pass without interruption through the
peduncular neuropil to the hypothalamus, though this has not been satisfactorily
demonstrated. In some fishes such a direct connection is evident and large; in
mammals the course of the ascending visceral-gustatory path is still uncertain.
Other connections of this neuropil, as shown in figure 23, include terminals of the
olfacto-peduncular tract from the anterior olfactory nucleus, probably the nervus
terminalis (observed in Necturus) fibers from the tectum, pretectal nucleus, dorsal
and ventral thalamus, and terminals of the fasciculus retroflexus (p. 202 and fig. 20).
These terminals of fibers from surprisingly diverse sources are all closely interwoven
with one anotlier and with the terminal dendrites of peduncular neurons, a unique
arrangement occurring, so far as known, only in Amphibia. I have indulged in the
following speculations upon its possible physiological significance.
In the first place, it is clear that this curious tissue is either an undifferentiated
primordium of a number of structures which are separately differentiated in more
specialized brains, or else it is a retrograde fusion of several such structures. The
former supposition seems more probable, for the phylogenetic history of one of its
components is easily read ('25, pp. 443-49). In Necturus there are no cell bodies
directly associated with this neuropil; in Amblystoma a few cells have migrated
out of the gray layer to its border (fig. 24) ; and in the frog the optic component of the
neuropil is separate and surrounded by a spherical shell of cell bodies, which is a true
basal optic nucleus (Gaupp, '99, p. 54, fig. 19). This nucleus attains large size and
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complexity in some reptiles, as described by Slianklin ('3.'3) and others. In the mammals
it retains its individuality as the chief terminus of basal optic fibers, though
other fibers of this system are rather widely spreatl in the surrounding tegmentum
(Gillilan, '41). The history of the visceral and other components of the amphibian
ventrolateral neuropil has not yet been written.
In my recent description ('42) of the optic system of Amblystoma, special attention
was given to the central distribution of thick and thin fibers from the retina,
and this was followed ('42, p. 295) by some speculations about its physiological significance.
In development the thick fibers appear first, and the number of thin
fibers is enormously increased in later stages, particularly at the time of metamorphosis.
Thick fibers conduct more rapidly than thin fibers, and this time factor
may play an important part in the central analysis of mixed retinal excitation.
Both thick and thin fibers end in the thalamus, pretectal nucleus, and tectum;
and in each of these fields their terminals are mingled, not segregated. The optic
fibers to the basal peduncular neuropil are moderately thick; upon retinal stimulation
this field, accordingly, is the first to be activated, and its excitation of the underlying
peduncular neurons may precede any influence upon these cells from the longer
paths by way of the tectum and thalamus. Figure 22 shows in continuous lines the
major optic tracts and the motor paths from the peduncle, and in broken lines some
internuncial connections. The thick fibers which descend from the tectum and
thalamus are myelinated; some of them are crossed in the posterior commissure
and the commissure of the tuberculum posterius, and some are uncrossed. They
connect primarily with the descending pathway in the ventral tegmental fascicles
(f.r.t.). The thinner correlating fibers take other pathways, and they may make
synaptic connection with peduncular neurons in any one or all of the four layers of
the neuropil. The efl'erent path may be to low er motor centers through the ventral
tegmental fascicles or to the muscles of the eyeball through the III nerve.
Figures 24 and 93 are diagrammatic transverse sections at the level of the III
nuclei and the middle of the tectum, illustrating some of the tecto-peduncular connections.
These fibers are all of medium or thin caliber and, for the most part,
unmyelinated. The dendrites of the peduncular neurons ramify widely throughout
the entire thickness of the brain wall, and few, if any, of them are in physiological
relation with any single one of the afferent systems of fibers. Each of them may be
activated by any or all of these systems. The only significant localized specialized
tissue here seems to be in the neuropil, where the texture is different in the four layers
and where all peduncular neurons spread their dendrites in all these layers. Since
the movements which are activated from this motor pool are not disorderly convulsions,
it is evident that the discriminative and well co-ordinated responses which
follow its excitation are not ordered primarily by the arrangement in space of the
motor elements. There are differences in the structural arrangements of the synaptic
junctions, though these are not so pronounced as in most other animals, and there
may be chemical and other factors yet to be determined. As I have elsewhere
pointed out, a time factor can be recognized by physiological experiment, and its
structural indicator can be identified histologically because large fibers have a faster
rate of conduction than small fibers and the interpolation of synaptic junctions in a
nervous pathway retards transmission.
In the structural setup before us it may be inferred that the first result of a retinal
excitation is the activation of the entire tectum, pretectal nucleus, and dorsal thalamus
through the tliick myelinated fibers of the optic nerve and tract and also of the
ventrolateral neuropil of the peduncle through the basal optic tract. This is presumably
a generalized nonspecific effect, and it will come to motor expression,
first, through the basal tract, for this is the shortest path. The resting state is
[Begin Page: Page 38]
changed to a state of excitation in both the peduncular gray and the peripheral
musculature with which it is connected. This is immediately followed by volleys
from the tectum, pretectal nucleus, and thalamus tlirough the myelinated tectoand
thalamo-peduncular tracts; and this may contribute a spatial factor determined
by the position of the exciting object in the visual field and the sector of the tectum
upon which this local stimulus is projected. The first overt movement, accordingly, is
an orientation of the body and the eyeballs with reference to the source of stimulus.
After an appreciable time the smaller fibers from the retina deliver their volleys, and
the small fibers of the correlating tracts are activated. These deliver to the peduncle,
not unmixed or purely visual impulses but discharges, fired or inhibited, as the case
may be, by the existing excitatory state of the correlating apparatus: and this, in
its turn, is determined by numberless nonvisual features of the total situation,
present and past. If, for instance, one of the visual or nonvisual components is
fatigued, this will affect the pattern of tectal discharge.
In salamanders the delay between the preliminary orientation of the body and the
consummation of the reaction may be, and commonly is, very long — a period of
tension, which in a man we would call "attention" and which Coghill called the
"regarding" reaction (p. 78; Coghill, '33, Paper XI, p. 334; '36). During this
period an inconceivably complicated resolution of forces is in process within the
central apparatus of adjustment. Inhibition plays an important role here, and it may
be that the chief function of the ventrolateral superficial neuropil of the peduncle is
control of the inhibitory phase of these activities comparable with tliat suggested in
chapter xiv for the specific interpeduncular neuropil. Of the details of these adjustments
our knowledge is scanty, but some hints may be gathered from urther examination
of the structure involved; and here, to simplify the problem, we shall confine
tJie discussion to the superficial peduncular neuropil.
This neuropil is interpolated "in series" in the visual-motor path of the basal
optic tract, and this short circuit is connected "in parallel" with the longer visualmotor
circuits by way of the tectum and thalamus. The latter are very much larger
and more complicated, and they evidently comprise the major part of the apparatus
by which behavior is regulated by visual experience. The basal optic system
seems to be ancillary to the major system and to be related with it in two quite
different ways, first, as a nonspecific primary activator, as already explained, and,
second (and subsequently), as a device for modifying or "inflecting" (to borrow
Arnold Gesell's expression) the standard patterns of behavior by intercurrent influence
of present activity in other fields, including, perhaps, conditioning and the
individuation of hitherto unaccustomed types of response. This second feature involves
further consideration of the nonvisual components. These have already been
listed, and some of them are shown in figure 23.
The largest components of this peculiar neuropil are the optic and tlie visceralgustatory
systems, and their fibers end exclusively here. This is why these are regarded
as the primary components; all other systems of entering fibers are spread
more or less widely also in the deeper layers of peduncular neuropil. In the visceralgustatory
system this neuropil is inserted in series in the ascending pathway
toward the hypothalamus, and there is probably a parallel system of conduction
with no synapse in the peduncle (fig. 8). As seen in tliis figure, peduncular neurons
activated from this neuropil send axons around the tuberculum posterius into the
hypothalamus; and there is a return path from both dorsal (mamillary) and
ventral (infundibular) parts of the hypothalamus to this neuropil and contiguous
parts of the peduncle (figs. 18, 'TIS). All visceral-gustatory influences which reach
the hypothalamus are, accordingly, previously modified or "inflected" in the superior
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visceral nucleus or in the peduncle. The excitatory state of the hypothalamus, in
turn, affects all activity in the peduncle.
This sort of circular activity is everywhere present in these urodele brains,
working through the diffuse periventricular and deep neuropil and in many places
also through specially differentiated tracts (p. 76). This is the primordial apparatus
of integration, and in its more differentiated form it is part of the apparatus
by which individuated partial patterns of local reflexes are kept in appropriate
relationship with the larger total patterns of behavior.
In a recent survey ('44o) of tlie optic and visceral nervous circuits here under
consideration, several different patterns of linkage of the component units were
listed. These include direct activation of eye muscles through the basal optic tract,
similar activation of the skeletal musculature, indirect activation of either or both
of these sj^stems of muscles by visual stimuli through the tectum and thalamus,
direct activation of either or both systems of muscles through the visceral-gustatory
path, indirect visceral -gustatory action by way of the superior visceral nucleus,
with or without intercurrent influence of the tectum upon this nucleus by way of
the tecto-bulbar tract, and the variable effects of concurrent discharge of many
other systems of fibers into each of the centers of adjustment involved. Since eacli
of these patterns of linkage is complex and the structural units themselves are not
simple, it is evident that in actual performance the number of ways in which the
known units may be combined and recombined is practically unlimited. The simplest
possible activity of stimulus-response type involves a central resolution of forces in
an equilibrated dynamic system of inconceivable complexity. Oversimplification
of the problem will not hasten its solution.
The preceding description illustrates the relations of a specific field of specialized
neuropil to other parts of the brain with known functions. These visible connections
exhibit a structural arrangement which can be interpreted as putative pathways of
transmission of the several components of a complex action system, some concerned
with stable reflex patterns and some with more labile individually acquired
components. The relations of these two classes of components of the action
system to each other and of local units to the integrated whole present the major
problems of neurology.
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SINCE the brain of Amblystoma presents a generalized structure
which is probably close to the ancestral type from which all
more highly specialized vertebrate brains have been derived, the
salient features of internal organization are here summarized in
schematic outline. Tlie accompanying diagrammatic figures 1-24
give the necessary topographic orientation, and the details may be
filled in by reference to the corresponding sections of Part 11. What
is here described may be regarded as the basic organization of the
brains of all vertebrates above fishes, that is, the point of departure
from which various specialized derivatives have been differentiated.
Amblystoma possesses the equipment of sensory and motor organs
typical for vertebrates at a rather low level of specialization and in
evenly balanced relations. All the usual systems are present, and none
shows unusual size or aberrant features. The great lateral-line system
of sense organs so characteristic of fishes is preserved, though somewhat
reduced after metamorphosis. On the motor side the organs of
locomotion and respiration have advanced from the fishlike to the
quadrupedal form, but in very simple patterns. In early phylogeny
the specialization of the motor systems seems to lag behind that of
the sensory systems because the aquatic environment of primitive
forms is more homogeneous than that of terrestrial animals, and,
accordingly, fewer and simpler patterns of behavior are needed.
Our search in this inquiry is for origins of human structures and
for an outline of the history of their evolution. From this standpoint
it is evident that in the central nervous systems of all vertebrates
there is a fundamental and primary difference between the cerebrum
above and the rhombencephalon (and spinal cord) below a transverse
plane at the posterior border of the midbrain (for further discussion
of this see chaps, viii and xiii).
The spinal cord and rhombic brain contain the central adjustors of
the basic vital functions — respiration, nutrition, circulation, reproduction,
locomotion, among others. This apparatus is elaborately
organized in the most primitive living vertebrates, as also no doubt
it must have been in their extinct ancestors. The cerebrum, on the
[Begin Page: Page 41]
other hand, except for the olfactory component, is a hiter acquisition.
This is suggested by what is seen in Amphioxus and by the retai-ded
development of the cerebrum in all vertebrate embryos, as illustrated
especially clearly in the early fetal development of the opossum.
At an early (and unknown) period of vertebrate ancestry a pair of
eyes was differentiated. These and the olfactory organs are the leading
distance receptors, and as such they gave to the vertebrate
ancestors more information about their surroundings and hence
greater safety in moving about freely. The nose and eyes, with the
associated oculomotor apparatus, early assumed the dominant role
in the recognition of food, mates, and enemies, and their cerebral
adjustors were enlarged accordingly. The contact receptors are adequate
for sedentary, crawling, or burrowing ancestors, and here the
response to stimulation follows immediately. But, as Sherrington
long ago pointed out, in a free-swimming animal there is a time lag
between reception of the stimulus from a distant object and the consummation
of the response. The pregnant interval between the anticipatory
and consummatory phases of the reaction gives the clue to an
understanding of the entire history of forebrain evolution. During
this interval there is a central resolution of forces, which eventuates
in appropriate behavior; and, with increasing complication of patterns
of behavior, this central apparatus of adjustment assumes more
and more structural complexity and physiological dominance over
the entire bodily economy (chap. vii).
The details of these internal connections are not relevant here. It
suffices to present two summaries, one in this chapter in topographic
arrangement by regions from spinal cord to olfactory bulbs as conventionally
described and one in the next chapter on a different plan,
i.e., an arrangement in longitudinal zones which are functionally defined.
For the present purpose it is convenient to recognize seventeen
subdivisions of the central nervous system, each of which is characterized
by special physiological activities, though these activities
are not localized here exclusively. This subdivision might be carried
further into detail indefinitely. Numbers 2-6 in the following paragraphs
are in the rhombic brain; the others are in the cerebrum.
The spinal cord is not described in this report except for some features
closely related to the brain, to which reference is made in the
next paragraph. The cord segments are organized for the regulation
[Begin Page: Page 42]
of local reflexes of the limbs and the integration of these reflexes with
one another and with the action of the trunk musculature, as in
ordinary locomotion.
The sector of the bulbo-spinal junction includes the upper segments
of the spinal cord and the lower part of the medulla oblongata.
It is the first center of correlation to become functional in embryonic
development (Coghill, '14, Paper I). Its dorsal part around the
calamus scriptorius receives fibers from the entire sensory zone of the
bulb and cord, so that this gray of the funicular and commissural
nuclei is a general clearing-house for all exteroceptive, proprioceptive,
and visceral functions of the body except vision and olfaction.
Here these functions are integrated in the interest of control of posture,
locomotion, visceral activity, and other basic components of
mass-movement type. Some of these connections are shown diagrammatically
in figures 3, 7, 8, 87; for details and discussion see chapter
ix and a recent paper ('446).
Efferent fibers from the dorsal nuclei are directed spinalward and
forward. Most of the latter connect with motor nuclei of the medulla
oblongata; some go farther forward to the cerebellum, tectum, and
thalamus; and there is a strong, ascending visceral-gustatory tract
to the isthmus and peduncle. The motor zone of this sector is occupied
chiefly by fibers of passage. The moderately developed gray substance
includes motor neurons for muscles of the neck region, for the
tongue muscles, and for special visceral motor elements of the accessorius
component of the vagus.
The medulla oblongata, or bulb, includes all the stem between the
isthmus and the calamus scriptorius except the cerebellum, there
being no pons. Its dorsal field receives all sensory fibers from the
head except the optic and olfactory, fibers from lateral-line organs
widely distributed over the body, and general visceral sensory fibers
chiefly by way of the vagus. The general visceral sensory and gustatory
root fibers are segregated from the others in the fasciculus
solitarius; and this group has its own system of secondary fibers,
which converge into the visceral motor nuclei of the medulla oblongata
and spinal cord. There is also a strong ascending secondary
visceral tract {tr.v.a.) to the isthmus, peduncle, and hypothalamus,
through which all cerebral activities may be influenced by visceral
and gustatory functions (fig, 8 and chaps, x, xi).
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U'lie other afferent fibers of the V to X cranial nerves, upon entrance
into the brain, are fascicuhitetl according to the functional systems
represented, as outlined in the next chapter and shown in figures 7, 9,
88, 89, 90. The general cutaneous, lateral-line, and vestibular fibers
are arranged in a series of fascicles bordering the external surface;
the visceral sensory and gustatory fibers are assembled in a single
deeper bundle, the fasciculus solitarius. The marginal fascicles of
root fibers are arranged from ventral to dorsal in the following order :
general somatic sensory (chiefly cutaneous), vestibular, and, dorsally
of these, five or six fascicles of fibers of the lateral-line roots of the
VII and X nerves. The details of this arrangement are variable within
the species and from species to species of urodeles. The fascicles of
vestibular and lateral-line roots, together with the underlying gray
and the intervening neuropil, comprise the area acusticolateralis.
The dorsal part of this, which receives only roots of the lateral-line
nerves, is lobulated on the ventricular side.
Most of these root fibers divide into ascending and descending
branches, and each fascicle spans the entire length of the medulla
oblongata. Some of the general cutaneous and vestibular fibers extend
far down into the spinal cord and upward into the cerebellum
(figs. 3, 7). Terminals and collaterals of all these fibers end in a common
pool of neuropil, from which secondary fibers go out to effect
local connections in the medulla oblongata, to enter the cerebellum,
to descend to the spinal cord, and to ascend in the lemniscus systems
to the tectum and thalamus. The physiological specificity of the root
fibers i.s largely, though not entirely, obliterated at the first synapse
in the neuropil of the sensory field, in sharp contrast with the mammalian
arrangement (chap. xi).
Prom this arrangement of the sensory systems of fibers and their
central secondary connections it is clear that the bulbar structure is
so organized as to facilitate mass movements of total-pattern type,
which may be activated by any one of the exteroceptive or proprioceptive
systems or by any conibination of these. There is some provision
here for local reflexes of the muscles of the head, but the structure
indicates that most of these are patterned from higher centers.
The central receptive field of the visceral-gustatory system is well
segregated from that of the general cutaneous and acousticolateral
systems; and this is the structural expression of the fundamental distinction
between the visceral and the somatic sensory physiological
systems, to which further reference is made on pages G7 and 83.
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Otherwise, there is httle histological evidence of precise localization
of function in the medulla oblongata. The visceral and somatic sensory
fields are cross-connected within the sensory zone, and they
converge into a common sensory field at the bulbo-spinal junction.
Proprioceptive adjustments are made throughout the spinal cord,
medulla oblongata, cerebellum, and tectum; and each of these regions
evidently plays a different role in the adjustments. Arcuate
fibers connect all parts of the sensory zone with the motor zone of the
same and the opposite side, and many of these divide into longdescending
and ascending branches, thus activating extensive areas
of the intermediate and motor zones.
The motor field of the medulla oblongata and the intimately related
reticular formation contain the complicated apparatus by
which the nuclei of the motor nerves are so interconnected as to act
in groups, each of which may execute a series of co-ordinated actions
in patterns determined by these connections. The tissues of the motor
tegmentum, which effect this analysis of motor performance, are so
intricately interwoven that it has not been possible to recognize the
components of the several functional systems, and further analysis
of this field is desirable.
The cerebellum is small and very simply organized, but the chief
structural features of the mammalian cerebellum are present except
the pontile system, which is totally lacking. The urodele cerebellum
consists of three major parts: (1) the median body, activated from
the spinal cord, trigeminal nerve, and tectum (figs. 1, 3, 10); (2) the
lateral auricles, which are enlargements of the anterior ends of the
sensory zones of the medulla oblongata (figs. 7, 91); and (3), ventrally
of the body of the cerebellum, a nucleus cerebelli, which is the
primordium of the deep cerebellar nuclei of mammals (figs. 10, 32,
This analysis of cerebellar structure is based on the comprehensive
studies of Larsell ('20-'47) and Dow ('42), whose descriptions of
Amblystoma, published in 1920 and 1932, I have confirmed in all
respects. It should be noted that my definition of the amphibian
auricle includes more than Larsell's, for he includes in this structure
only the vestibular and lateral-line components. I find that these
terminals and the related field of neuropil are so intimately related
with the terminals of the trigeminus, the visceral-gustatory system,
and lemniscus fibers that their segregation is not practical anatomi-
[Begin Page: Page 45]
cally. The auricle, accordingly, is here regarded as the common
primordium of several structures which in higher animals are diversely
specialized for different functions. The most notable of these
are the superior or pontile nucleus of the trigeminus and the floccular
part of the flocculonodular lobe of the cerebellum. The primordia of
these structures are clearly evident, and the history of their further
differentiation in higher animals has been written.
Efferent fibers of tractus cerebello-tegmentalis leave all parts of the
cerebellar complex for the underlying gray; and one fascicle of
these — the brachium conjunctivum — passes forward to a ventral
decussation and distributes its fibers to the isthmic tegmentum of
both sides (figs. 10, 71). No primordium of the nucleus ruber or of the
inferior olive has been recognized.
This primitive cerebellum exhibits the typical vertebrate pattern
in very instructive form, with localization of the vestibular system
laterally and the other systems medially. It is an appendage added
to the basic sensori-motor systems; it supplements them, not as an
aid in determining the pattern of performance, but to insure efficient
execution. In species in which it is greatly enlarged, it contains
enormous reserves of potential nervous energy, which is released during
motor activity to reinforce and stabilize the operation of the
effectors. For additional details see chapters x and xii.
The isthmus is unusually large in urodeles and is clearly circumscribed
from surrounding parts. Dorsally it is small, containing in
and near the superior medullary velum a special segment of the
mesencephalic V nucleus and probably other peripheral connections
through the nerves of the chorioid plexuses and meninges. Below this
there is the superior visceral-gustatory nucleus (figs. 2B, 8, 23, 34).
The nucleus isthmi, which is large in the frog, is here undifferentiated.
The ventral part of the isthmus is very large, containing the nucleus
of the IV nerve and a mass of tegmental cells. This isthmic tegmentum
is interpolated between the primary sensori-motor systems of the
medulla oblongata and midbrain, and it serves as an intermediary
between them. There is a large central nucleus of small cells which
receives fibers from a wide variety of correlation centers of intermediate-
zone type. These enter by all the dorsal tegmental fascicles
and by several other paths (figs. 16, 17, 21). This nucleus is enveloped
by a group of larger cells, which is continuous posteriorly with similar
tegmental cells of the region of the trigeminus (figs. 29, 30, 91). The
[Begin Page: Page 46]
complex as a whole is believed to have two chief functions: (1) Here
are organized the patterns of the local reflexes of the musculature of
the head, particularly those concerned with feeding. (2) The smallcelled
central nucleus is a special differentiation of the periventricular
gray, which serves, in addition to the specific functions just mentioned,
a more general, nonspecific, totalizing function; that is, it is a
part of that integrating apparatus which appears in mammals as the
dorsal tegmental nucleus and the related fasciculus longitudinalis
dorsalis of Schiitz (p. 208). The details of structure are given in
chapter xiii.
The isthmic tegmentum occupies a strategic position between the
primitive bulbo-spinal mechanisms and the higher cerebral adjustors;
it plays a major role both in the patterning of local reflexes and in the
integration of all bodily activities. This mass of tissue, which in
urodeles is at a low level of differentiation, in higher animals is split
up and distributed so that in mammals the identity of the isthmic
tegmentum as an anatomical entity is lost in the adult brain, though
the isthmic sector is plainly marked in the early embryonic stages.
The interpeduncular nucleus also is unusually large in urodeles.
It is not interpeduncular but interisthmic, extending from the fovea
isthmi back to the level of the V nerve roots. The histological texture
is extraordinary. A well-defined, trough-shaped column of cells
borders the ventral angle of the ventricle, with dendrites extending
downward through the ventral commissure, to arborize with tufted
endings in a ventromedian band of neuropil (figs. 65, 66, 82, 83, 91).
The axonic components of this interpeduncular neuropil come from
various sources: (1) terminals of the fasciculus retroflexus, which
take the form of a flattened spiral (fig. 50); (2) terminals of tr.
tegmento-interpeduncularis from small cells of the overlying tegmentum
with tufted endings, which join with the dendritic tufts of
the interpeduncular nucleus to form small glomeruli (figs. 60-66, 84) ;
(3) collaterals of thick fibers of tr. tegmento-bulbaris from the large
cells of the tegmentum with similar tufted endings in the glomeruli
(fig. 68); (4) collaterals of tr. interpedunculo-bulbaris, which also
enter glomeruli (figs. 83, 84) ; (5) terminals of tr. mamillo-interpeduncularis
with dispersed free endings (figs. 60, 61); (6) similar
terminals of tr. olfacto-peduncularis (fig. 59); (7) less numerous
terminals from several other sources. The slender, unmyelinated
axons of the interpeduncular cells branch freely in the interpeduncu-
[Begin Page: Page 47]
lar neuropil and continue from the nucleus in two strands (figs. 83,
84). The ventral interpedunculo-bulbar tract descends beyond the
nucleus for an undetermined distance in the lip of the ventral fissure.
The dorsal tract descends dorsally of the fasciculus longitudinalis
medialis and turns laterally to end in wide arborizations in the
tegmentum as far back as the IX nerve roots. Associated with these
dorsal fibers are interpedunculo-tegmental fibers, which end in the
neuropil of the isthmic tegmentum. The dorsal and interpedunculotegmental
fibers are regarded as comparable with the isthmic and
bulbar parts of the mammalian f. longitudinalis dorsalis of Schiitz.
The physiological problems suggested by this peculiar structure
are puzzling. In the light of such scanty experimental evidence as we
possess, I have ventured to suggest that the interpeduncular complex
provides both activating and inhibitory components of reflex and
general integrative activities, the actual patterns of which are elsewhere
Topographically, this nucleus lies in the motor zone, but its functions
clearly are of intermediate-zone type. It is present in all vertebrates
at the anteroventral border of the isthmus, that is, at the
boundary between cerebrum and rhombencephalon. Most of its
afferent fibers come from the cerebrum, and evidently it serves chiefly
as an intermediary adjustor between the sensory and intermediate
zones of higher levels and the motor zone of the rhombic brain (for
details see chap. xiv).
At this point in our analysis we. cross the boundary between
rhombencephalon and cerebrum. The radical differences in structure
and physiological properties of these two chief parts of the brain are
masked and in large measure overruled, especially in higher animals,
by ascending and descending connectives, of which the interpeduncular
system is a typical illustration.
The tectum and the pretectal nucleus, as sectors of the sensory
field, together with the dorsal thalamus, form a physiological unit
within which all exteroceptive sensory systems are integrated in the
interest of cerebral control of all lower sensori-motor systems involved
in the operation of the skeletal musculature. This unit is
intimately related with the cerebral peduncle and ventral thalamus.
In the most primitive vertebrates and in early embryonic stages of
all vertebrates, these structures might appropriately be united as a
middle subdivision of the brain, which serves as the dominant center
[Begin Page: Page 48]
of cerebral control of all somatic activities. But in the adult animal
the parts of this natural subdivision have so many distinctive connections
and physiological properties that it seems preferable to
treat them separately.
In vertebrates below the mammals the tectum opticum is the chief
central end-station of the optic nerve; and, since the eyes are the
chief distance receptors in most of these animals, fibers of correlation
of all other sensory systems concerned with external adjustment
naturally converge to this station. The tectum, accordingly, becomes
the dominant adjustor of all exteroceptive systems. The tectum
mesencephali of Aml^lystoma has a larger optic part — the superior
colliculus — and a small, poorly differentiated nucleus posterior — the
primordial inferior colliculus. The latter is interpolated between the
tectum opticum and the cerebellum, and its connections suggest that
its most primitive functions are proprioceptive. It receives a small
primordial lateral lemniscus and evidently also serves such generalized
auditory functions as this animal possesses (chap. xv). The
development of the optic nerve and adult tectal structure and connections
have been described in detail ('41, '42). Chapter xvi is devoted
to the visual system ; for the arrangement of the mesencephalic
nucleus and root of the V nerve see page 140 and figure 13.
Optic and lemniscus tracts and smaller numbers of fibers from
various other sources all terminate in a broad sheet of intermediate
neuropil, which is spread through the entire tectum and is nearly
homogeneous in texture (figs. 11, 93). The tectum is not definitely
laminated, though separation of the layers, which are conspicuous in
the frog, is incipient. Fibers diverge from it in all directions (figs. 12,
18, 21-24, 93). It is inferred from this structure that movements
activated directly from the tectum are of total-pattern type. Such
local visual reflexes as this animal possesses are probably patterned
elsewhere — in the thalamus and dorsal and isthmic tegmentum. Conditioning
of reflexes is probably effected in these areas and perhaps
also in the ventrolateral peduncular neuropil (p. 38). Experiments
upon Triturus and anurans (Stone and Zauer, '40; Sperry, '43, '44,
'45, '456) demonstrate anatomical projection of retinal loci upon the
tectum opticum. This is true also in Amblystoma (Stone, '44; Stone
and Ellison, '45), though the nervous apparatus employed has not
been described.
The pretectal nucleus (figs. 2B, 35, 36, receives fibers directly
from the retina and from the tectum, habenula, and cerebral
[Begin Page: Page 49]
hemisphere. Its efferent fibers go to the tectum, thalamus, hypothalamus,
and cerebral peduncle (figs. 11, 12, 14, 15, 16, 22, 23).
Its functions are unknown, but, by analogy with mammals, this may
be part of the apparatus for regulation of the intrinsic musculature of
the eyeball. Doubtless other functions are represented also. This area
is the probable precursor of the mammalian pulvinar and neighboring
The thalamus receives many fibers from the retina, and it is broadly
connected with the tectum by uncrossed fibers passing in both
directions in the brachia of the superior and inferior colliculi (figs. 11,
12). There are also systems of tecto-thalamic and hypothalamic and
thalamo-hypothalamic tracts which decussate in the postoptic commissure
; some of these crossed fibers take longer courses to reach the
peduncle and isthmic tegmentum (figs. 12, 15). This intimate
thalamo-tectal relationship is radically changed in higher animals,
where the thalamo-cortical connections are highly elaborated.
I have separated the dorsal thalamus into three sectors: (1) anteriorly,
the small nucleus of Bellonci of uncertain relationships ; (2) a
well-defined middle part, an undifferentiated nucleus sensitivus,
which is the primordium of most of the sensory nuclei of the mammalian
thalamus; and (3) a vaguely delimited posterior sector, which
apparently contains the undifferentiated primordium of both lateral
and medial geniculate bodies (chap. xvii).
The middle and posterior sectors receive numerous terminals and
collaterals of the optic tracts, terminals of the general bulbar and
spinal lemnisci, and, through the brachia of the superior and inferior
colliculi, these sectors are broadly connected with the tectum by
fibers running in both directions. There is a similar, but much
smaller, connection with the habenula.
From the middle sector a small, well-defined tr. thalamo-frontalis
goes forward to the hemisphere (figs. 15, 71, 72, 95, 101,;
this is the common primordium of all the thalamo-cortical projection
systems of mammals, though here few, if any, of its fibers reach the
pallial area. Other efferent fibers go to the ventral thalamus, hypothalamus,
peduncle, and tegmentum. These thalamic reflex connections
antedate in phylogeny the thalamo-cortical connections,
and they persist in mammals as an intrinsic paleothalamic apparatus,
an important part of which is the periventricular thalamic contribution
to the f. longitudinalis dorsalis of Schiitz. The largest pathwaj^s
[Begin Page: Page 50]
of efferent discharge from the dorsal thalamus go backward to the
peduncle and tegmentum by both crossed and uncrossed tracts (figs.
15, 18, 21, 23). The peduncular connection puts all the primary systems
of total-pattern type under some measure of thalamic control.
The connections with the dorsal and isthmic tegmentum probably
co-operate in the patterning of local reflexes, particularly supplying
the visual component of the feeding reactions.
The "peduncle" described here is not the equivalent of the human
cerebral peduncle (p. 21). The intimate relations of this field with
the overlying tecto-thalamic field have been commented upon in the
preceding paragraphs. This ventral field is a well-defined column of
cells, differentiated at the anterior end of the basal plate of the
embryonic neural tube. It is the head of the primary motor column
(of Coghill), which in all vertebrates, from early embryonic stages to
the adult, contains the nucleus of the oculomotor nerve and a much
larger mass of nervous tissue, which activates the primitive mass
movements of locomotion. It maintains cerebral control of the lower
bulbo-spinal segments of the latter systems, and some other motor
functions also are represented here. Into it fibers converge from all
other parts of the cerebrum (figs. 12, 14, 15, 17, 18, 20-24), and from
it efferent fibers go out in four groups: (1) Ventromedial tracts go
to the medulla oblongata and spinal cord. The longest of these fibers
are in the f. longitudinalis medialis (fig. 6). (2) The oculomotor nerve
supplies intrinsic and extrinsic muscles of the eyeball (figs. 22, 24).
Associated with these peripheral fibers are central connections with
the nuclei of the IV and VI nerves, so arranged as to execute conjugate
movements of the eyes. The details of the apparatus employed
are unknown. (3) Visceral sensory and gustatory fibers enter the
peduncle (fig. 8), and with these are related efferent fibers to the hypothalamus
and to lower levels of the motor zone, The pathways
taken by the latter in the amphibian brain have not been clarified.
(4) From both ventral thalamus and peduncle, fibers diverge to
various surrounding parts, notably to the hypothalamus and isthmic
tegmentum. These probably provide for co-ordination of various
local reflex activities with the basic peduncular functions.
At the ventrolateral border of the peduncle there is an area of
superficial neuropil, which is the terminus of the basal optic tract,
large secondary and tertiary visceral-gustatory tracts, some fibers of
the f. retroflexus, and fibers from several other sources (figs. 22, 23,
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24). This is an undifferentiated primordium of the basal optic nucleus
and some other structures of the mammalian brain (pp. 35, 221).
It is related with the olfacto-visceral functions of the hypothalamus
and probably also with conditioning of the fundamental peduncular
There are anterior and posterior sectors of the ventral thalamus
which differ in embryological origin (p. 239) and in certain connections
of intermediate-zone type. Both sectors are here included in the
motor zone because their chief efferent connections resemble those of
the "peduncle," of which the posterior part is physiologically an
anterior extension. The ventral thalamus is the primordium of the
motor field of the mammalian subthalamus. The anterior sector contains
a nucleus specifically related to the stria medullaris and
amygdala and, above this, the eminentia thalami, which is a bednucleus
of tracts related to the primordium hippocampi (chap, xviii;
figs. 16, 17, 19, 20, 96).
The ventral thalamus and peduncle of urodeles form a single massive
column, which is anatomically well defined. The specialized
structures derived from it in mammals are dispersed among large
masses of tissue of more recent phylogenetic origin; but in the human
brain this region still retains cerebral control of the primordial coordinated
movements of the musculature of the eyeballs and of the
trunk and limbs.
In early embryonic stages the retina is part of the brain, and, as
development advances, it absorbs much of the diencephalic sector of
the early neural tube. This precociously accelerated development results
from the dominance of vision in exteroceptive adjustment from
the time that the larva begins to feed. For further details of this
development and of the organization of the visual-motor apparatus
see chapter xvi.
1-2. IIABEN(jL.\
As described in chapter xviii, this specialized part of the epithalamus
receives fibers from almost all parts of the telencephalon and
diencephalon and from the tectum (fig. 20). The habenular commissure
connects the two habenulae, and it also contains two commissures
of pallial parts of the hemispheres — commissura pallii posterior
and com. superior telencephali. The chief efferent path from the
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habenula is the f. retroflexus (chap, xviii), which terminates in the
cerebral peduncle and interpeduncular nucleus. In the brains of lower
vertebrates the habenular complex is one of the most widely spread
and physiologically important members of the central correlating
apparatus. Its primary function seems to be to integrate the activities
of all parts of the brain that are under olfactory influence with
the exteroceptive functions of the tectum and thalamus in the interest
of higher cerebral control of the feeding reactions of the skeletal
In the large preoptic nucleus and hypothalamus, olfactory connections
dominate the picture, as they do in the habenular system; but
here the nonolfactory functions represented are interoceptive instead
of exteroceptive. All parts of the cerebral hemisphere are connected
with the hypothalamus by fibers passing in both directions in the
medial forebrain bundles (p. 273), stria terminalis (p. '^55), and
fornix (p. 254) systems. The visceral-gustatory afferent paths are
shown in figure 8. Large tracts from the thalamus and tectum also
end here, so that all kinds of sensory experience of which the animal
is capable are represented in the hypothalamus. This experience is
here organized in terms of visceral responses. The efferent tracts go
to the peduncle, tegmentum, interpeduncular nucleus, and descending
fibers in the deep neuropil which are precursors of the f. longitudinalis
dorsalis of Schiitz. There is a large tract to the hypophysis
for nervous control of endocrine activity. There is also evidence that
some neuro-endocrine functions are performed in the hypothalamus
itself (Scharrer and Scharrer, '40). The structure of the hypothalamus
has been described ('21a, '27. ''^5a, '36, '42, and in the embryological
papers, '37-'41). It is similar to that of Necturus, of which more
detailed descriptions have been published ('336, '346). For the composition
of the postoptic commissure see chapter xxi.
The primordial corpus striatum occupies the thickened ventrolateral
wall of the cerebral hemisphere and, like all the rest of the
hemisphere, is under olfactory influence. This is stronger at its anterior
and posterior ends. Anteriorly, it is divided by a striatal sulcus
into dorsal and ventral parts (fig. 99), and posteriorly it is much enlarged
as the amygdala (figs. 1, 96, 97), which has the typical mammalian
connections (fig. 19).
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The ventral sector of the anterior olfactory nucleus is interpolated
between the olfactory bulb and the corpus striatum, as in Necturus
(figs. 6, 86). This is the primordium of the tuberculum olfactorium
('27, p. 290), which is enormously enlarged in the lungfishes (Rudebeck,
'45). Posteriorly of this nucleus is a poorly defined field, which
embraces the ventral angle of the lateral ventricle and is regarded as
the probable precursor of the head of the caudate nucleus (fig. 99)
It is intimately connected with the rest of the striatum and the
septum. The chief efferent path is the olfacto-peduncular tract to the
dorsal hypothalamus, ventral border of the peduncle, and interpeduncular
The middle sector of this complex is the undifferentiated primordium
of the mammalian lentiform nucleus, as shown by its
fibrous connections. It is characterized by very dense, sharply circumscribed
neuropil in the white substance (p. 96; figs. 98, 99, 108,
109) and has the typical striatal connections with the overlying pallium
and the thalamus, including a small sensory projection tract
from the dorsal thalamus (fig. 15, The chief efferent path is
the lateral forebrain bundle (f. lateralis telencephali, /.Za^./.), which
contains strio-thalamic, strio-peduncular, and strio-tegmental fibers
comparable with the corresponding components of the mammalian
extrapyramidal system. There is also a strio-tectal and strio-pretectal
connection (figs. 11, 14, 101). The separation of the lentiform nucleus
into globus pallidus and putamen is incipient (p. 97).
The septum complex occupies the ventromedial wall of the hemisphere
between the anterior olfactory nucleus and the lamina terminalis
and hippocampal area (figs. 4, 98, 99) . Its position and connections
are similar to those of mammals. It is directly connected
with the olfactory organ by the nervus terminalis, and it receives
fibers from the olfactory bulb, anterior olfactory nucleus, pallium,
and hypothalamus. The chief efferent paths are by the medial forebrain
bundle (f . medialis telencephali, and to the overlying
pallium by the f. olfactorius septi ('27, p. 291). There is also a broad
connection across the ventral aspect of the hemisphere with the
amygdala and the piriform area, the diagonal band of Broca (figs. 96,
97, 98, d.b.), and a connection with the habenula by tr. olfactohabenularis
anterior and tr. septo-habenularis (chap, xviii).
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The olfactory bulb is very large, embracing the anterior end of the
lateral ventricle and extending back in the lateral wall for about half
the length of the hemisphere (figs. 1, 3, 4, 85, 100, 105, 110; '246, '27).
All peripheral olfactory fibers end in the glomeruli of the bulb.
Fibers of the second order pass in large numbers to the anterior
olfactory nucleus, and they enter longer olfactory tracts with wide
distribution (fig. 6), The olfactory tracts are mixtures of fibers from
the bulb and the anterior nucleus, as in Necturus ('336, figs. 6 16).
They reach all parts of the cerebral hemisphere, the habenula, and
the hypothalamus. Some of these decussate in the ventral part of the
anterior commissure and some in the habenular commissure (com.
superior telencephali).
The histological texture of the olfactory bulb is more differentiated
than that of Necturus ('31), but more generalized than that of higher
vertebrates. I have contrasted this with the mammalian pattern and
added a theoretic interpretation of probable differences in physiologic
properties of the tissue ('246). In brief, this tissue is interpreted as
illustrating several transitional stages in the differentiation of polarized
nervous elements from an unpolarized or incompletely polarized
matrix. In Necturus ('31) the transitional character of this tissue is
still more clearly evident. The granule cells, in particular, give no
structural evidence of physiological polarity, i.e., of differentiation
of dendrites from axon, though the connections of these cells in
Amblystoma suggest that they have a transient and reversible polarity.
In connection with this description ('246, pp. 385-95) there are
some speculations regarding possible phylogenetic stages in the differentiation
of permanently polarized neurons from an unspecialized
nonsynaptic nerve net or neuropil.
In Amblystoma there is a moderately developed accessory olfactory
bulb, but no other evidence of local specialization in the primary
olfactory center. (There are hints of this in some mammals, e.g., the
mink, Jeserich, '45, and references there cited). In 1921, I described
the peripheral and central connections of the accessory bulb of
Amblystoma and compared these with the more specialized structures
of the frog. The anatomical connections there described are, I
believe, correct, but the theoretic interpretation of the relationships
in vertebrates generally between the vomeronasal organ, accessory
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bulb, and amygdala is less secure and awaits confirmation or correction.
The anterior olfactory nucleus is a zone of relatively undifferentiated
cells interpolated between the bulbar formation and the more
specialized areas posteriorly of it (figs. 6, 86B and C, 105, 109; '27,
p. 288). In higher animals much of this tissue seems to be specialized
and added to the adjoining fields ('24(/). A very large proportion of
the fibers of the olfactory tracts, arising from both the bulbar formation
and the anterior nucleus, are assembled in a dense superficial
sheet of fibers in the medial sector of the anterior olfactory nucleus,
which I have named the "fasciculus postolfactorius" (figs. 5, 100,
105, 110, /./JO.). Here these fibers take a vertical course and then are
distributed to all the olfactory tracts. In chapters vii and xix there
is further discussion of the significance of the olfactory system in the
morphogenesis of the hemisphere.
The pallial part of the hemisphere can be distinguished from the
stem part, though there is no laminated cortex. There are three sectors
(figs. 96-99) — the dorsomedial primordium hippocampi {p.hip.),
the dorsolateral primordium piriforme {p.pir., or nucleus olfactorius
dorsolateralis, nuc.oLd.L), and between these a dorsal sector of uncertain
relationships (p.p.d.). The gray, as elsewhere in these brains,
is confined to a thick periventricular layer except in the hippocampal
sector, where the cell bodies are dispersed through the entire thickness
of the wall and are imbedded in dense neuropil. This is evidently
a first step toward differentiation of superficial cortex. The homologies
of the hippocampal and piriform sectors with those of mammals
are clear, as shown by substantially similar nervous connections.
Further discussion will be found in chapter vii and the references
there given.
Throughout the length of the central nervous system all parts of
the two sides are broadly connected by systems of commissural and
decussating fibers. These are in two series, dorsally and vent rally of
the ventricles. Their composition is summarized in chapter xxi, with
references to more detailed descriptions. In the aggregate they make
provision for the co-ordinated action of the motor organs on right and
left sides of the body.
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The preceding outline of a regional analysis is framed in very general
terms. The evidence upon which it is based is assembled in Part
II of this work and references there given. This evidence, though far
from complete, is regarded as adequate for the anatomical arrangements
described. The physiological inferences drawn from these arrangements
and the general theory expressed in the following chapters
rest on a less secure basis. The correctness of these conclusions
can be tested experimentally, and the hope that this will be done has
motivated the labor expended upon this program of histological
[Begin Page: Page 57]
THE brain of Amblystoma performs three general classes of functions,
with corresponding local differentiation of structure. We
recognize, accordingly, three zones on each side — a dorsal receptive
or sensory zone; a ventral emissive or motor zone; and, between
these and infiltrating them, an intermediate zone of correlation and
Figures 4 and 5 are sketches of longitudinal sections of the cerebrum
of adult Amblystoma tigrinum to illustrate the areas included
in the motor and sensory zones as here arbitrarily defined. The zones
of the medulla oblongata as seen in transverse section are shown in
figure 9. The sensory zone includes those parts of the brain which
receive afferent fibers from the periphery, together with more or less
closely related tissue of correlation. The motor zone includes those
parts from which efferent fibers go out to the periphery, together
with related apparatus of motor co-ordination. Both these zones
contain some areas which, though not directly connected with the
periphery, are nevertheless primarily concerned with specific types
of sensory or motor adjustment. What is left over is assigned to the
intermediate zone, and whether a particular area will be included
here depends on one's estimate of its preponderant physiological
character. The body of the cerebellum and the pallial part of the
cerebral hemispheres are excluded from the zones as supra-segmental
The lines drawn in this analysis are frankly arbitrary, chosen primarily
for convenience of description; but, as will appear, this functional
analysis contributes to an understanding of the meaning of the
structure, and, moreover, it has morphological justification as well.
These zones are not autonomous units when viewed either structurally
or physiologically. Their interconnections are intimate and
complicated. The more important of these connections are shown in
[Begin Page: Page 58]
a number of diagrams, some in this contribution and some in previous
This analysis of the more obvious structural features of an amphibian
brain in terms of physiological criteria is an artificial schematization
of a complicated fabric, the several parts of which are so
intimately connected that there is an over-all integration of their
activities. The main highways of through traffic have been mapped,
with signboards pointing the way at the crossroads. Selected examples
of some of the lines of fore-and-aft through traffic are illustrated
in the diagrams ; but this kind of analysis does not take us to
our destination. It does not tell us how mixed traffic is actually
sorted out and so reorganized as to give the body as a whole efficient
adjustment to the momentarily changing exigencies of common experience.
These problems are discussed in subsequent chapters, but,
first, the schematic outline will be summarized here.
Each zone is structurally diversified, and many of these local differentiations
are directly correlated on the sensory side with the
modalities of sense represented in the end-organs with which they
are connected and on the motor side in a similar way with synergic
systems of muscles. Each sensory and motor system of nerves has a
local primary central station in direct connection with the periphery,
and each of these stations has widely spread connections within its
own zone and with other zones, thus insuring efficient correlation of
sensory data, co-ordination of motor responses, and integration of
the action system as a whole. In this summary the sensory systems
are given special attention because these are the most useful guides
in the analysis of the structure of this brain.
The sensory zone is defined as those parts of the brain that receive
fibers from peripheral organs of sense. In some fields the number of
such fibers is large, in others it is very small; and some parts of the
brain, like the cerebral peduncle, have both sensory and motor
peripheral connections. Within the sensory zone there is a complicated
apparatus of correlation, and in lower vertebrates the receptive
areas and surrounding tissues dominated by them are so large that
most of the mass of the brain can be blocked into fields appropriately
designated "nosebrain," "eyebrain," and so on ('31a, p. 129). This
feature is due to the fact that in these animals the sense organs are
well developed and highly specialized, but the motor apparatus is
[Begin Page: Page 59]
more simply organized, chiefly for co-ordinated mass movements.
The sensory zone with its own apparatus of correlation, accordingly,
bulks larger than the motor zone.
Though the peripheral sensory apparatus in Amblystoma differs
from the human in many details, yet the general principles of its
organization are similar; the structural organization of the central
apparatus of adjustment, on the contrary, is so radically different
that comparisons are difficult. Here the several functional systems of
peripheral nerve fibers enter the brain in fascicles of the nerve roots,
which are physiologically as specific as are those of mammals ; but at
the first synapse this specificity may almost completely disappear, in
so far as it has visible structural expression. The root fibers of all
sensory systems (except, perhaps, the olfactory) terminate by wide
arborizations in a few common fields of neuropil, in each of which
several of these systems are inextricably mingled. This neuropil is a
common synaptic pool for all entering systems. The several pools are
interconnected with one another and with similar pools in other
parts of the brain stem, and there is no supreme cortical regulator.
The translation of sensory experience into adaptive behavior and the
integration of this behavior are somehow accomplished within this
interplay of the local activities of the brain stem.
The sensory zone is continuous from the dorsal gray colunm of the
spinal cord to the olfactory field, comprising the dorsolateral part of
the medulla oblongata, the auricle in the cerebellar region, the anterior
medullary velum and a small amount of contiguous tissue, the
tectum of the midbrain, pretectal nucleus, dorsal thalamus, olfactory
bulb with the adjoining anterior olfactory nucleus, and optionally the
septum and some other parts of the hemisphere, a portion of the
hypothalamus, and the ventrolateral neuropil of the peduncle. The
fields optionally included receive terminals of the nervus terminalis
(p. 267); the hypothalamus has a small but significant connection
with the optic nerve, the basal root of which also connects with the
peduncle. In some vertebrates the epithalamus receives fibers from
the parietal eye, but in Amblystoma these have not been seen, and in
this animal the predominant functions of the "optional" areas are of
intermediate-zone type. The body of the cerebellum and the pallial
part of the cerebral hemisphere might be assigned to the sensory zone
as here defined anatomically; yet, as previously mentioned, they are
excluded from this zone because of their distinctive physiological
characteristics and their remarkable specialization in higher animals.
[Begin Page: Page 60]
In the sensory zone of the medulla oblongata there are two elongated
synaptic pools of neuropil, into which terminals of the sensory
root fibers converge (chap. xi). One of these receives terminals of all
somatic sensory systems; the other lies more ventrally and internally
in the visceral lobe and receives terminals of the visceral sensory and
gustatory systems (figs. 9, 89). The secondary fibers which emerge
from these pools are distributed locally to the motor zone of the
medulla oblongata, downward to the spinal cord, and upward to
higher levels. The last take different courses, some to the cerebellum,
some to the tectum and thalamus, and some to the hypothalamus.
Each of these pathways discharges into a higher synaptic pool of
neuropil, where its terminals are in physiological relation with terminals
of other related sensory systems. The relations to which reference
has just been made are in terms of the types of response to be
evoked. Thus the tectum becomes the dominant regulator of somatic
adjustments to exteroceptive stimulation, the hypothalamus becomes
the regulator of visceral responses to olfacto-visceral stimulation,
and the cerebellum provides regulatory control of the action of
the skeletal muscles. The dorsal thalamus is ancillary to the tectum
and shows a very early stage in the evolution of the ascending sensory
projection systems to the cerebral hemispheres.
These local differentiations, each with characteristic structure and
connections, are receptive fields for the several systems of peripheral
sensory fibers, though some of them receive few peripheral fibers and
are concerned chiefly with sensory correlation.
The motor zone as here defined includes the peripheral motor
neurons and those areas of the brain stem concerned with the organization
of motor impulses in patterns of synergic action. It includes
the following histologically different parts: (1) corpus striatum
(paleostriatum); (2) anterior part of the ventral thalamus; (3) posterior
part of the ventral thalamus; (4) nucleus of the tuberculum
posterius ("peduncle" in the restricted sense); (3) isthmic tegmentum;
(6) trigeminal tegmentum; (7) a poorly defined tegmental field
extending farther posteriorly through the length of the medulla
oblongata into continuity with the ventral gray column of the spinal
The floor plate of the embryonic neural tube probably ends anteriorly
at the fovea isthmi (fig. 2B, f.i.), and the adjacent basal
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plate, which is the primordial motor zone, extends forward of this to
include the whole of the peduncle and probably more or less of the
hypothalamus and ventral thalamus. This primordial zone contains
not only nervous elements with peripheral connections, like the
sensory zone, but also an elaborate apparatus of central co-ordination
of the neuromotor systems.
Anteriorly of the peduncle the motor zone has no peripheral connections,
but the apparatus of motor co-ordination extends forward
through the thalamus into the lateral wall of the hemisphere. Since
the present analysis is based primarily on physiological criteria, this
anterior extension of the motor field is included in the motor zone.
The anterior boundaries of this zone are, of course, arbitrarily drawn ;
that they are artificial is emphasized by the fact that the large basal
optic root terminates in the peduncle, which is in the motor zone as
here defined. Efferent fibers have been described as leaving the brain
in many places outside the motor zone, even as here broadly defined.
Vasomotor and other visceral efferent fibers have been reported in
various animals associated with the nervus terminalis and the olfactory
and optic nerves and in other places for distribution to meninges
and chorioid plexuses. We have nothing new to report about Amblystoma
in this connection.
In the spinal cord and medulla oblongata the peripheral motor
neurons are so mingled with the co-ordinating neurons of the tegmentum
and reticular formation and they are so similar in form that it is
often impossible to distinguish the peripheral neurons except in cases
where their axons are seen to enter the nerve roots. The cells of the
nuclei of the eye-muscle nerves are fairly clearly segregated, and in
some reduced silver preparations they react specifically to the chemical
treatment (fig, 104); but even here their dendrites are widely
spread and intertwined with those of tegmental cells, so that both
kinds of neurons would appear to be similarly activated by the
neuropil within which they are imbedded. The cell bodies are locally
segregated; but their dendrites, where most of the synaptic contacts
are made, are not segregated.
In the medulla oblongata the motor tegmentum contains small and
large cells in an endless variety of forms, but these elements are not
segregated in accordance with either size or morphological type. It
is true that the arrangement of their cell bodies may show some
rather ill-defined local segregation, but their dendrites and axons are
so intimately intertwined in the neuropil that nothing comparable
[Begin Page: Page 62]
with the localized nuclei of higher brains can be recognized. Farther
forward in the isthmus and peduncle the tegmental tissue of coordination
is much increased in amount and somewhat more differentiated.
In some of my former papers (e.g., '30, p. 76) the term
"nucleus motorius tegmenti" was used loosely (and inaccurately)
to include a tegmental zone defined topographically. This seemed to
be justified in the case of Necturus by the lack of localization of the
large motor elements which characterize this region; but this justification
is inadequate, both factually and morphologically — see the
discussion by Ariens Kappers, Huber, and Crosby ('36, pp. 653, 666).
It is obvious that most of the tissue of the motor zone is concerned
with co-ordination of the action of the peripheral elements, so that
synergic groups of muscles are activated in appropriate sequence;
but, with the technic available, it has not been possible to analyze
this complex so as to reveal the mechanism employed. In the medulla
oblongata this organization is chiefly for local control of bulbar and
spinal reflexes, the intermediate zone participating. In the isthmus
and peduncle the number of peripheral elements is relatively small
and the co-ordinating apparatus larger, giving these areas control
over all motor fields spinal ward of them. This intrinsic motor apparatus
is supplemented by a segregated band of correlating tissue in
the intermediate zone, the subtectal dorsal tegmentum. In mammals
both these zones are further specialized into separate nuclei distributed
in the tegmentum.
The primary patterns of somatic movements are predetermined by
the course of central differentiation within the motor and intermediate
zones in premotile stages of development. After connection
with the peripheral musculature is established, each of these muscles
seems to exert some sort of distinctive reciprocal influence upon that
motor field of the central nervous system from which its innervation
is derived. The nature of this influence is unknown, but its reality is
well attested by experiments of Paul Weiss ('36, '41) and colleagues
upon "myotypic response" and "modulation."
In later stages the primary motor patterns may be modified, or
"inflected," by sensory experience and practice. Influence of use or
some other functional factors seem to be essential for maintenance of
motor efficiency, as graphically shown by Detwiler's observations
('45, p. 115; '46) on the behavior of decerebrate larvae of Amblystoma
(to which further reference is made on p. 118). In young
larvae of stage 37, swimming movements may be perfectly executed
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after transection immediately below the auditory vesicle under control
of the lower medulla oblongata and spinal cord (Coghill, '26,
Paper VI, p. Ill; '29, p. 15); but, subsequent to Harrison's stage 40,
Detwiler finds that sustained motor activities, including swimming,
fail rapidly if the influence of the midbrain is blocked in prefunctional
stages, though feeding reactions are preserved after complete
ablation of hemispheres and visual organs. The midbrain evidently
supplies a factor essential for maintenance of motor efficiency.
The motor field of this brain is smaller and more simply organized
than the sensory field because most of the activities are mass movements
of total-pattern type. Within this larger frame of total behavior,
the partial patterns of local reflexes are individuated with
more or less capacity for autonomous action. The number of these
local partial patterns is smaller than in higher animals, and all of
them are far more closelj^ bound to the total patterns of which they
are parts. The segments of each limb, for instance, may, upon appropriate
stimulation, move independently; but in ordinary locomotion
they move in a sequence related to the action of the entire limb,
the other limbs, and the musculature of the trunk.
The peripheral motor nerves (omitting the general visceral components
of preganglionic type not here considered) are in three
groups: (1) the spinal nerves; (2) the eye-muscle nerves. III, IV, and
VI pairs of cranial nerves, which are somatic motor; and (3) the
special visceral motor nerves of the V, VII, IX, and X pairs, innervating
the striated musculature of the visceral skeleton of the
head. The primary movements of trunk and limbs are organized for
locomotion in the motor zone of the spinal cord. This organization is
under exteroceptive and proprioceptive control locally throughout the
length of the cord and more especial!}^ at the bulbo-spinal junction;
it is under additional proprioceptive control from the labyrinth and
the cerebellum; there is further control from the cerebrum — optic,
olfactory, and the related apparatus of higher correlation. The bulbar
group of special visceral motor nerves is primarily concerned with
movements of the head, notably those of respiration and feeding.
The feeding reactions are under visual, olfactory, somesthetic, gustatory,
and general visceral afferent control, and the pattern of performance
seems to be organized in the large isthmic tegmentum.
The very large and complicated interpeduncular nucleus is an isthmic
structure which is physiologically of intermediate-zone type (chap.
xiv) . Details of the structure and connections of the various parts of
[Begin Page: Page 64]
the motor zone are in Part II, and the pecuhar features of its forward
extension in the cerebral hemisphere are discussed in chapter vii.
The characteristics of this zone are imphcit in the preceding account
of the sensory and motor zones. It is more elaborately developed
and its boundaries are more clearly defined in parts of the
cerebrum than in the rhombencephalon. These boundaries are necessarily
arbitrary, for all parts of the brain are involved in correlation
and integration of bodily activities ; but throughout the length of the
spinal cord and brain there is a band of tissue between the sensory
and motor zones primarily concerned with these adjustments. At
lower levels I have termed this tissue the "reticular formation," and
here it infiltrates the other zones with no clear boundaries (for details
see chap. xi). At higher levels it increases in amount and is more
clearly segregated. It would be appropriate to include in this zone
most of the diencephalon and telencephalon except the specific optic
and olfactory terminals ; but, for reasons mentioned above, a different
subdivision has been adopted, primarily for convenience of description.
The dorsal tegmentum, or subtectal area, is a typical representative
of this zone in position and physiological connections. In the
isthmic and bulbar tegmentum the characteristics of the intermediate
and motor zones are inextricably mingled. The habenula, hypothalamus,
and interpeduncular nucleus, as elsewhere described,
clearly belong physiologically to the intermediate zone; and the
whole cerebral hemisphere, except the olfactory bulb, might appropriately
be so classified in all Ichthyopsida.
In the most primitive vertebrates the intermediate zone is scarcely
recognizable as an anatomical entity. As the action system becomes
more complicated in higher animals, this zone shows corresponding
differentiation. This specialization is more directly dependent upon
complication of the peripheral motor apparatus than upon sensory
differentiation, for, so long as the action system is largely confined to
mass movements, the patterning of these total activities is effected in
the sensory and motor zones. In tetrapods and birds more complex
central adjustors are required, and these are differentiated between
the two primary zones and anteriorly of them. With the appearance
of more autonomy of the local reflex systems, more efficient apparatus
of integration is demanded. The final result is that in the human
brain the apparatus of intermediate-zone type has increased so much
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that it comprises more than half the total weight of the brain, for
both cerebral and cerebellar cortices are derivatives of this primordial
matrix, as will appear in the ensuing discussions.
The preceding physiological analysis of the brain obviously rests
upon the peripheral relations of its several parts. The two primary
functions of the nervous system are, first, the maintenance of the
integrity of the individual, with efficient co-operation of parts among
themselves and with the total organization, and, second, the analysis
of experience and the translation of the sensory data into appropriate
behavior. The peripheral nerves are key factors in both these domains.
Our knowledge of the functional analysis of the cranial nerves
has been greatly increased during the last fifty years, largely by the
work of the so-called American school of comparative neurologists,
which I have recently reviewed ('43).
Before I discuss the components of these nerves, a few definitions
are in order. In the attempt to envisage the nervous system from the
operational standpoint, distinctions have been drawn between sensory
correlation, motor co-ordination, and those central processes
that provide integration, and some measure of spontaneity of action
which might be grouped under the name "association" ('24c, p. 235;
'31a, p. 35). This classification is necessarily artificial, for all these
processes are interrelated. They interpenetrate, and they are not
sharply localized in the structural fabric. Nevertheless, these several
types of action are recognizable components of the unitary dynamic
system, and there are local differentiations of the structural organization
correlated with preponderance of one or another of them, more
clearly so in higher vertebrates than in lower.
Sensory correlation, as the term is here employed, refers to interaction
of afl^erent impulses within the sensory zone, that is, within the
field reached by terminals oi peripheral sensory fibers. The interplay
of these diverse afi'erent impulses takes two forms: (1) in fields of
undifferentiated neuropil, the activation of which results in alterations
of the central excitatory state or in mass movements of large
numbers of synergic muscles; (2) in more restricted areas (nuclei),
which activate the neuromotor apparatus of local reflexes. The members
of both groups are interconnected by systems of internuclear
fibers like the lemniscus systems, all within the sensory zone, so that
all activities of this zone interact one with another. These inter-
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nuncials are so arranged that functional systems of afferents, which
normally co-operate to effect a particular type of motor response, are
more intimately associated. Thus the tectum opticum receives most
of the lemniscus fibers of all somesthetic systems and minimum numbers
of olfactory and visceral systems. This basic pattern as seen in
Ambly stoma is changed in mammals, where higher associational centers
have taken over most of the functions of correlation.
Motor co-ordination is effected primarily in the motor zone, which
is so organized as to activate synergic groups of muscles in appropriate
sequence with inhibition of their antagonists. This grouping
may be adapted for mass movements or for local reflexes. Internuclear
tracts connect the various parts of the sensory zone directly
with appropriate parts of the motor zone. More refined analysis and
conditioning of motor responses are effected through the intermediate
zone, and the tissues of the latter group are greatly enlarged and
complicated in higher brains.
The activities of stimulus-response type which have just been considered
are so interconnected with internuclear tracts and the interstitial
neuropil as to facilitate the integration of all local activities in
the interest of the requirements of the body as a whole. Every local
part of the brain is a component of the apparatus of general integration,
and some of these parts have this association as their dominant
function. In Ambly stoma most of this suprasensory and supramotor
tissue is dispersed as interstitial neuropil. In mammals, higher types
of associational tissue have been differentiated locally, notably in the
cerebral cortex and its dependencies, with corresponding enhancement
of those synthetic functions which are manifested as conditioning,
educability, and reasoning. Parallel with these changes there is
an enormous increase in accumulated reserves of potential nervous
energy, which come to expression as spontaneity, memory, and creative
A survey of the nerve fibers of Amblystoma as a whole in view of
the principles just expressed shows that they may be classified in four
groups: (1) the peripheral afferent systems and associated internuclear
correlating tracts within the sensory zone (lemniscus systems,
etc.) ; (2) the peripheral efferent systems and the related coordinating
fibers of the motor zone; (3) the central internuclear systems
intercalated between the preceding two and so interconnected
as to yield appropriate responses to ordinary recurring stimuli; and
(4) infiltrating these mechanisms of stimulus-response type, a differ-
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ent sort of adjusting apparatus which insures general integration of
these systems, with provision for conditioning of reflexes and other
forms of individually acquired behavior and for release of accumulated
reserves of nervous potential as needed. These four groups
intergrade but, in general, are recognizable.
The peripheral fibers are grouped in functional systems, each of
which is defined as comprising all nerve fibers and related endorgans,
which are so arranged as to respond to excitation in a common
mode, either sensory or motor. These functional systems are
convenient anatomical units also, for all fibers of each sensory system,
regardless of variations in the peripheral distribution of their
end-organs and regardless of the particular nerve trunks or roots
through which they connect with the brain, are segregated internally
and converge into local areas or zones. In higher vertebrates (but less
so in lower) the secondary connections of these terminal stations tend
to retain their physiological specificity. From this it follows that the
peripheral systems of sensory analyzers are extended into the brain
as far as related central pathways are separately localized — in the
human brain it may be even up to the projection areas of the cerebral
cortex. Accordingly, we include in the sensory zone as here defined
not only the terminal nuclei of peripheral sensory nerves but also
their related nervous connections, so far as these are with other parts
of the sensory zone and not directly with the motor zone. The neuromotor
apparatus can be similarly analyzed into functional systems,
each of which is concerned with the synergic activation of some
particular group of muscles.
This anatomical segregation of the functional systems is not carried
to perfection, even in the human nervous system. The various
modalities of cutaneous and deep sensibility, for instance, are not
completely segregated and localized either peripherally or centrally.
Yet this differentiation has gone so far that it provides our most useful
guide in the analysis of the structure of the brain.
The activities of the body may be divided into two major groups;
(1) those concerned with adjustment to environment, the somatic
functions, and (2) those concerned with the maintenance and reproduction
of the body itself, visceral functions. These, of course, are not
independent of each other; nutrition, for instance, involves somatic
activity in the search and capture of food and visceral activity in its
digestion and assimilation. Nonetheless, these types of function are
so different, especially in the responses evoked, that this strictly
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physiological criterion marks also the most fundamental structural
analysis of the nervous system. Anatomically, the somatic systems
of peripheral organs and nerves and central adjustors, including the
proprioceptors, are, in general, rather sharply distinguished from the
visceral. The systems are cross-connected by internuclear tracts, and
some sensory systems, like the olfactory, may serve, on occasion,
either somatic or visceral adjustments.
A phylogenetic survey of these systems reveals remarkable plasticity
in their interrelationships. Thus, taste buds, which in most vertebrates
are typical interoceptors, may in some fishes be spread over
the external surface of the body, where they serve exteroceptive functions,
with corresponding changes in the anatomical pattern of the
central apparatus of adjustment (chap, x; '446). On the motor side
the apparatus of feeding and respiration exhibits still more remarkable
transformations. In fishes this musculature is connected with the
visceral skeleton — jaws, hyoid, and gill arches — and the functions
performed are obviously visceral, though the larger part of this
musculature is striated. The related parts of the nervous system are
classified as special visceral motor. With suppression of the gills in
higher animals, some of these muscles undergo remarkable transformations.
Those which are elaborated to form the mimetic facial
musculature of mammals become physiologically somatic ('22, '43).
The classification of peripheral end-organs and their related nerves
which has proved most useful grew out of the analysis of these nerves
into their functional components, to which reference has just been
made, by histological methods. Serial sections through the entire
bodies of small vertebrates differentially stained for nerve fibers
enable the investigator to reconstruct not only the courses of the
nerves but also the arrangement of the functional systems represented
in each of them and to follow these components to their
peripheral and central terminals, a result that cannot be achieved by
ever so skilful dissection. The first successful application of this
method was Strong's analysis of the nerve components of the tadpole
of the frog in 1895, a fundamental research which provided the generalized
pattern which prevails, with endless modifications of details,
throughout the vertebrate series, as has been abundantly demonstrated
by numerous subsequent studies by many workers.
This was followed in 1899 by my Doctor's dissertation on the nerve
components of the highly specialized teleost, Menidia. From these
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and subsequent studies the peripheral nervous system of the head
was analyzed into functional systems as follows:
1. Somatic sensory fibers of two groups. — (1) Exteroceptive systems,
including (a) the specialized olfactory (in part), optic, auditory,
and lateral-line nerves with differentiated end-organs, and (6)
the nerves of general cutaneous and deep sensibility with simple free
endings, these entering chiefly in the V nerve root with some in the
VII, IX, and X roots. (2) Proprioceptive fibers from specialized endorgans
of the internal ear and (probabljO lateral-line organs and also
fibers from muscles, tendons, and other deep tissues. Here belongs
also the peculiar mesencephalic root of the V nerve. See chapter x for
further comments on the proprioceptive system.
2. Visceral sensory fibers of two types. — (1) With specialized endorgans,
viz., the olfactory organ (in part) and the taste buds, the
latter entering by the VII, IX, and X nerve roots. (2) Fibers of general
visceral sensibility with free endings, entering in the same roots
as the preceding and mingled with them.
3. Somatic motor fibers. — Somatic motor fibers which supply striated
muscles derived from the embryonic somites, those in Amblystoma
being limited to the nerves of the extrinsic muscles of the eyeball
in the III, IV, and VI nerves.
4. Visceral efferent fibers of two types. — (1) Special visceral motor
fibers of cranial nerves supplying striated muscles, not of somitic
origin, related with the visceral skeleton, jaws, hyoid, branchial
arches, and their drivatives (in the V, VII, IX, and X roots).
(2) Preganglionic fibers of the general visceral (autonomic) system,
terminating in sympathetic and parasympathetic ganglia, where they
activate postganglionic fibers distributed to unstriated and cardiac
muscles and glands (in the III, VII, IX, and X roots). The last system
is not further considered in this work. For application of this
analysis to the human nervous system see my Introduction to Neurology
('31a, chaps, v and ix).
This analysis has yielded our most useful clues for resolution of the
complexity of both peripheral nerves and brain. Descriptions of the
peripheral end-organs and the courses of the nerves do not lie within
the scope of this work. Some of these details which are significant for
understanding their central connections are included in chapter x.
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IN A primitive brain like that of Amblystoma the stable framework
of localized centers and tracts performs functions that are primarily
analytic. The sense organs are analyzers, each attuned to
respond to some particular kind of energy. The sensory systems of
peripheral nerves and the related internal sensory tracts are parts
of the analytic apparatus, in so far as their functional continuity
with the peripheral organs of the several modalities of sense can be
On the motor side similar conditions prevail. The neuromotor
apparatus is organized in functional systems, each of which is
adapted to call forth the appropriate sequence of action in a particular
group of synergic muscles. These units are as truly analyzers
as are those of the sensory systems, though in an inverse sense. Out
of the total repertoire of possible movements, those, and only those,
are selected which give the appropriate action. The efferent fibers are
grouped, the members of each group being so bound together by
central internuclear connections that they act as a functional unit
adapted for the execution of some particular component of behavior,
such as locomotion, conjugate movements of the eyeballs, seizing and
swallowing food, and so on.
The several sensory systems are so interconnected within the sensory
zone as to react mutually with one another. They form a
dynamic system so organized that all discharges from this zone are
resultants of this interaction. This interplay has pattern. The various
modalities of sense are not discharged into a single common pool of
equipotential tissue. The sensory components of the nerves are segregated,
more or less completely, so that related systems converge into
dominant centers of adjustment— exteroceptors in the tectum, proprioceptors
in the cerebellum, olfacto-visceral systems in the hypothalamus,
olfacto-somatic systems in the habenula, and so on.
A review of the internal architecture of the adult brain of Amblystoma
suggests that the specifications of the general plan are drawn
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in terms of current action. The elaboration of the analytic apparatus
on the sensory side is carried only so far as is requisite to facilitate
responses to any combination of sensory stimuli in patterns determined
by the appropriate use of such motor equipment as the animal
possesses. In species with simpler action systems the central analytic
apparatus is less elaborate; in species endowed with more complicated
motor organs the central architecture is more elaborate. In all
species the peripheral sensory equipment determines the architectural
plan of the primary centers of the sensory zone; internally of
this level the details of the plan are shaped by two additional factors :
first, the motor equipment available and, second, the amount and
quality of the apparatus of correlation and integration required for
the most efficient use of such sensory excitations as the animal experiences.
The cross-connections between the sensory and motor
zones are quite direct and simple in early embryological stages, so
arranged as to provide uniform stereotyped responses to oft recurring
situations. But as development advances these connections become
more and more complicated, an intermediate apparatus of correlation
is interpolated, and, correlated with this, the behavior becomes more
diversified and unpredictable.
In the sequence of development of behavior patterns this change
can be accurately dated. For instance, in Amblystoma between the
early swimming and early feeding stages, at about Harrison's stage
40, the swimming movements, which in younger stages are perfectly
co-ordinated by the bulbo-spinal central apparatus alone, lose this
autonomy, and participation of the midbrain is essential for the
maintenance of efficient swimming, as was mentioned on page 62 in
describing experiments by Detwiler ('45, '46). It is during this period
that tecto-bulbar and tecto-spinal connections of essentially adult
pattern are established ('39, p. 112). In human fetal development
there is a similar critical period at about 14 weeks of menstrual age
(Hooker, '44, p. 29). At this time the upper levels of the cerebrum
acquire functional connections with the lower brain stem, and the
behavior shows a corresponding change. "The fetus is no longer
marionette-like or mechanical in the character of its movements,
which are now graceful and fluid, as they are in the new-born."
Synthesis and integration may be effected in various ways. The
most evident nervous structures employed here are the internuclear
tracts which form a complicated web of conductors, which interconnect
the analytic units with one another so that the entire com-
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plex forms an integrated equilibrated system. This is the apparatus
of the stable heritable components of the action system — the reflexes
and instincts. A second integrating apparatus is found in the allpervasive
neuropil, and a third in specialized derivatives of the latter,
the associational tissues locally differentiated in the brain stem and
reaching maximal development in the cerebral cortex.
The total behavior of neuromuscular type emerged within a preexisting
bodily organization, which maintained the unity of the individual
by nonnervous apparatus. The nervous system is from its first
appearance a totalizing apparatus. Local differentiations of tissue
for the analysis of sensory experience and of motor responses arise
within this integrated structure, and local reflexes similarly emerged
within a total neuromuscular pattern of action adapted to maintain
the unity of the organization. As development advanced, the mechanisms
of the local reflexes acquired increasing autonomy, but they
are never completely emancipated from some control in the interest
of the behavior of the body as a whole. The organic unity of the
whole is preserved while local specificity is in process of development,
and this unitary control is never lost during the normal life of the
The stimulus-response formula has wide application and great
usefulness as a basic concept in physiology and psychology, but its
apparent simplicity is illusory and has tended to divert attention
from essential features of even the simplest patterns of behavior.
This I have illustrated ('44a) by an examination of the simplest reflex
connection known in Amblystoma — from retina to ocular muscles by
way of the basal optic tract.
The late G. E. Coghill, during a productive period of foi'ty years,
studied the development of the action system of Amblystoma and
the correlated processes of bodily growth. These researches have
demonstrated beyond question that in this animal the neuromuscular
system is so organized in prefunctional stages that, when first activated
from the sensory zone, the resulting movement is a total response
of all the musculature that is mature enough to respond to
nervous excitation. These "total patterns" of activity are not disorderly,
and they become progressively more complicated while the
apparatus of local reflexes ("partial patterns") is slowly differentiated
within the larger frame of the total pattern. The development
of both the total pattern and the partial patterns is initiated cen-
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trally, and throughout Hfe all of them are under some measure of unified
central control so that the body acts as an integrated whole with
diverse specialization of its parts (Coghill, '29; Herrick, '29). Coghill's
contributions of factual observations and the principles derived
from them have been critically reviewed by the writer in a book
('48), to which the reader is referred.
The patterning of these orderly movements is determined by the
intrinsic structure of the nervous system. This structural pattern is
not built up during early development under the influence of sensory
excitations, for in the embryo the motor and sensory systems attain
functional capacity independently of each other; and when central
connection between the sensory zone and the motor zone is made, the
first motor responses to excitation exhibit an orderly sequence, the
pattern of which is predetermined by the inherited organization then
matured (Coghill '29, p. 87; '30, Paper IX, p. 345; '31, Paper X,
pp. 158, 166). This early structural differentiation goes on independently
of any stimulus-response type of activity, though the
latter may modify the pattern of subsequent development. This is a
principle of wide import, applicable not only in lower vertebrates but
in higher forms as well (Coghill, '40), including man (Hooker, '44).
The stimulus-response mechanism is not a primary factor in embryogenesis;
it is a secondary acquisition.
It has been pointed out that the functions of the sensory and
motor zones are fundamentally analytic — analysis of environmental
influences and analysis of performance in adjustment to those influences.
How the units of the analytic apparatus are actually related so
as to insure the appropriate correlated action of the separate parts is
the key problem, which must be resolved before animal (and human)
behavior can be approached scientifically in other than a descriptive
way. Good progress has been registered. The sensory and motor
analytic apparatus has been exhaustively studied and well described;
and this was the appropriate place to begin, for these organs are most
accessible to observation and experiment. Because these systems of
peripheral end-organs and the related pathways of conduction and
centers of control are, in the human nervous system, obviously interconnected
in stable and definitely localized patterns, it was natural
to use this structural framework as the point of departure in the
elaboration of the hypothetical superstructure of current doctrines of
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reflexology. But reflexes can be conditioned, and this name for a
well-known physiological fact is for the neurologist scarcely more
than a symbol of complete ignorance of the mechanisms actually
The several reflexes have been so closely colligated with specific
details of central architecture that the reflex arc came to be regarded
as the primary unit of nervous organization, and it was assumed that
the increasing complexity of the upper levels of the brain in higher
vertebrates has been brought about by progressively more intricate
interconnections among these elementary units. The integrative action
of the nervous system was conceived in terms of the definition of
mathematical integration — "the making up or composition of a
whole by adding together or combining the separate parts or elements."
This conception leaves unexplained how any additive process
of this sort can result in such a unique centrally controlled unitary
organization as we actually observe, capable of conditioning the
reflexes in terms of individual experience (learning), of abstracting
some common features of mixed experience and synthesizing these
into quite original patterns of response, and of maintaining some
measure of "spontaneous" or self-determined directive control.
A far more serious charge against traditional doctrines of reflexology
is the observed fact that in the development of Ambly stoma
the early responses to external stimulation are not local reflexes but
total movements of the entire available musculature. The integrated
total pattern precedes in time the appearance of the partial patterns.
These are individuated within the total pattern; they are integral
parts of it, and for an appreciable time they are subordinate to it.
Even in the adult animal the local partial patterns are not completely
emancipated from control by the body as a whole. It is, indeed, impossible
to find in this brain any sharply defined, well-insulated reflex
What happens during the emergence of specific reflexes from the
total reactions is, first, the development of an increasing number of
collateral branches of the primary axons and the central linkage of
sensory and motor pathways in ever more complicated patterns.
Then, second, in the adjusting centers additional neurons are differentiated,
the axons of which take longer or shorter courses, branching
freely and participating in the formation of a nervous feltwork of
extraordinary complexity. These neurons are not concerned primarily
with specific reflexes but with the co-ordination and Integra[
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tion of all movements. Some parts of this intricate fabric, generally
witli thicker fibers, more or less well fasciculated, activate mass
movements of primitive type, and other parts control local reflexes
as these are individuated. But these systems of fibers are not segregated
in comjjletely insulated reflex arcs. They are interconnected by
collateral branches with one another and with the interstitial neuropil.
There are lines of preferential discharge, but whether any one
of them is actually fired depends on numberless factors of peripheral
stimulation and central excitatory state.
The phylogenetic history is parallel. The further down we go toward
the primitive ancestral vertebrates, the less clear evidence do
we find of definitely localized reflex arcs, and the overt behavior
tends more toward mass movements of total-pattern type.
It must be borne in mind that the development of the individual
does not exactly recapitulate the phylogenetic development (Hooker,
'44, pp. 15, 33). The pattern of the sequence of structural changes'
which take place during prefunctional stages of growth is determined
by the organization of the germ plasm and the interaction of the
genetic factors with one another. This organization, in turn, has been
determined during preceding evolutionary history in adaptation to
the environment and habitus of the species in question. In broad
lines the history of ancestral development is repeated in the growth
of the embryo, but cenogenetic modifications of it may appear in
adaptation to changing conditions, as illustrated, for instance, by the
appearance of some local reflexes earlier in mammals than in amphibians.
The structural organization of the brain sets off in sharp relief a
few important general physiological principles. First, it is to be noted
that the "resting" nervous system is not inert. The body acts before
it reacts. There is always some spontaneous — that is, centrally excited
— activity, and the importance of this factor increases as we
ascend the phylogenetic scale. There is always intrinsic activity, as
demonstrated, for instance, by the Berger rhythms, and it is always
acted upon by numberless extrinsic agencies. When an excitation is
received from the periphery, there results a change in the central
excitatory state both locally and diffusely, which involves both activation
and inhibition.
Another general principle may be mentioned here. The flow of
nervous impulses from receptor to effector is not one-way traflSc.
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The excitation of a peripheral sense organ may be followed by an
efferent discharge back to the receptor. An instructive illustration of
this is seen in the auditory apparatus of mammals. Excitation of the
cochlea is followed by an efferent return to the tensor tympani and
stapedius muscles and also to the cochlea itself (the latter pathway
recently demonstrated by Rasmussen, '46). Almost all contracting
muscles report back to the center by a system of proprioceptive
fibers. The central nervous system is full of similar reciprocating systems.
Many of the fasciculated tracts of Ambly stoma are two-way
conductors, transmitting in both directions, and there are numberless
illustrations of a circular type of connection, efferent fibers of one
center activating another, which has a return path, perhaps by a
devious route, back to the first center. A neuropil may be interpolated
in any of these types of circuit. The thalamo-cortical connections
of the human brain are of this sort, exhibiting what Campion
and Elliot Smith ('34) have aptly named a "thalamo-cortical circulation,"
a circulation not of blood but of nervous transmission. All
parts of the cerebral hemispheres are in similar reciprocal interconnection,
as has recently been emphasized and illustrated by Papez
Here reference may be made to Dewey's ('96) stimulating analysis
of the reflex-arc concept or, as he prefers to say, the "organic circuit"
concept. This he elaborated in terms of psychology, and nearly
twenty years later I made this comment about it ('13«) :
"Let us see how it may be applied to biological behavior. The simple reflex is
commonly regarded as a causal sequence: given the gun (a physiologically adaptive
structure), load the gun (the constructive metabolic process), aim, pull the trigger
(application of the stimulus), discharge the projectile (physiological response), hit
the mark (satisfaction of the organic need). All of the factors may be related as
members of a simple mechanical causal sequence except the aim. For this in our
illustration a glance backward is necessary. An adaptive simple reflex is adaptive
because of a pre-established series of functional sequences which have been biologically
determined by natural selection or some other evolutionary process. This gives
the reaction a definite aim or objective purpose. In short, the aim, like the gun, is
provided by biological evolution and the whole process is implicit in the structurefunction
organization which is characteristic of the species and whose nature and
origin we need not here further inquire into The aim (biological purpose) is
so inwrought into the course of the process that it cannot be dissociated. Each step
is an integral part of a unitary adaptive process to serve a definite biological end, and
the animal's motor acts are not satisfying to him unless they follow this predetermined
sequence, though he himself may have no clear idea of the aim. These reactions
are typically organic circuits Always the process is not a simple sequence
of distinct elements, but rather a series of reactions, each of which is shaped
by the interactions of external stimuli and a preformed or innate structure which
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has been adapted by biological factors to modify the response to the stimuH in
accordance with a purpose, which from the standpoint of an outside observer is
teleological, i.e., adapted to conserve the welfare of the species."
This apparent teleology is commented upon in chapter viii. Since
the passage just quoted was written, control of gunfire by radar has
been perfected, thus reinforcing our analogy at one weak spot. In
the reflex the "aim" does not precede the stimulus that pulls the
trigger; it is automatically adjusted to the stimulus as in radar. But
this automatism in both cases is dependent upon the presence of a
preformed structure adapted to provide it.
Our analysis of the adult structure of the brain of Amblystoma
confirms and supplements the conclusions reached by Coghill from
his study of the development of the same species. His major contribution,
as I see it, was the demonstration of the primacy of the
integrative factors in the development of behavior patterns and of
some of the features of structural growth during the individuation of
local partial patterns within the larger total pattern. The adult
structure of the brain of Amblystoma is in perfect conformity with
the conclusions to which he was led. One of these conclusions should
receive special emphasis here, for it clarifies our conception of what
the reflex is in general, and in particular it helps us over some hard
places in our attempt to discover the actual mechanisms involved in
the individuation of local reflex patterns within the frame of the
total pattern.
In the central resolution of forces which eventuates in some particular
pattern of overt movement there is always an inhibitory factor
(Coghill, '36, '43). In discussing the individuation of partial patterns
(local reflexes) from the total pattern, he wrote ('40, p. 45):
"Individuation is obviously the result of organized inhibition
The major division of the total pattern must be under inhibition
when a part acquires independence of action, and the same part can
be inhibited while the major segment of the total pattern acts. So
that the whole individual probably acts in every response, either in
an excitatory or inhibitor}^ way," This he generalized in the following
statement ('30, p. 639):
"For an appreciable period before a particular receptor field acquires specificity
in relation to an appropriate local reflex its stimulation inhibits the total reaction.
Inhibition, accordingly, through stimulation of the exteroceptive field, begins as a
total pattern. It is then in a field of total inhibition that the local reflex emerges.
The reflex may, therefore, be regarded as a total behavior pattern which consists of
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two components, one overt or excitatory, the other covert or inhibitory. The essential
anatomical basis for this is (1) in the mechanism of the total pattern of action,
or primary motor system, and (2) in the mechanism of the local reflex, or secondary
motor system; the mechanism of the total pattern being inhibited and that of the
reflex excited. But since inhibition is not a static condition but a mode of action,
the mechanism of the total pattern must be regarded as participating in every local
This conception of the reflex as involving a factor of inhibition of
the total pattern Hnked with excitation of the partial pattern is
fruitful. Total inhibition plays a more obvious role in the overt behavior
of amphibians than in most other animals, not only in embryogenesis
of behavior but also in the adult. This was emphasized
by Whitman ('99) in his classic description of the behavior of Necturus.
In my manuscript notes of a conference with Dr. Coghill on
January 1, 1929, I find a record of his remarks which is here transcribed.
"The first neurons to differentiate in Amljlystoma are in the floor-plate. These
and others adjacent form the primary motor column, the dominant function of
which is activation of muscles of the same side for mass movement of the trunk and
limbs and inhibition of the musculature of the opposite side which is in the same
phase of locomotor movement. In later stages, when mechanisms of specific local
reflexes emerge, residual neurons in the region of the floorplate maintain their functional
importance for mass movements as activators of the whole somatic motor
apparatus. They may prime this neuromotor system, putting it into a subliminal
excitatory state in advance of its patterned activation.
"At an age which immediately precedes the first feeding reactions and before it is
possible to open the mouth and swallow, the larva will react to a moving object in
front of the eyes by a total reaction, a leap forward. It cannot seize the object. The
general activator mechanism here comes to overt expression before the specific local
reflex patterns are mature enough to function. After feeding activities have matured
there is a similar general activation, accompanied by inhibition, as illustrated by the
'regarding' reaction [p. 38]. A larva which had been feeding for several days was
stimulated by moving a hair slowly across the field of vision. The animal responded
by moving the head slowly following the hair. The head is bent to the side, with
rotation of the eyes, movement of the fore limbs, and adduction of both hind limbs.
When the hair was not too far distant, the animal finally, at the end of this 'regarding'
reaction, jumped after it. Here there is a clear distinction between what Sherrington
calls the anticipatory phase and the consummatory phase of the reaction,
and evidently in the anticipatory phase inhibition plays the major role. This is
obvious also in almost all adult behavior of these animals."
The mechanism of central inhibition is still obscure. There is some
evidence that a nervous impulse impinging upon a central neuron
may, on occasion, activate the element, or under other conditions of
central excitatory state, strength, or timing of the afferent flow it
may inhibit activity ui process. Whether or not this is true, it is well
known that a central neuron may exhibit a large variety of types of
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synaptic junctions, differing in histological structure, electrical properties,
and perhaps also in chemical reactivity. These afferent fibers
may come from widely separated regions with diverse functions, and
the impulses delivered may differ in intensity and temporal rhythm.
Bodian's description ('37, '4'2) of axon endings on Mauthner's cell
of the medulla oblongata shows four main types of synaptic contact
which vary from 0.5 to 7/i in extent, with a wide variety of arrangements.
There are between four and five hundred of these endings on a
single cell, and the presumption is legitimate that these diverse
structures are correlated with significant differences in electrical and
chemical properties, including the timing of the pulses of transmission.
It has been suggested that some of the influences transmitted
across the synaptic junctions are excitatory and that others are inhibitory.
Synaptic junctions on dendrites are in some cases structurally
different from those on the axon hillock or axon, and they
may be activated from different sources. Some observers believe that
excitation of dendrites is excitatory and of axons is inhibitory, a
supposition supported with physiological evidence by Gesell and
Hansen ('45, p. 156). In their theory of the electronic mechanism of
activation and inhibition, these functions are viewed as basically
similar, activation being associated with an increasing, and inhibition
with a decreasing, intensity of the electronic current. The connections
of horizontal cells of the retina as described by Polyak ('41, p.
385) suggest to him a different inhibitory apparatus. The horizontal
cells may exert an inhibitory influence upon the synapses between
the rods and cones and the bipolar cells, that is, the synapses of the
horizontal cells may function as "countersynapses" to the photoreceptor-
bipolar synapses.
Whatever may be the mechanism employed in central inhibition,
it is clear that in some parts of the brain excitatory functions predominate,
in other parts inhibitory functions. Noteworthy examples
of the latter are (1) the head of the caudate nucleus (Fulton, '43, p.
456) ; (2) a region in the reticular formation of the medulla oblongata
explored by Magoun ('44) ; and (3) certain specific zones of the cerebral
cortex (areas 4^, ^s, 19s, and some others) which are known as
"suppressor bands." In all these cases, excitatory and inhibitory
fields are intimately related physiologically in such a way as to secure
appropriate balance of activation and inhibition of the members of
synergic systems of muscles in proper sequence.
The role of general inhibition in the patterning of behavior has
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been under investigation for several years by Beritoff and his colleagues.
The first half of the fifth volume of the Transactions of his
institute is devoted to studies on the nature of general inhibition and
its role in the co-ordination of cortical activity and reflex reactions
of the spinal cord. Beritoff believes that the neuropil possesses an inhibitory
function — slow changes in voltage, expressing the active
state of the neuropil, show an anelectrotonic effect on the cellular
bodies, lowering excitability in them and weakening the excitation.
The evidence is drawn from both somatic and visceral stimulation.
He writes ('43, p. 142) : "Thus, during each reflex reaction in the
visceral organs, taking place in response to a stimulation of the interoceptors
and of visceral afferent fibers, just exactly as during
somatic reflexes, the spinal cord acts as a whole, making the given
reflex local and every spinal reflex reaction entire by means of general
inhibition." This is essentially the same as Coghill's position as stated
in the preceding quotations. In other articles in the same volume the
role of the neuropil in a great variety of spontaneous and stimulated
activities of the brain is emphasized by Beritoff.
The neuropil as a whole is not, in my view, a specific inhibitor. It
may partipciate on occasion in either excitation or inhibition, and in
the inhibitory phase it acts as part of the covert component of the
reflex or of mass action, as the case may be, in Coghill's analysis as
quoted above. In my discussion of the habenular system (chap, xviii)
and the interpeduncular nucleus (chap, xiv) I have ventured to suggest
a possible mechanism through which general inhibition effected
in the interpeduncular neuropil may operate in the facilitation of
both mass movement and local reflexes. On this hypothesis this local
band of neuropil must be able to act as a specific inhibitor in Beritoff's
The amphibian neuropil in its various forms . is structurally
adapted for a considerable variety of functions of different grades
of specialization. There is generally a diffuse spread of terminals, so
that a single incoming fiber may activate many neurons of the second
order. If the receptive tissue is homogeneous, this provides for simple
central summation. If the receptive tissue is heterogeneous, as in
most sensoiy fields, this arrangement facilitates mass movement of
the musculature or total patterns of action. If many fibers converge
upon a single neuron, the threshold of central excitation is lowered,
as in the mitral cells of the olfactory bulb and in the *'motor pool,"
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as this concept has been developed by Sherrington. If the activated
motor pool is large, with wide distribution of the efferent fibers, complicated
integrated mass movement may result. If the pool is small,
with a single final common path, a local reflex may follow. If the outlet
comprises a number of open channels with different connections
and physiological properties, there is provision for discriminative
response, the selection being made (presumably) in terms of the
central excitatory state of the components of the system ('42, p. 295).
It has been objected that the preceding comments on the limitations
of current doctrines of reflexology are based upon the amphibian
organization, which is aberrant and degenerate and therefore not
typical or significant in the interpretation of the behavior of higher
animals. But, even so, the Amphibia live well-ordered lives, and their
behavior conforms in basic patterns with that of other vertebrates.
We want to know how they behave as they do. Accepting the current
view that Amblystoma is a retrograde descendant of some more
highly specialized ancestor now extinct and that some of its characters
are aberrant, yet the evidence seems to me adequate that such
retrogression as may have occurred has been toward a generalized
form ancestral to modern amphibians and mammals.
Conclusion. — I have assembled in these pages some factual description
of observed structure, together with speculative interpretations
of its probable physiological significance. The organic structure
here under consideration is not something vague and ill-defined.
Its anatomical distribution, histological organization, and fibrous
connections can be described with precision. Not until this has been
done can our imperfect knowledge of its functions be advanced by
experiments designed to reveal its physiological properties.
In a discussion of "localized functions and integrating functions"
more than a decade ago ('34a), the significance of neuropil in the
evolution of cerebral structure was summarized in these words :
"The neuropil is the mother tissue from which liave been derived both the specialized
centers and tracts which execute the refined movements of the local reflexes
and the more general web which binds these local activities together and
integrates the behavior. It retains something of embryonic plasticity and so is available
as a source of raw material for two very dift'erent lines of specialization — first,
toward the structural heterogeneity requisite for the execution of localized reflex
and associational functions, and, second, toward the more generalized and dispersed
apparatus of total or organismic functions of tonicity, summation, reinforcement,
facilitation, inhibition, 'spontaneity,' constitutional disposition and temperament,
and extra-reflex activities in general."
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The gi-eat advances that have been made in the diagnosis and
treatment of nervous diseases have been due in large measure to the
more accurate mapping of the structural features of the nervous system
and recognition of the specific functions of its several parts.
Before a disorder can be successfully treated we must know what it
is and where it is. The most notable triumphs in this medical field
have been registered with those diseases whose situs can be recognized
and then subjected to appropriate therapy or surgery. Even a
systemic disorder like anemia has localization in blood corpuscles
and blood-forming organs; and a general infection, like poliomyelitis,
spreads in preferential paths determined by the histochemical structure
of the tissue. The stable heritable tissues of the nervous system
are most accessible to this kind of inquiry, of diagnosis, and of treatment;
conquest of the unlocalized disorders has been retarded.
Some kinds of disorder, particularly those of primary concern to
psychiatrists, have resisted all attempts at localization in accordance
with conventional principles, and in the field of physiology the concept
of local reflex arcs has limited application. The various attempts
to elaborate a comprehensive account of animal and human behavior
in terms of conventional reflexology have broken down. These conspicuous
failures have led some competent authorities to question
the over-all significance of localization in space of nervous functions
and to search for other principles in the realm of pure dynamics or
chemical interaction or some as yet unknown factors which operate
quite independently of stable structural patterns. But no nervous
tissue is structurally homogeneous or physiologically equipotential.
In this connection it is interesting to note that Lashley, the leading
advocate of the equipotentiality of the nervous tissues, has given us
clear demonstration of point-to-point projection of retinal loci upon
the lateral geniculate body and the cerebral cortex of the rat (Lashley,
'34, '34a). This is the most refined anatomical localization of function
known. In a later communication ('41) he demonstrated a very
precise projection of the thalamic nuclei upon the cerebral cortex and
added: "A functional interpretation of the spatial arrangement of
the thalamo-cortical connections is not justified on anatomic grounds
alone for any sensory system."
Somewhere between the extreme views of rigid localization in spatial
patterns and a labile physiological equipotentiality a practicable
working conception of the meaning of the structural configuration