Table Of ContentSTUDIES ON THE DEVELOPMENT OF
BEHAVIOR AND THE NERVOUS SYSTEM
Volume 3
NEURAL AND BEHAVIORAL
SPECIFICITY
Edited by
GILBERT GOTTLIEB
Psychology Laboratory
Division of Research
North Carolina Department of Mental Health
Raleigh, North Carolina
ACADEMIC PRESS · New York San Francisco London 1976
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LIST OF CONTRIBUTORS
Numbers in parentheses indicate the pages on which the authors' contributions begin.
KAO LIANG CHOW (155), Department of Neurology, Stanford University
School of Medicine, Stanford, California
J. D. DANIELS (195), Division of Biology, California Institute of Technology,
Pasadena, California
GILBERT GOTTLIEB (25, 237), Psychology Laboratory, Division of Research,
North Carolina Department of Mental Health, Raleigh, North Carolina
PAUL GROBSTEIN (155), Department of Pharmacological and Physiological
Sciences, University of Chicago, Chicago, Illinois
M. J. KEATING (59), Division of Developmental Biology, National Institute
for Medical Research, London, England
WILLIAM R. LIPPE (5), Psychology Laboratory, Division of Research,
North Carolina Department of Mental Health, Raleigh, North Carolina
RONALD L. MEYER (111), Division of Biology, California Institute of Tech
nology, Pasadena, California
J. D. PETTIGREW (195), Division of Biology, California Institute of Tech
nology, Pasadena, California
R. W. SPERRY(III), Division of Biology, California Institute of Technology,
Pasadena, California
RICHARD C. TEES (281), Department of Psychology, University of British
Columbia, Vancouver, British Columbia, Canada
ix
PREFACE
Historically speaking, a large measure of the progress in neurobiology and
biopsychology has come from the recognition of neural specificities of var
ious sorts, such as Descartes' reflex paths (an inevitable reaction to an
external stimulus because of the connection between stimulus and re
sponse via a specific nervous pathway); Charles Bell's law (the ventral spinal
cord is specifically motor in function, while the dorsal cord is specifically
sensory in function); Johannes Muller's "specific energies of nerves" (each
sensory nerve, however stimulated, gives rise to its own sensory process);
and Charles Sherrington's notion of "adequate stimulation" (each sense
organ responds optimally to a specific form of stimulation—each organ of
sense is specifically irritable, as Muller put it).
In this century, particularly in the last decade, the specificity of peri
pheral-central neural connections has been added to the list in the neuro-
biological sphere, and the species-specificity of motor movement (fixed or
modal action patterns), perception, and even learning has been added in the
behavioral and psychological spheres.
Specificity, whether behavioral or neural, is a phenotype—it is the out
come of a developmental process. Such a multilevel process involves not
only molecular biology and biochemistry, but intrinsic and extrinsic func
tional factors as well. The fact that a developing organism's spontaneous and
evoked sensory and motor experience may play an important role in the at
tainment of neural and behavioral specificity is a relatively new idea, one
that is explored rather fully in this volume.
While specificity is a problem which is best experimentally analyzed from
a developmental point of view, it is also a comparative problem, one that
must be studied in various animal groups in order to appreciate singularity (if
it be so) or multiplicity of "mechanism." Thus, the comparative coverage is
fairly broad, including fish, amphibians, birds, and mammals. Finally, there
are some long-standing conceptual problems common to the behavioral and
X
PREFACE xi
neural realms and these are described in the two introductory chapters and
the final chapter.
A word about the term "specificity." It is used in several different senses
throughout the volume. Whereas certain authors (Keating, and Meyer and
Sperry) mean to refer to the biochemical individuality of neurons by the term
neural specificity, other authors (Daniels and Pettigrew, and Gottlieb) use
the term to refer to specific or selective electrophysiological functions of
neurons (orientation-selective visual cells, for example) and/or highly
specific anatomical pathways (as, from certain points in the retina to certain
points in the visual cortex). The meaning each author has in mind for neural
specificity is usually made clear, either by the context or by overt definition.
The term "behavioral specificity," on the other hand, always refers to be
havior which is typical or characteristic of a species at a given stage of
development.
I am grateful to William R. Lippe and Ronald W. Oppenheim, the two
consulting editors for this volume, for their editorial suggestions. Mary
Catharine Vick provided her usual careful and cheerful assistance with
copyediting. Paul G. Roofe graciously lent a portrait of C. Judson Herrick.
GILBERT GOTTLIEB
C. Judson Herrick (1932)
DEDICATION ΤΟ
C. JUDSON HERRICK (1868-1960)
In view of the fact that Charles Judson Herrick died only 16 years ago, it
is startling to realize that his life began in "frontier" days. Minnesota had
entered the Union only a scant 10 years before his birth, and the city of
Minneapolis, his birthplace, was incorporated only the year before he
was born.
C. Judson Herrick's academic career intertwined with that of his older
brother Clarence. In 1885, when Clarence became professor of geology at
Denison University in Granville, Ohio, Judson accompanied him and en
rolled in the preparatory department of the college. In 1888, Clarence re
signed from Denison to accept a similar appointment at the University of
Cincinnati. In 1889, Judson followed Clarence to the University of Cincin
nati, where, in the following year, he was appointed laboratory assistant in
biology. In 1891, Judson became an instructor in the preparatory depart
ment at Denison and soon thereafter was awarded his B.S. degree from
Cincinnati. Meanwhile, his brother accepted an appointment at the Uni
versity of Chicago, one which he was to resign in only a few months, once
again returning to Denison. In that year (1892), Judson had accepted a pro
fessorship of natural science in Ottawa University, Kansas. In 1893, how
ever, he rejoined Clarence at Denison as a teaching fellow. Several months
later, Clarence became incapacitated by pulmonary tuberculosis and Judson
assumed most of his brother's teaching duties, as well as management of the
Journal of Comparative Neurology, which Clarence had founded three years
earlier. (Judson was to serve in a key editorial capacity on this journal until
1927, at which time he resigned as Managing Editor, and was succeeded by
G. E. Coghill.) In 1895, Clarence moved to New Mexico, and, in the follow
ing year, Judson pursued his Ph.D. research at Columbia University, return
ing to Denison in 1897. The following year, he was promoted to Professor
of Zoology (from Assistant Professor of Biology). He received his Ph.D.
degree from Columbia in 1900 for the research completed there in 1896 (on
xiii
Xiv DEDICATION TO C. JUDSON HERRICK (1868-1960)
the cranial nerves of Menidia, smelt-like fishes). Seven years later, Herrick
moved to the University of Chicago, where he took up duties as Professor
of Neurology in the Department of Anatomy. He stayed at Chicago for the
remaining 30 years of his active academic life.
While Herrick worked primarily on the neural structure and function of
fish and amphibian brains, he had very broad philosophic and scientific
interests, so he kept himself abreast of general developments in psychology,
zoology, and physics, as well as other fields. He numbered among his friends
and colleagues the comparative physiological psychologists R. M. Yerkes,
Heinrich Kliiver, and Karl Lashley, as well as the neuroanatomists George
E. Coghill and Gerhardt von Bonin, all of whom had strong interests in
psychological development and the evolution of the brain. In 1924, Herrick
published a book on the Neurological Foundations of Animal Behavior.
Although a regular contributor to the scientific literature throughout
his career, Herrick described himself as a slow study. (He was here no
doubt comparing himself to Clarence, who was an intellectual collossus
by anyone's standards.) In any event, C. J.'s variegated interests culminated
in several general books, published many years after his retirement from
the University of Chicago. The first of these volumes, published in 1948,
summarized his lifelong study of the tiger salamander's brain and was titled
simply The Brain of the Tiger Salamander. (It is by no means a straight
forward empirical treatment but includes a theoretical synthesis of the
probable course of cerebral development and evolution in vertebrates as a
whole. It was Herrick's assumption that the urodele amphibians represent
the most generalized version of the primitive brain and early behavior of
vertebrates, so, for him, they were the choice starting point for evolutionary
study.) The next year he published George Ellett Coghill, Naturalist and
Philosopher, in which he not only summarized Coghill's doings, but also
the content of innumerable philosophic conversations which he and Coghill
had engaged in over the years (Coghill had died in 1941). By his own admis
sion, there is considerable of Herrick's own philosophizing in that book; he
makes it clear that he shared Coghill's interest in such abstract conceptions
as "space, time, and consciousness."
The abiding question had to do with "psychogenesis"—the evolution of
mental development. When does consciousness (awareness) enter the phylo-
genetic picture? What features of the brain account for human intelligence,
perception, and cognition? In answer to the first question, in an imaginary
dialog which concludes the biography, Herrick has Coghill say:
There are ample precedents for giving "mind" a wider connotation than "consciousness."
If you prefer some other expression, like "experience," that can be split into conscious
and unconscious experience, I have no quarrel with that.... The thing that we agree upon
is that integrative experience, as you call it, and mentation, as I call it, is a total-pattern
DEDICATION TO C. JUDSON HERRICK (1868-1960) XV
type of activity common to all organisms and that there has been progressive expansion and
individuation of this pattern in evolutionary history and in personal development. As you
have suggested, this organic property may have its roots in what you call pattern of perfor
mance in the inorganic realm; it probably does. In any case the organic pattern is different
from anything known in the inorganic realm. Somewhere in this series a conscious component
of the pattern emerges. We don't know where, but there is no evidence at all that it is
anywhere present in the inorganic realm. Consciousness is a true emergent. Are we agreed
about this?
Herrick has himself reply:
Yes, and in this connection I would refer again to ... [the] conception of integrative levels
In discussing psychogenesis I prefer to stress the emergent capacities inherent in all natural
processes. In animals the total pattern of integration is necessarily changed, and the apparatus
employed undergoes differentiation parallel with every complication of the partial patterns as
these are successively individuated. Translating this clumsy verbiage into the vernacular, this
means that, during organic evolution and the struggle for existence, every individual preserves
his own life despite the multitude of different things he had to do about it. And the fullness of
that life is enlarged with every increase in his control of the environment which sustains him.
When conscious control is added to unconscious control, life is enriched by opening up an
entirely new domain of experience.
Herrick answered the question of the neural basis of perception and
cognition in the last book he published, The Evolution of Human Nature
(1956). The former ("analytic processes") he identified with the projection
areas of the brain; the latter ("synthetic or integrative processes") he identi
fied with the association areas of the brain. He wrote:
The brain is a glorified sorting machine and the projection centers of the cortex make the final
refinements of this analysis of the data of experience. In the remainder of the cortex the raw
data are rearranged in patterns which are in large measure determined by the use made of them,
that is, by experience. This is an integrative process which employs mechanisms and mechan
ical principles of different order from those of the analytic systems.
While certain of Herrick's psychological terms and concepts may seem a
bit "dated" (as no doubt ours will to those who succeed us), his multidis-
ciplinary orientation embodied in the term Psychobiology anticipated to
day's mode by more than half a century. As Herrick himself made abundant
ly clear, both he and his lifelong friend Coghill were intellectually indebted
to C. J.'s elder brother Clarence for their orientation. (As mentioned earlier,
Clarence was the founder of the Journal of Comparative Neurology. Judson
called it "the exponent of his [Clarence's] psychobiological interests." It
is significant that the journal was originally called the Journal of Comparative
Neurology and Psychology.)
Early on, Clarence envisioned a scientific meta-department of psycho-
biology, a holistic biological approach to the problem of behavior, meaning
its anatomical, physiological, and psychological study from the mutual per
spectives of phylogeny and ontogeny. Although Clarence published more
xvi DEDICATION TO C. JUDSON HERRICK (1868-1960)
than 150 papers and monographs between 1877 and 1910, it is through the
labors of his younger brother, Coghill, and Adolf Meyer, the father of Amer
ican psychiatry, that the concept of psychobiology comes down to us today.
C. J. actualized the concept through his evolutionary reconstruction of the
higher vertebrate brain by intensive anatomical analysis of fish and of
amphibian material (especially the urodeles). Coghill actualized the onto
genetic aspect through his correlative neuroanatomical-behavioral studies
of developing salamanders (urodeles).
In the best spirit of the psychological conception, C. Judson Herrick
always had his eye on behavior when thinking about the structure and
function of the nervous system. For example, in his classic The Brain of the
Tiger Salamander he wrote:
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 thé formation of a nervous
feltwork of extraordinary complexity. These neurons are not concerned primarily with
specific reflexes but with the coordination and integration of all movements. Some parts of
this intricate fabric, generally with 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 completely 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.
And when he turned his attention to matters of individual development,
Herrick of course recognized the principle of motor primacy and the innap-
propriateness of applying a simple stimulus-response formula to even the
earliest stages of behavioral activity in the most primitive of vertebrate
embryos:
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.... [Coghifl's]
researches have demonstrated beyond question that in this animal [salamander embryo] the
neuromuscular system is so organized... 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 develop
ment of both the total pattern and the partial patterns is initiated centrally, and throughout life
all of them are under some measure of unified central control ... 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
