Development Neuropsychobiology

486 Pages·1986·11.635 MB·English

by  William Greenough (Eds.)

BEHAVIORAL BIOLOGY
AN INTERNATIONAL SERIES
Series Editors
James L. McGaugh
Department of Psychobiology
University of California
Irvine, California
John C. Fentress
Department of Psychology
Dalhousie University
Halifax, Canada
Joseph P. Hegmann
Department of Zoology
The University of Iowa
Iowa City, Iowa
A list of books in this series is available from the publisher on request.
Developmental
NeuroPsychobiology
Edited by
William T. Greenough
Department of Psychology, Department of Anatomical Sciences,
and Neural and Behavioral Biology Program
University of Illinois
Champaign, Illinois
Janice M. Juraska
Department of Psychology
Indiana University
Bloomington, Indiana
ACADEMIC PRESS, INC.
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COPYRIGHT © 1986 BY ACADEMIC PRESS, INC.
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ACADEMIC PRESS, INC.
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United Kingdom Edition published by
ACADEMIC PRESS INC. (LONDON) LTD.
24-28 Oval Road, London NW1 7DX
LIBRARY OF CONGRESS CATALOGING IN PUBLICATION DATA
Main entry under title:
Developmental neuropsychobiology.
Includes index.
1. Developmental neurology. 2. Developmental
psychobiology. I. Greenough, William T. II. Juraska,
Janice M. [DNLM: 1. Behavior —physiology.
2. Neurophysiology. 3. Psychophysiology. WL 103 D489]
QP363.5.D48 1985 599'.0188 85-6121
ISBN 0-12-300270-2 (hardcover) (alk. paper)
ISBN 0-12-300271-0 (paperback) (alk. paper)
PRINTED IN THE UNITED STATES OF AMERICA
86 87 88 89 9 8 7 6 5 4 3
In memory of Ryo Arai, editor for Academic Press, who instigated and
nurtured this volume and affected our lives in other ways as well.
Contributors
Numbers in parentheses indicate the pages on which the authors' contributions begin.
JEFFREY R. ALBERTS (449), Psychology Department, Indiana University,
Bloomington, Indiana 47405
ELLIOTT M. BLASS (423), Department of Psychology, The Johns Hopkins
University, Baltimore, Maryland 21218
RONALD G. BOOTHE1 (295), Department of Psychology, and
Department of Ophthalmology, University of Washington, Seattle,
Washington 98195
FEN-LEI F. CHANG (95), Department of Anatomy and Cell Biology, Center
for Neuroscience, University of Pittsburgh School of Medicine,
Pittsburgh, Pennsylvania 15261
BEN M. CLOPTON (363), Kresge Hearing Research Institute ,The University
of Michigan School of Medicine, Ann Arbor, Michigan 48109
JOHN S. EDWARDS2 (73), Max-Planck-Institut für Verhaltenphysiologie,
Abteilung Hüben, D8131 Seewiesen, Federal Republic of Germany
WILLIAM T. GREENOUGH (387), Department of Psychology, Department
of Anatomical Sciences, and Neural and Behavioral Biology Program,
University of Illinois, Champaign, Illinois 61820
LAWRENCE S. HONIG3 (1), Laboratory for Developmental Biology,
University of Southern California, Los Angeles, California 90089
Present address: Yerkes Primate Center, Department of Psychology, and Department of
Ophthalmology, Emory University, Atlanta, Georgia 30322.
2Present address: Department of Zoology, University of Washington, Seattle, Washington
98195.
3Present address: University of Miami, School of Medicine, Miami, Florida 33101.
xiii
XIV CONTRIBUTORS
JANICE M. JURASKA4 (409), Department of Psychology, Indiana
University, Bloomington, Indiana 47405
HELMUT KREBS (119), Laboratory of Developmental Neurobiology,
University of North Carolina School of Medicine, Chapel Hill, North
Carolina 27514
JEAN M. LAUDER (119), Laboratory of Developmental Neurobiology,
University of North Carolina School of Medicine, Chapel Hill, North
Carolina 27514
PAUL C. LETOURNEAU (33), Department of Anatomy, University of Min-
nesota, Minneapolis, Minnesota 55455
RAYMOND D. LUND (95), Department of Anatomy and Cell Biology,
Center for Neuroscience, University of Pittsburgh School of Medicine,
Pittsburgh, Pennsylvania 15261
ROBERT R. PROVINE (213), Department of Psychology, University of
Maryland Baltimore County, Catonsville, Maryland 21228
MARILYN SCHNECK (295), Department of Psychology, and Department
of Ophthalmology, University of Washington, Seattle, Washington 98195
WOLF SINGER (271), Max-Planck-Institut für Hirnforschung, 6000
Frankfurt am Main 71, Federal Republic of Germany
DENNIS J. STELZNER (241), Department of Anatomy, State University
of New York Upstate Medical Center, Syracuse, New York 13210
DENNIS SUMMERBELL (1), The National Institute for Medical Research,
The Ridgeway, Mill Hill, London NW7 1AA, England
RICHARD C. TEES (317), Department of Psychology, The University of
British Columbia, Vancouver, British Columbia, Canada V6T 1W5
C. DOMINIQUE TORAN-ALLERAND (175), Center for Reproductive
Sciences, and Department of Neurology, and Department of Anatomy
and Cell Biology, Columbia University College of Physicians and
Surgeons, New York, New York 10032
ELSI VASSDAL (295), Department of Psychology, and Department of
Ophthalmology, University of Washington, Seattle, Washington 98195
4Present address: Department of Psychology, University of Illinois, Champaign, Illinois
61820.
Preface
A motivating force behind the organization of this book was our perception
of the mutual isolation of the fields of developmental neuroscience and
developmental psychobiology. Each has its separate societies, journals, and
international meetings, and there is remarkably little overlap in membership
and even less in attendance at meetings. The editors of this book have often
found it difficult to classify themselves as either developmental psychobi-
ologists or developmental neuroscientists (although we feel that those other
members who identify themselves with one group tend to class us in the other
group). Similarly, perhaps because we borrow paradigms and techniques from
both, we have had difficulty in perceiving a natural break between the two
disciplines.
The two developmental disciplines fall on a continuum, stretching from
the molecular through the cellular and systems level to the behavioral level
of analysis, and investigations at one level often have important implications
for others. For example, issues of genetic constraints upon or determination
of species-typical patterns have potential answers at all these levels, as do
questions about the roles of hormones, neurotransmitters, and other neu-
romodulaters, and even about the roles of experience in behavioral
development.
In deciding upon the chapters for this book, we attempted to pick represen-
tative examples of particularly fruitful approaches across the range of studies
of neurobehavioral development. The selections emphasize fundamental
issues rather than paradigms. The ordering imposed upon these selections
may appear arbitrary, but it reflects one possible view of the developmental
neuro/psychobiology continuum. The list is not meant to be comprehensive.
Indeed, it is difficult to conceive of one's being comprehensive in an area
with as much good research as this one has.
XV
XVI PREFACE
Although we do not feel that a formal organization of the book into sub-
sections would be appropriate, in the sense that a definition of categorical
boundaries would break up the continuity with which this field should be
viewed, the topics we have chosen fall into logical groupings in terms of the
research problems they address. The initial chapters deal largely with intrinsic
mechanisms, specifying pattern formation in the developing nervous system.
Summerbell and Honig begin by describing the coordinate systems that appear
to govern peripheral patterns in limb development and the matching of spinal
nerve ordering to the peripheral map. Letourneau discusses mechanisms of
expression of pattern information at the cellular level, particularly as dis-
cerned from neurite-substrate interactions in vitro. Edwards then describes
the generation of pattern in vivo in insects, where individual fibers can be
reidentified across the developmental sequence, and their roles in pioneering
pathways, as well as their responses to experimental and genetic manipu-
lations, can be specifically assessed. In the final chapter on this topic, Lund
and Chang consider the mechanisms whereby patterns are established in the
vertebrate visual system, noting especially the nearly ubiquitous phenomenon
of exuberant overprojection, followed by competitive restriction of terminal
fields, as well as the evidence for the association of neuronal death with
terminal loss in more peripheral projections.
The chapters of Provine and Stelzner also deal with pattern, but at a higher
order, focusing upon the implications of the establishment of systems and
how the sequences whereby these systems become established are manifested
in the development of behavior. Working from a broad comparative per-
spective, Provine describes embryonic and postnatal behavioral manifes-
tations of somatic neural maturation and their neural substrates. Stelzner
then deals with encephalization, the process whereby supraspinal centers exert
control, in a partly nonreversible manner, over spinal circuitry. In this context,
Stelzner discusses a phenomenon often found in the developing mammalian
nervous system, that of greater sparing or recovery of behavioral function
when CNS damage is sustained earlier in life.
The chapter by Lauder and Krebs and that by Toran-Allerand discuss
intrinsic and extrinsic modulatory influences, both upon the timing and
sequencing of the genesis of neurons and synapses and upon the functional
organization that results from these influences. Noting the mounting evidence
for a morphogenetic role for neurotransmitters in embryonic development,
Lauder and Krebs speculate upon the orchestrating roles of neurotransmitters,
neurohumors, and hormones as differentiation and recognition signals from
the time of neural tube development through postnatal ontogeny and suggest
a broadened use of the term "critical period." The best understood example
of hormonal interactions with the developing mammalian brain, that of the
role of gonadal steroid hormones in sexual differentiation, may serve as a
PREFACE XVII
model for the less behaviorally specific effects of other hormones. Toran-
Allerand reviews work indicating structural and functional sexual
dimorphisms in the brain and describes in vitro approaches to determination
of the mechanisms whereby steroid hormones alter brain organization.
Further implications of possible hormonal influences at a more molar ana-
tomical and behavioral level are discussed in the chapter by Juraska, who
reviews sex differences in the developing brain's responses to environmental
conditions, in the context of human data that suggest greater male vulnera-
bility to insult.
The chapter by Singer could easily be grouped with the previous topic,
since among its several foci are the forces controlling the periods of greatest
sensitivity to experience. However, since it also concentrates upon the incor-
poration of information gained from experience—the organism's interactions
with its environment—it seems better grouped with others discussing the roles
of experience in the development of mammalian sensory systems. Singer
reviews the visual and nonvisual experiential controls of the maturation of
mammalian visual system physiology, as well as its central modulation, and
proposes rules and mechanisms for Hebbian synapses that could underlie
the effects of experience. Boothe, Vassdal, and Schneck consider the
structural development of the visual system, with an emphasis upon synaptic
changes underlying the physiological and behavioral effects of experience
manipulations. Tees casts a critical eye upon those who argue that behavioral
assessments of visual deprivation effects are too imprecise for comparison
with physiological and anatomical measures, arguing that although much
work has been deficient, such work need not be so. Clopton considers the
degree to which observations on the visual system are paralleled by the much
less frequent studies of other sensory systems. Greenough presents evidence
that many of the consequences of early sensory manipulations upon brain
structure are also seen after later manipulations of the complexity and learning
opportunities the environment provides, but argues for a fundamental
difference in the manner in which the changes originate in sensory
development versus later life.
Finally, the chapters of Alberts and Blass represent a separate category
in that they focus on the organism as part of a system within which
development takes place. Blass describes the role of olfactory information
from the pre- and postnatal environment in maintaining social orientation
and organization during development. Alberts evaluates previous models of
the forces driving parent-offspring relations and suggests a new model in
which both infant-infant interactions and offspring-parent interactions result
in mutually beneficial outcomes.
The papers are intended to be comfortably read by advanced followers
of the biological and/or psychological sciences, whether or not they are
XVIII PREFACE
familiar with work in the specific areas discussed. The chapters vary in the
degree to which technical details are discussed, largely because the technical
details are more critical to an understanding of theories and interpretations
of experimental tests in some areas than in others. Where the degree of
detailed knowledge necessary to understand an argument or explanation
exceeds the knowledge expected of, say, a graduate student in biology or
experimental-biological psychology, we have tried to ensure that the necessary
information is included within the chapter (unless it is available within others
to which the reader is referred). The book's greatest potential will be realized
if readers not really familiar with any of the areas covered will gain a per-
spective on the coherence that actually exists across the broad range of
approaches to brain-behavior development, an appreciation of the progress
that has been made, and a feel for the excitement with which workers within
the area view the prospects for major advances in the immediate future.
Finally, we thank the staff at Academic Press for consistent encouragement
over the far-too-long time it took to bring this book together, and we thank
for their patience the authors who got their chapters in on schedule.
WILLIAM T. GREENOUGH
JANICE M. JURASKA