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The Biology of Early Influences PDF

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The Biology of Early Influences The Biology of Early Influences Edited by Richard L. Hyson dna Frank Johnson Florida State University Tallahassee, Florida Kluwer Academic / Plenum Publishers New York, Boston, Dordrecht, London, Moscow Library of Congress Cataloging-in-Publication Data The biology of early influences / edited by Richard L. Hyson and Frank Johnson. p. cm. "Proceedings of the Florida State University Neuroscience Program Symposium on the Biology of Early Influences, held March 6-8, 1998 in Tallahassee, Florida"-T.p. verso. Includes bibliographical references and index. ISBN 0-306-46298-2 I. Developmental neurobiology--Congresses. I. Hyson, Richard Lee. II. Johnson, Frank. III. Florida State University Nenroscience Program Symposium on the Biology of Early Influences 0998 : Tallahassee, Fla.) QP363.5 .B567 1999 573.--dc2 99-049490 Proceedings of the Florida State University Neuroscience Program Symposium on the Biology of Early Influences, held March 6-8, 1998, in Tallahassee, Florida ISBN 0-306-46298-2 ©1999 Kluwer Academic/Plenum Publishers, New York 233 Spring Street, New York, N.Y. 10013 http://www.wkap.nl 10 9 8 7 6 5 4 3 2 1 A C.I.E record for this book is available from the Library of Congress All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher Printed in the United States of America PREFACE The underlying theme of this book si the role of experience in the development of the nervous system. It is now widely acknowledged that there are a variety of organism- environment interactions that guide the development of the nervous system. The popular press has also picked up on this theme and parents are being advised to enrich their child's sensory experience as early as possible. The importance of experience in development is so well accepted that it has begun to dictate public policy. In 1997, the President and First Lady hosted "The White House Conference on Early Childhood Development and Learning: What New Research on the Brain Tells Us About Our Youngest Children." Along with this conference came a reemphasis on programs directed at enriching the envi- ronment of America's youth. In some cases laws have been passed to assure enhanced early experience. In Georgia, the former governor proposed sending newborn children home from the hospital with classical music CDs. This received some praise, but was also ridiculed by others who felt the policy was not justified by the available scientific evidence. Here in Florida, enhanced "brain development activities" are mandated for state- funded child care facilities. Chapter 402.25 of the 1998 State of Florida Statues reads (emphasis added): Infants and toddlers in state-funded education and care programs; brain development activities.--Each state-funded education and care program for children from birth to 5 years of age must provide activities to foster brain development in infants and toddlers. A program must provide an environment rich in language and music and filled with objects of various colors, shapes, textures, and sizes to stimulate visual, tactile, auditory, and linguistic senses in the children and must include classi- cal music and at least 03 minutes of reading to the children each day.... A program must provide training for the infants' and toddlers' parents including direct dialogue and interaction between teachers and parents demonstrating the urgency of brain development in the first year of a child's life. Family day care centers are encouraged, but not required, to comply with this section. Whether it is exposure to Mozart or foreign language, there is a confidence that these early experiences enhance brain development and make for a more intelligent adult. This commonly accepted folklore regarding the importance of early sensory experience does have some scientific backing. One of the classic examples comes from the early work on differences between rats raised in an "enriched" environment and those raised in vi Preface "impoverished" environments (see Renner and Rosenzweig, 1987 for review). Such studies demonstrated, for instance, that animals perform better at maze learning tasks when raised in "enriched" environments which contain complex sensory stimuli, allow for social interactions, and permit a greater variety of motor behaviors (Forgays and Forgays, .)2591 Additionally, the enhanced rearing conditions lead to morphological signs of more robust brain development, such as larger brains and more dendritic branches in cortical neurons (Globus et al., 1973). Although the differences between groups are commonly viewed as "enrichment" effects, they could just as easily be viewed as deprivation effects due to raising the "impoverished" rats in the sterile environment of the typical rat home cage. In fact, it can reasonably be argued that even the "enriched" condition si relatively impoverished compared to the rich natural environment in which the rat evolved. Nev- ertheless, whether viewed as enrichment or deprivation effects, the fact that differences between groups emerge can be taken as evidence that experience plays a key role in reg- ulating brain and behavioral development. A less semantic question regarding the effects of these enrichment experiments ,si how do these differences emerge? What is it about the early experience that enhances (or prevents reduction in) brain growth? Clearly the complex constellation of differences between enriched and impoverished rearing conditions makes this question difficult to answer. A fruitful approach to get at the more mechanistic biological questions comes from studies in which the manipulation of experience si defined more concretely. This is commonly accomplished by restricting early experience in a single sensory modality. Depriving the subject of sensory experience within a specific modality provides a cleaner definition of the exact manipulation of experience than is possible when using the more general "enrichment" manipulation. This allows a focused analysis on the specific sensory system, and the biological mechanisms underlying these changes can be explored in a systematic manner. Probably the most famous of this type of experiment are the studies of Hubel and Wiesel on the effects of altering early visual experience (Wiesel and Hubel, 1963a,b; Wiesel and Hubel, 1965; Hubel and Weisel, 1970; Hubel et al., 1977). The work on the visual system stemming from these landmark studies has been frequently and extensively reviewed elsewhere (Lam and Shatz, 1991; Katz and Shatz, 1996; Crair et al., .)8991 Consequently, in this volume we emphasize what has been learned from studies of a variety of other model systems. For the purposes of this book, "experience" si broadly defined to include neural activity, hormonal environment, social interactions, as well as exposure to sensory stimuli. As will be discussed in each of the chapters, these early factors have dramatic effects on the ultimate fate and function of neurons. While it is no longer necessary to ask "if" experience influences brain development, much is left to be known "how" expe- riential influences exert their effect. Thus, a common theme in the work of all of the chap- ters is the biological mechanisms of early experiential influences in neural development. The word "early" (as in "early influences") ,si of course, a relative term. With this in mind, the chapters in this book are organized into 3 sections loosely based on the time at which the experiential manipulation is typically performed. The first section contains chapters that examine the lifelong influences of embryonic or perinatal manipulations, exemplified by studies on the motor, auditory and gustatory systems. The second section deals with the changes that are produced by manipulations early after birth or hatching and these chapters focus on the olfactory and auditory systems. The final section exam- ines changes during later developmental periods and, in particular, during major periods of transformation in the organism's life. Here, the model systems include moths, frogs, birds, and crayfish. Preface vii One purpose of our symposium was to bring together the ideas of investigators who use a variety of model systems to study the biology of early influences. Consequently, in this compilation we have intentionally juxtaposed work using different model systems, but which share common themes related to the development of the nervous system. It is hoped that the breadth of approaches will lead the reader to a greater depth of under- standing and broader appreciation for the possible mechanisms by which environmental factors influence neural development. Discussion of the importance of early experience is prevalent in the current public and scientific forums. While media, public health advocates, parents, and even legislators are all trumpeting the need for enriching our children's lives, it is not the primary goal of this volume to inform public policy. However, given the recent extensive air play on the importance of early experience in brain development, we felt it was time for us to evaluate critically what we know about the biological underpinnings of early influences. Richard Hyson Frank Johnson REFERENCES Crair, MC, Gillespie, DC and Stryker, MP (1998) The role of visual experience in the development of columns in cat visual cortex. Science 279:56(~570. Forgays, DG and Forgays, JW (1952) The nature of the effect of free-environmental experience in the rat. J Comp Physiol Psych 45:322-328. Globus, A, Rosenzweig, MR, Bennet, EL and Diamond, MC (1973) Effects of differential experience on den- dritic spine counts in rat cerebral cortex. J Comp Physiol Psychol 82:175 181. Hubel, DH and Weisel, TN (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol (Lond) 206:41%436. Hubel, DH, Wiesel, TN and LeVay, S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond (Biol) 278:377-409. Katz, LC and Shatz, CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133 1138. Lam, DM-K and Shatz, C J, Eds. (1991 ) Development of the Visual System. Proceedings of the Retina Research Foundation Symposia. Vol. .3 Cambridge, MIT Press. Renner, MJ and Rosenzweig, MR (1987) Enriched and impoverished environments. Effects on brain and behav- ior. New York, Springer-Verlag. Wiesel, TN and Hubel, DH (1963a) Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate nucleus. J Neurophysiol 26:978-993. Wiesel, TN and Hubel, DH (1963b) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 26:1003-1017. Wiesel, TN and Hubel, DH (1965) Comparison of monocular deprivation and binocular deprivation in cortex of cats. J Neurophysiol 28:1029 1040. ACKNOWLEDGMENTS The chapters in this volume were submitted by participants in a symposium enti- tled "The Biology of Early Influences" that was held in Tallahassee in March of 1998. The main goal of this symposium was to better understand the biological mechanisms by which early experience influences neural development. Towards this end, we brought together investigators who study a variety of model systems for a weekend of instructive and lively discussion. This symposium was part of the annual Rushton lecture series sponsored by the Program in Neuroscience at the Florida State University thanks to funding from the College of Arts and Sciences. Partial support for this symposium was also provided by the Congress of Graduate Students at the Florida State University. The annual lecture series is named for eminent neuroscientist .W A. H. Rushton, who was formerly a regular visitor to FSU. Additional information about the Program in stnapicitraP at the 8991 Rushton :muisopmyS The Biology of Early .secneulfnI Front wor (left to right): Dan ,senaS Edwin Rubel, Janis ,skeeW Robert Contreras, Donald .sdrawdE Back row: Michael Stryker, leahciM Leon, Ronald ,miehneppO Gail Burd, David Hill, Richard Hyson, Thomas Parks, Frank .nosnhoJ ix stnemgdelwonkcA x Neuroscience and Rushton lecture series can be obtained via the Internet at http://www.neuro.fsu.edu/. We as organizers and editors would like to thank the Program for Neuroscience, comprised of the departments of Psychology and Biology of the College of Arts and Sciences, and the department of Nutrition, Food and Exercise Sciences of the College of Human Sciences. We also thank Kathleen Carr for editorial assistance and MaryAnn McCarra at Kluwer Academic/Plenum Publishers for her assistance (and patience) in publishing these proceedings. CONTENTS I. Lifelong Influences from the Beginning Mechanisms of Activity-Dependent Motoneuron Development and Survival in the Chick Embryo ................................. Ronald W. Oppenheim . Cochlear Influences on Development of the Brainstem Auditory System ... 15 Thomas N. Parks . Early Influences on Gustatory Development .......................... 35 David L. Hill . Influence of Early Salt Diet on Taste and Blood Pressure in Rats ...... 53 Robert J. Contreras II. Youthful Exposure 5. The Role of Early Experience in Olfactory Bulb Cell Survival ........... 73 Brett Johnson and Michael Leon . Transneuronal Signals for Afferent Regulation in the Chick Auditory System .................................................... 87 Richard L. Hyson 7. The Developmental Influence of Inhibitory Synaptic Transmission ........ 105 Dan H. Sanes, Vibhakar C. Kotak, and Kent K. Fitzgerald III. Transformations 8. Metamorphosis as Midlife Crisis: What to Do with the Leftover Neurons? .................................................. 135 Janis C. Weeks 9. Development of the Olfactory System in the African Clawed Frog, Xenopus Laevis ............................................. 153 Gail D. Burd ix xii Contents .01 Afferent Regulation of Developmental Fate in the Songbird Telencephalon .............................................. 171 Frank Johnson 11. The Effects of Neuronal Growth and Social Experience on the Development of Behavioral Plasticity ........................... 185 Donald H. Edwards Index ............................................................. 201

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