Brain Organization and Memory This page intentionally left blank Brain Organization and Memory: Cells, Systems, and Circuits Edited by JAMES L. McGAUGH NORMAN M. WEINBERGER GARY LYNCH New York Oxford OXFORD UNIVERSITY PRESS Oxford University Press Oxford New York Toronto Delhi Bombay Calcutta Madras Karachi Kuala Lumpur Singapore Hong Kong Tokyo Nairobi Dar es Salaam Cape Town Melbourne Auckland and associated companies in Berlin Ibadan Copyright © 1990 by Oxford University Press First published in 1990 by Oxford University Press, Inc., 200 Madison Avenue, New York, New York 10016 First issued as an Oxford University Press paperback, 1992 Oxford is a registered trademark of Oxford University Press All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise, without prior permission of Oxford University Press. Library of Congress Cataloging-in-Publication Data Brain organization and memory : cells, systems, and circuits / edited by James L. McGaugh, Norman M. Weinberger, Gary Lynch. p. cm. Based on the Third Conference on the Neurobiology of Learning and Memory organized by the Center for Neurobiology of Learning and Memory of the University of California, Irvine, held at Irvine on Oct. 14-17, 1987. Includes bibliographies and index. ISBN 0-19-505496-2 ISBN 0-19-507712-1 (Pbk.) 1. Memory —Congresses. 2. Cerebral cortex Physiology—Congresses. 3. Neural circuitry—Congresses. L McGaugh, James L. II. Weinberger, Norman M. III. Lynch, Gary. IV. University of California, Irvine. Center for the Neurobiology of Learning and Memory. [DNLM: L Cerebral Cortex physiology -congresses. 2. Memory—physiology-congresses. 3. Models, Neurological—congresses. 4. Nervous System- physiology—congresses. WL 102 B8132 1987] QP406.B735 1989 153.T2 dc19 DNLM/DLC for Library of Congress 88-38920 9 8 7 6 5 4 3 21 Printed in the United States of America Preface This volume is the third in a series. Like its predecessors, Neurobiology of Learn- ing and Memory and Memory Systems of the Brain, this book is the outgrowth of a conference that was organized by the Center for the Neurobiology of Learn- ing and Memory of the University of California, Irvine. The Third Conference was held at Irvine on October 14-17, 1987. One might ask, as we did, whether a book summarizing work on how the brain encodes and uses memory is needed every two to three years. An examination of the tables of contents of the three books clearly answers this question. Some of the central theoretical and meth- odological issues addressed in this book are not so much as noted in the indexes of the previous volumes. This attests to the active and expanding interest in research on brain, learning, and memory. This book focuses on three related topics: forms of memory, regulation of cor- tical function in memory, and representations. Some of the themes developed in the first two volumes are given further emphasis in this book. Prominent among these are the efforts to relate learning and memory as they are studied in animals to those processes observed in humans. Despite steady experimental and conceptual progress, development of an adequate taxonomy of memory continues to hamper efforts to achieve unification of memory theory. This annoying fact should temper our hopes for a rapid and complete integration of the subtle and surprising phenomena of memory with those of brain cells, sys- tems, and circuits. Nonetheless, it is clear that the rate of progress in understand- ing the cellular processes underlying memory continues to accelerate. We are beginning to see the emergence of a consensus regarding the physiological and chemical events that translate activity patterns into long-term changes in the strength of connections between brain cells. We are also now seeing behavioral studies of memory using predictions derived from understanding of synaptic plasticity. One can only be impressed at how quickly the world of ions and receptors is being translated into the realm of memory systems and mazes. Special emphasis is given in this volume to computational and modeling approaches to the study of brain and memory. The development of network vi Preface models and computer simulations of memory permeates current research. This effort is explicitly recognized in the final section of the book, but the use of net- work models is seen throughout the book. Experimentalists working on cortex and hippocampus are attempting to link cells to systems with interesting and powerful models. However, the gap between formal mathematically tractable models and the stuff of brains remains clear and provides a continuing challenge for experimentalists and theorists alike. In all, the leitmotif of this book, like that of its predecessors, is excitement. Excitement about what we have learned as well as what we can now ask. We hope that readers of Brain Organization and Memory: Cells, Systems, and Cir- cuits will share our excitement as well as our eagerness to follow this intellectual drama in volumes yet to come. Irvine, Calif. J. L. McG. October 1988 N. M. W. G. L. Acknowledgments The conference on which this book is based was planned and organized by the members of the Center for the Neurobiology of Learning and Memory at the University of California, Irvine. The selection of topics and authors grew out of extensive discussions with our colleagues John Ashe, Michel Baudry, Richard Granger, Mary-Louise Kean, Mark Rosenzweig, Gordon Shaw, Larry Squire, and Larry Stein. Funding for the conference was provided by a number of orga- nizations: the UCI Office of Research and Graduate Studies, the Office of Naval Research, the Air Force Office of Scientific Research, the National Science Foun- dation, the Sloan Foundation, the Irvine Company, Searle Research and Devel- opment, Beckman Instruments, and Hoechst-Roussel Pharmaceuticals. We thank Lynn Brown, Nan Collett, and Lori LaSalle for their skilled coordination of all aspects of the conference. Special thanks are also due to Lynn Brown for editorial assistance. This page intentionally left blank Contents 1. Neurobiology of Memory: The Significance of Anomalous Findings 3 JAN BURES I Forms of Memory Introduction 23 MICHELA GALLAGHER 2. The Development of Learning and Memory in Aplysia 27 THOMAS J. CAREW EMILIE A. MARCUS THOMAS G. NOLEN CATHARINE H. RANKIN MARK STOPFER 3. Synaptic Plasticity, Neural Architecture, and Forms of Memory 52 RICHARD G. M. MORRIS 4. Forms of Memory in Pavlovian Conditioning 78 PETER C. HOLLAND 5. Functional Forms of Human Memory 106 MARCIA K. JOHNSON COMMENTARIES AND ALTERNATIVE PERSPECTIVES 6. Neuromnemonics: Forms and Contents 137 NORMAN M. WEINBERGER 7. Time and Memory 145 ROBERT W. DOTY 8. Forms of Memory: Issues and Directions 159 ARTHUR P. SHIMAMURA
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