THE LIMBIC SYSTEM

THE LIMBIC SYSTEM

Robert L. Isaacson Department of Psychology University of Florida Gainesville, Florida

PLENUM PRESS • NEW YORK AND LONDON

Library of Congress Cataloging in Publication Data

Isaacson, Robert Lee, 1928-The limbic system.

Bibliography: p. 1. Limbic system.!. Title.

[DNLM: 1. Limbic system. WL307 173L 1974) QP383.2.I82 599'.01'88 74-8298 ISBN-13:978-1-4613-4S07-7 e-ISBN-13:978-1-4613-4S0S-3 DOl: 1O.1007/978-1-4613-4S0S-3

First Printing - August 1974 Second Printing - May 1976 Third Printing - July 1978

© 1974 Plenum Press, New York Softcover reprint of the hardcover 1st edition 1974

A Division of Plenum Publishing Corporation 227 West 17th Street, New York, N.Y. 10011

United Kingdom edition published by Plenum Press, London A Division of Plenum Publishing Company, Ltd. 4a Lower John Street, London WIR 3PD, England

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

PREFACE

While this book is intended to be an introduction to the neuroanatomy of the limbic system and to studies of the behavior of animals in which the limbic system is stimulated or damaged, it is primarily intended for advanced students of brain-behavior relationships. I have assumed the reader to have some under­standing of the structure of the brain, of basic neurophysiology, and of modern behavioral techniques. It has been written for

students in graduate programs in psychobiology, physiological psychology, and the neurosciences, but it also should be of interest to some medical students and to others with catholic interests in the biology of behavior.

In the first chapter, I review the structure of the limbic system and in subsequent chapters consider the behavioral effects of lesions and stimulation of components of the limbic system. Supplement information derived from recording the electrical signals of the brain is included where it seems appropriate. The final chapter presents a perspective of the limbic system related to brain stem mechanisms and the neocortex. Understanding the behavioral contributions of the limbic system presupposes under­standing how the limbic system interacts with other systems of the brain.

v

vi Preface

Even though there is only one chapter overtly devoted to theoretical issues. various biases of mine influence all chapters. Anyone reading the book with a critical attitude will soon be aware of them. I would like to alert the reader to some of them ahead of time.

Simply put: the book is flavored by my own orientation to research and reading. For the past 15 years. I have been in­volved in research programs which were directed at elucidating the effects of limbic system destruction on behavior in the rat. cat. and rabbit. Therefore. studies using these species and using lesion techniques probably are overly represented. Other biases of mine will be apparent.

In many later chapters. consideration is given to the behavioral correlates of electrical rhythms recorded from various limbic structures. In these chapters. the effects of electrical stimulation of various limbic structures on behavior are also discussed. Yet. while these topics are discussed. much less emphasis is placed on them and on studies using other species with which I am less well acquainted.

My biases. the topics and areas given emphasis. come in part from my own research. This research is based on beliefs pertaining to research strategies. I believe that the most sub­stantial knowledge available about the limbic system comes from the use of stimulation and lesion techniques in rats and cats. There is far less' useful information available today arising from work using other techniques and other species. Since a great deal more information is needed before an adequate con­ceptualization can be achieved. this information must come from careful studies using species like the cat and the rat. These animals are amenable to laboratory experimentation and can be used in sufficient numbers so as to provide this information relatively quickly. If we had to rely on studies using nonhuman primates. our understanding of the behavioral contributions made by the limbic system could be greatly delayed. The rat is a necessary laboratory tool. both for neuroanatomists and for those interested in the behavioral contributions of the limbic system. The cat makes its greatest contribution to neurophysio­logical research.

The other obvious orientation of the book is the emphasis

Preface vii

placed on understanding the functions of the limbic system as revealed by destruction of its parts. For 30 years and more, investigations have been underway of the behavior of animals which have had some portion of the limbic system destroyed by aspirative or by electrolytic lesions. Seeking to understand a structure by destroying it is a useful technique for the behaviorally oriented neuroscientist, although it has many faults, dangers, and traps for the unwary experimenter. Nevertheless, equally dangerous are the faults and traps awaiting those using other techniques in the neurobehavioral sciences. In reality, the lesion technique is no better or worse than any other, such as recording electrical rhythms or recording from single units. Satisfactory understanding of the limbic system will not come from the studies of animals with lesions of this or that part of the limbic system or from the analysis of single cell activity but from theoretical contributions derived from the use of all available techniques. Theories must be evaluated on the basis of whether they make sense of the facts to be explained. A theory must provide a meaningful and useful synthesis of information derived from any and all techniques.

Even though the book has a large number of references to published work on the limbic system, it is not a truly com­prehensive review of the literature. I doubt that a totally com­prehensive review of the experimental literature can be done by anyone. Still. I have tried to represent fairly most of the impor­tant studies which have influenced present research directions. Nevertheless, some of my colleagues will be offended by not finding their favorite studies in the book. To them I apologize for the oversight. On the other hand, some studies were omitted because I felt that they had not added a great deal to our under­standing of the limbic system. I have tried to select articles from the literature which highlight information of the greatest importance for the understanding of the limbic system.

Theories of limbic function have not been emphasized in this book, since I do not think there are any adequate theories of limbic system function. My theory, presented in the last chapter, is offered in an apologetic fashion. At best, it offers only the broadest of outlines for a schema of limbic system function. In almost a playful spirit it is offered as a potential stimulant

viii Preface

to others. In a lecture given at the University of Florida in the spring of 1973, Paul Maclean suggested that scientists did not belong in the laboratory if their work and the generation of ideas were not fun. All of my days in the laboratory have been rewarding. I cannot imagine a more fascinating or more interesting life than struggling to find out how the brain works. Therefore, I hope the reader will evaluate the last chapter with understanding.

But my research and study of the limbic system is motivated by far more than the joy it provides. It is motivated by the belief that learning at least some of the secrets of the nervous system will be of value to mankind. This is not an intangible or abstract motive. Retarded children are very real, as are people with other brain disorders. While much of my present work is directed toward problems of general interest rather than toward retardation specifically, the ultimate goal is to better understand the human condition and to help provide information on which effective therapies and treatments for the brain-damaged can be based.

Accordingly, this is the appropriate time to acknowledge the fact that much of the research summarized in this book, my own included, would not have been possible without the financial support provided by two agencies of the government: the National I nstitute of Mental Health and the National Science Foundation. The administrators in these agencies who have been advocates and supporters of the peer-review system for the support of biobehavioral sciences have made a real contribution.

Part of the joy which comes from the academic life and the laboratory is the association with young, powerful minds coming to grips with the challenge of science. One of the most pleasant features, therefore, of my academic life has been the opportunity to watch students become accomplished neuro­behavioral scientists. I feel that I have been very lucky to count among my former students so many who have made substantial contributions to man's knowledge of brain and behavior. Therefore, if this book has any group to whom it should be dedicated, it would be to my graduate students, both those who have left the laboratory and those who are presently struggling through the ordeals of graduate education. The present group of students has helped me in the preparation of this book by their thoughts and criticisms. These include Michael L. Woodruff. Ron Baisden,

Preface ix

Barbara Schneiderman, linda lanier, Ted Petit, and Tom lanthorn. In addition, in the preparation of this book I have benefited

from the advice of friends, well known in neurobehavioral fields, who have read portions of the manuscript. These include Dr. Paul Maclean, Dr. Graham Goddard, Dr. Charles Votaw, Dr. Elliot Valenstein, Dr. Joel lubar, and Dr. Frederick A. King. Most especially, I would like to acknowledge the comments made by my colleagues Drs. Carol Van Hartesveldt and Peter Molnar. Their ideas and research in the area of the limbic system function always have been top flight.

At last, I would like to thank Mrs. Virginia Walker for her help in preparing the manuscript in all of its various revisions. She has tolerated the almost endless changes of the text I have made and without her assistance the book just could not have been completed.

Gainesville, Florida Robert L. Isaacson

CONTENTS

CHAPTER 1 The Structure of the limbic System.

The Limbic System in Nonmammals The Question of Homology The Hypothalamus

Nuclear Groups Fiber Systems

The Amygdala Nuclear Groups Fiber Systems

The Hippocampus . Layers of the Hippocampus Subdivisions of the Hippocampus Layers of the Fascia Dentata . . . Transitional Zones to the Hippocampus The Fornix .

The Septal Area Nuclear Groups Fiber Connections

xi

1

3 8

10 12 13 18 18 19 27 29 34 34 37 40 45 46 46

xii

The Mammillary Bodies, the Anterior Thalamus, and the Cingulate Cortex

Limbic System-Midbrain Relations

CHAPTER 2 The Hypothalamus

Pleasurable Reactions . The Location of Pleasure Regions Pain and Punishment . . . . . The Location of Pain Regions .. Elicited Behaviors . . . . . . . . .

Changes in Elicited Behaviors Self-Stimulation, Arousal and Elicited

Behaviors ............. . Relations with the Autonomic Nervous System Lesions of the Lateral Hypothalamus . . . . . .

A Modification of the Lateral Hypothalamic Syndrome ..

Escape Behavior . . . . . . . . Sensory Neglect . . . . . . . .

Ventromedial Hypothalamic Lesions Selective Lesions in the Hypothalamus. Neurochemical Systems ....... . The Neurochemistry of Eating .... . The Neurochemistry of Behavioral Suppression The Mammillary Bodies, the Mammillothalamic

Tract, and the Cingulate Cortex ..... . Lesions of the Mammillothalamic Tract The Cingulate Cortex: Avoidance Tasks Other Behavioral Contributions of the

Cingulate Cortex . Reflections and Summary ........ .

Chapter 3

Contents

50 55

59

60 62 63 65 67 68

71 74 75

78 79 81 82 83 86 89 93

95 95 98

100 103

The Amygdala ....... 107

General Effects Produced by Amygdala Stimulation or Lesions . . . . . . . . . . . . . . . 108

Contents xiii

Autonomic Effects 108 Orienting and Habituation 110 Emotional Changes . . . . 111 Arousal and Social Reactivity 114

Studies of Learning and Memory 117 Aversive Conditioning . . . . 117 Response Suppression in Appetitive Tasks 124

Transfer and Transposition 128 Reflections and Summary 131

CHAPTER 4 The Septal Area 133

General Changes Following Septal Lesions 133 Emotionality . . . . 133 Water Consumption 136 Social Behavior . . 138 Activity 1 39

Changes in Performance on Learning Tasks After Septal Lesions-Avoidance Behaviors. 140

Response Inhibition in Appetitive Tasks . . . .. 145 Electrical Stimulation of the Septal Area . . . .. 149

Autonomic Effects Produced by Septal Stimulation 153 Neurochemical Considerations 154 Reflections and Summary 157

CHAPTER 5 The Hippocampus .... 161

General Changes Produced by Hippocampal Damage 161

Locomotor Activity 163 Distractibility 165 Alternation . . . . . 167 Relations to the Autonomic Nervous System 169 Endocrine Relations . . . . . . . . . . . . 170

Studies of Learning and Memory-Avoidance Conditioning 171

Learning in Appetitive Tasks . . . . . . . . . . 175

xiv Contents

The DRL Impairment 176 Discrimination Learning 178

Frustration 188 Individual Differences in Learning Studies 192 Perseveration ............... 193

Regional Differences Within the Hippocampus 195 Electrical Rhythms of the Hippocampus . . . . 200

The Conditioning of Hippocampal Slow Waves 206 Electrical Seizure Activity . . . . . . . 207 Seizures and Memory . . . . . . . . . 209 Behavioral Consequences of Artificial

Epileptogenic Foci 211 Summary and Reflections ......... 214

CHAPTER 6 The Graven Image, Lethe, and the Guru 219

The Triune Brain 220 Animals with Predominantly Protoreptilian

Brains .. ' .............. 221 More Complicated Forms of Learning and Memo~ . . . . . . . . . . . . . . . . . 224

The Limbic System and the Paleomammalian Brain 229

Proactive Interference . . . . . . . . . . . .. 232 Inferred Characteristics of the Reptilian Core

Brain The Neocortex: The Guru

References . . Author Index . Subject Index

235 239

245 281 289