The Neurobiology of Motivation and Reward

The Neurobiology of Motivation and Reward

James R. Stellar Eliot Stellar The Neurobiology of Motivation and Reward With 66 Figures Springer-Verlag New York Berlin Heidelberg Tokyo

James R. Stellar Department of Psychology and Social Relations Harvard University Cambridge, Massachusetts 02138 U.S.A. Eliot Stellar Department of Anatomy and Institute of Neurological Sciences University of Pennsylvania Philadelphia, Pennsylvania 19104 U.S.A. Library of Congress Cataloging in Publication Data Stellar, James. The neurobiology of motivation and reward. Bibliography: p. Includes index. 1. Motivation (Psychology)-Physiological aspects. 2. Reward (Psychology) I. Stellar, Eliot, 1919- II. Title. [DNLM: 1. Motivation-physiology. 2. Nervous System-physiology. 3. Reward. WL 102 S8235n] BF503.S82 1985 153.8 84-26729 1985 by Springer-Verlag New York, Inc. Softcover reprint of the hardcover 1st edition 1985 All rights reserved. No part of this book may be translated or reproduced in any form without written permission from Springer-Verlag, 175 Fifth Avenue, New York, New York 10010, U.S.A. The use of general descriptive names, trade names, trademarks, etc., in this publication, even if the former are not especially identified, is not to be taken as a sign that such names, as understood by the Trademarks and Merchandise Marks Act, may accordingly be used freely by anyone. Typeset by David E. Seham Associates Inc., Metuchen, New Jersey. 9 8 7 6 5 4 3 2 1 ISBN-13: 978-1-4615-8034-8 e-isbn-13: 978-1-4615-8032-4 DOl: 10.1007/978-1-4615-8032-4

To Betty, Teresa, jennifer, Liz, Chip, and Katie

Preface This book was conceived many years ago as an abstract goal for a father-son team when the father was working in university administration and the son was just getting into the academic business. Eventually, the father returned to the laboratory, the son began to get his feet on the ground, and the goal became concrete. Now the work is finished, and our book enters the literature as, we hope, a valuable contribution to understanding the terribly complex and subtle problem of the neurobiology of motivated behaviors. We would also like the book to stand as a personal mark of a cooperative relationship between father and son. This special relationship between the authors gave us an extra dimension of pleasure in writing the book, and it would delight us if it gave anyone else an extra dimension of enjoyment from reading it. One thing we hope happens is that anyone considering a similar partnership, or simply considering entering similar fields, will take the existence of this book as encouragement. Such relationships are highly satisfying if both parties take care to protect the partnership. When we actually sat down to write the book, we were humbled by the immense literature and the smallness of both our conceived space for putting it down and of our brains for processing all the information. In some places, we consciously did not discuss a particular study or area of literature. Certainly, there are also papers we have forgotten to cite or of which we are unaware. Therefore, we invite you to write to us with your suggestions if you feel some important work or a body of literature is neglected. We would like to acknowledge the many people who helped us with

Vlll Preface the preparation of this work. First, we would like to thank the other members of our family, who allowed this book to occupy much of our time together, and who actively supported us in its writing. Richard Solomon, Alan Epstein, Dale Corbett, and Meg Waraczynski all gave us their professional opinions on some of the chapters. Janet Gulotta, Mary Jack, Aimee Hamilton, and Kristin Quinlan provided valuable assistance on the word processors and in production aspects. Teresa Stellar helped us with the bibliography and with proofreading. Finally, the staff of Springer-Verlag gave us the encouragement and support we needed to work throllgh the vagaries of production of a finished manuscript. March, 1985 James R. Stellar Eliot Stellar

Contents 1 Introduction 1 The Scope and Use of this Book 1 The Book's Structure 2 The Book's Direction 3 2 A Brief History of Motivation and Reward Concepts 6 Instincts and Taxes 8 Hedonism 11 Sensory Psychology and Physiology 13 Temperament, Emotion, and Affect 14 Reinforcement 17 Regulatory Physiology 19 Neurobiology 20 The Concept of Motivation 22 3 Behavioral Aspects of Motivation and Reward 25 Behavioral Concepts and Definitions 29 Motivated Behavior 29 Reinforcement and Reward 30 Incentive 30 Preference, Aversion, and Choice 30 Competition Among Drives 31 Motivation 32

x Contents Measurement of Motivation 32 Deprivation and Drive 34 Satiation and Satiety 35 Acquired Motivation 35 Taste-Aversion Learning 35 Opponent Process Theory 36 Non-Homeostatic Motivation 38 Emergence of Motivated Behavior and Hedonic Responses in Phylogeny 40 Affect and Hedonic Response 43 Summary 49 4 Physiological Aspects of Motivation and Reward 51 Brain States 52 Neural Hierarchies 58 Peripheral and Central-Neural Interactions 65 Medial Hypothalamic Interactions 65 Lateral Hypothalamic Interactions 67 Feeding, Satiation, and Satiety 69 Conceptual Schemes of Peripheral-Central Interactions 71 Motor Control of Motivated Behavior 73 Reward, Affect, and Hedonic Response 76 Summary 81 5 The Measurement of Brain Stimulation Reward 83 Background 83 The Problem of ESB Reward Measurement 87 Continuous Reinforcement Lever-Pressing 89 The Input-Output Curve, Rate-Intensity, and Threshold 92 The Variable Parameter in an Input-Output Curve 93 Threshold and Half-Maximal Criterion 94 A Discrete Trial Procedure 95 The Reward Summation Function 97 The Extinction Paradigm 103 Autotitration or Set-Reset Method 106 Post-Reinforcement Pause 108 Response Strength Method 109 Choice and Other Methods 113 ESB Reward Psychophysics 114 Summary 120 6 The Neuroanatomy of Brain-Stimulation Reward 121 The Lateral Hypothalamus and Medial Forebrain Bundle: Many Possible Substrates 122 What Is Activated by the Electrode? 123

Contents xi Psychophysics of ESB Reward: Refractory Periods 128 Psychophysics: Linkage, Conduction Velocity, and Direction 130 Psychophysics: Other Structural and Anatomical Properties 135 Lesion Studies of ESB Reward 136 The Descending Path Hypothesis 140 Origin of the Descending Path 142 Some Subtleties and the Termination of the Descending Path 145 The Frontal Cortex: ESB Reward from Another Site 149 Single Unit Recording 151 Summary 154 7 Dopamine and ESB Reward 156 Some Basic Facts 157 Dopamine Brain Systems 162 ESB Reward and the Effects of Systemic Dopamine Blockade 169 Improving Selectivity through Drug Choice or Brain Injection 174 Food Reward and the Effects of Dopamine Blockade 178 Lesion Studies 182 Drug Self-Administration and Place Preference 184 Opiates 185 Some Models of Dopamine Function: Reward, Behavioral Activation, and Effort 186 The Ventral Tegmental Area and the Nucleus Accumbens 190 Whatever Happened to Norepinephrine? 192 Conclusions 193 8 Overview 195 Behavioral Phenomena Associated with ESB 195 Priming 196 Relation of ESB to Natural Reward 199 Evoked Motivational Effects 200 Approach-Withdrawal Function 202 Hierarchical Organization 205 Peripheral and Central-Neural Controls 208 General Arousal Versus Specific Activation 209 Localization of Function and Hierarchical Organization 209 Nature-Nurture and Role of Experience 210 Motivation and Phylogeny 211 Motivation and Ontogeny 211 Conclusions 212 Future Outlook 214 References Index 215 251