Brain Dynamics and the Striatal Complex Conceptual Advances in Brain Research A series of books focusing on brain dynamics and information processing systems of the brain. Edited by Robert Miller, University of Otago, New Zealand (Editor-in-chief). Günter Palm, Universität Ulm, Germany and Gordon Shaw, University of California at Irvine, USA. Volume 1 Brain Dynamics and the Striatal Complex edited by R.Miller and J.R.Wickens Forthcoming Volumes Complex Brain Functions—Conceptual Advances in Russian Neuroscience edited by A.M.Ivanitsky and P.Balaban Time and the Brain edited by R.Miller Sex Differences in Brain Lateralization edited by V.L.Bianki and E.B.Filipova Cortical Areas: Unity and Diversity edited by A.Schüz and R.Miller Volumes in Preparation The Female Brain Neural Determinism Dynamics of Brain Function Brain Oscillations and Functional Memory This book is part of a series. The publisher will accept continuation orders which may be cancelled at any time and which provide for automatic billing and shipping of each title in the series upon publication. Please write for details. Brain Dynamics and the Striatal Complex Edited by R.Miller and J.R.Wickens School of Medical Sciences University of Otago New Zealand harwood academic publishers Australia • Canada • France • Germany • India • Japan Luxembourg • Malaysia • The Netherlands • Russia • Singapore Switzerland This edition published in the Taylor & Francis e-Library, 2004. Copyright © 2000 OPA (Overseas Publishers Association) N.V. Published by license under the Harwood Academic Publishers imprint, part of The Gordon and Breach Publishing Group. All rights reserved. No part of this book may be reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying and recording, or by any information storage or retrieval system, without permission in writing from the publisher. Printed in Singapore. Amsteldijk 166 1st Floor 1079 LH Amsterdam The Netherlands British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library. ISBN 0-203-30491-8 Master e-book ISBN ISBN 0-203-34307-7 (Adobe eReader Format) ISBN: 90-5702-478-0 (Print Edition) ISSN: 1029-2136 v CONTENTS Series Preface vii Preface ix List of Contributors xi 1 Relationships of Substantia Nigra Dopamine Neurone Activity to Behaviour 1 Brian I.Hyland 2 The Role of Dopamine in the Control of Locomotor Activity and Reward-Related Incentive Learning 29 Richard J.Beninger and Mary C.Olmstead 3 Stimulants and Motor-Related Striatal Neuronal Activity 51 George V.Rebec 4 Dopamine Regulation of Synaptic Plasticity in the Neostriatum: A Cellular Model of Reinforcement 65 Jeffery R.Wickens 5 The Amygdaloid Complex: Input Processor for the Midbrain Dopaminergic Nuclei and the Striatum 77 Robert Miller 6 Synaptology and Physiology of Neostriatal Neurones 111 Ben D.Bennett and Charles J.Wilson 7 Neural Dynamics and Surround Inhibition in the Neostriatum: A Possible Connection 141 Jeffery R.Wickens and Dorothy E.Oorschot 8 The Domain Hypothesis: A Central Organizing Principle for Understanding Neostriatal Circuitry? 151 Dorothy E.Oorschot 9 Adaptive Classification of Cortical Input to the Striatum by Competitive Learning 165 Dietmar Plenz and Stephen T.Kitai 10 Insights from Gene Regulation into the Functional Role of Dopamine in the Striatum 179 Charles R.Gerfen 11 Dopaminergic Regulation of Striatal Physiology 195 D.James Surmeier Contents vi 12 Striatal Contention Scheduling and the Split Circuit Scheme of Basal Ganglia-Thalamocortical Circuitry: From Anatomy to Behaviour 209 Daphna Joel and Ina Weiner 13 Motor and Non-Motor Roles of the Cortico-Basal Ganglia Circuitry 237 Emilio Salinas, Ioan Opris, Antonio Zainos, Adrián Hernández and Ranulfo Romo 14 Discussion Section 257 POSTLUDE Striatal Circuitry: Categorically Selective, or Selectively Categorical? 289 Charles J.Wilson Index 307 vii SERIES PREFACE The workings of the brain, including the human brain are a source of endless fascination. In the last generation, experimental approaches to brain research have expanded massively, partly as a result of the development of powerful new techniques. However, the development of concepts which integrate and make sense of the wealth of available empirical data has lagged far behind the experimental investigation of the brain. This series of books entitled Conceptual Advances in Brain Research (CABR) is intended to provide a forum in which new and interesting conceptual advances can be presented to a wide readership in a coherent and lucid way. The series will encompass all aspects of the sciences of brain and behaviour, including anatomy, physiology, biochemistry and pharmacology, together with psychological approaches to defining the function of the intact brain. In particular, the series will emphasise modern attempts to forge links between the biological and the psychological levels of describing brain function. It will explore new cybernetic interpretations of the structure of nervous tissue; and it will consider the dynamics of brain activity, integrated across wide areas of the brain and involving vast numbers of nerve cells. These are all subjects which are expanding rapidly at present. Subjects relating to the human nervous system as well as clinical topics related to neurological or psychiatric illnesses will also make important contributions to the series. These volumes will be aimed at a wide readership within the neurosciences. However, brain research impinges on many other areas of knowledge. Therefore, some volumes may appeal to a readership, extending beyond the neurosciences. Books suitable for the series are monographs, edited multiauthor collections or books deriving from conferences, provided they have a clear underlying conceptual theme. In order to make these books widely accessible within the neurosciences and beyond, the style will emphasise broad scholarship comprehensible by readers in many fields, rather than descriptions in which technical detail of a particular speciality is dominant. The next decades promise to provide major new revelations about brain function, with far-reaching impact on the way we view ourselves. These great breakthroughs will require a broad interchange of ideas across many fields. We hope that the CABR series plays a significant part in the exploration of this important frontier of knowledge. ix PREFACE This book is the first volume in a new series of books, entitled Conceptual Advances in Brain Research. Relatively few books have been written addressing the way in which dynamic functions are related to cellular structure and synaptic organization in the basal ganglia. At present this is a somewhat speculative relation. Nevertheless a number of relatively solid themes have emerged in recent years. Indeed, there has probably been greater progress in relating structure to function within the basal ganglia than in some other areas of the mammalian forebrain. The striatum is the largest and best characterised nucleus within the basal ganglia, and understanding of the basal ganglia as a whole cannot get very far without a detailed model of the striatum, relating structure to function. In compiling this volume we have used a rather broad definition of the striatum, including the ventral (so-called limbic) parts of it. We have also included material concerning the structures and processes on the afferent side of the striatum (the cerebral cortex, the dopamine rich divisions of the midbrain, and the amygdala, and their respective functions). In later chapters, the two-way interplay between striatum and cerebral cortex is discussed from a wider perspective. Major issues addressed by the various contributing authors are as follows: Dominating the early chapters of the book are several chapters dealing with the role of the dopaminergic input to the striatum. These include consideration of the behavioural role of dopamine, the functions of dopamine as seen in electrophysiological experiments in behaving animals, and the actions of dopamine at the cellular and synaptic level. The link between psychological concepts of reward-related learning (including some other aspects of instrumental conditioning paradigms) and the underlying biology is explicitly discussed in some of these early chapters. The middle section of the book deals with cellular, synaptic and network organization of the striatum, considered by itself. Of some importance are attempts to derive descriptions of network dynamics in the striatum from cytological and single-neurone electrophysiological evidence. Another issue dealt with in some chapters of the middle section is the relative roles of the so-called ‘direct’ and ‘indirect’ outflow pathways from the striatum, and the possibility that they are modulated by different dopamine receptors. Both these issues have theoretical significance well beyond the striatum, indeed for the dynamics of the forebrain as a whole. However, empirical evidence relating to both these issues is at present insufficient for making definitive conclusions. The last part of the book contains two chapters exploring the mutual interaction between striatum and cerebral cortex. A distinctive feature of the book is a discussion section which was organized by electronic mail. This consists of an edited dialogue between some of the chapter authors (and other invited discussants). This section seeks consensus on some issues, and explores some of the remaining controversies.