THE BASAL GANGLIA VIII ADVANCES IN BEHAVIORAL BIOLOGY Editorial Board Jan Bures Institute of Physiology, Prague, Czech Republic Irwin Kopin National Institute of Mental Health, Bethesda, Maryland Bruce McEwen Rockefeller University, New York, New York Karl Pribram Radford University, Radford, Virginia Jay Rosenblatt Rutgers University, Newark, New Jersey Lawrence Weiskranz University of Oxford, Oxford, England

Recent Volumes in This Series

Volume 39 THE BASAL GANGLIA III Edited by Giorgio Bernardi, Malcolm B. Carpenter, Gaetano Di Chiara, Micaela Morelli, and Paolo Stanzione Volume 40 TREATMENT OF DEMENTIAS: A New Generation of Progress Edited by Edwin M. Meyer, James W. Simpkins, Jyunji Yamamoto, and Fulton T. Crews Volume 41 THE BASAL GANGLIA IV: New Ideas and Data on Structure and Function Edited by Gérard Percheron, John S. McKenzie, and Jean Féger Volume 42 CALLOSAL AGENESIS: A Natural Split Brain? Edited by Maryse Lassonde and Malcolm A. Jeeves Volume 43 NEUROTRANSMITTERS IN THE HUMAN BRAIN Edited by David J. Tracey, George Paxinos, and Jonathan Stone Volume 44 ALZHEIMER’S AND PARKINSON’S DISEASES: Recent Developments Edited by Israel Hanin, Mitsuo Yoshia, and Abraham Fisher Volume 45 EPILEPSY AND THE CORPUS CALLOSUM 2 Edited by Alexander G. Reeves and David W. Roberts Volume 46 BIOLOGY AND PHYSIOLOGY OF THE BLOOD-BRAIN BARRIER: Transport, Cellular Interactions, and Brain Pathologies Edited by Pierre-Olivier Couraud and Daniel Scherman Volume 47 THE BASAL GANGLIA V Edited by Chihoto Ohye, Minoru Kimura, and John S. McKenzie Volume 48 KINDLING 5 Edited by Michael E. Corcoran and Solomon Moshé Volume 49 PROGRESS IN ALZHEIMER’S AND PARKINSON’S DISEASES Edited by Abraham Fisher, Israel Hanin, and Mitsuo Yoshida Volume 50 NEUROPSYCHOLOGY OF CHILDHOOD EPILEPSY Edited by Isabelle Jambaqué, Maryse Lassonde, and Olivier Dulac Volume 51 MAPPING THE PROGRESS OF ALZHEIMER’S AND PARKINSON’S DISEASE Edited by Yoshikuni Mizuno, Abraham Fisher, and Israel Hanin Volume 52 THE BASAL GANGLIA VII Edited by Louise F.B. Nicholson and Richard L.M. Faull Volume 53 CATECHOLAMINE RESEARCH: From Molecular Insights to Clinical Medicine Edited by Toshiharu Nagatsu, Toshitaka Nabeshima, Richard McCarty, and David S. Goldstein Volume 54 THE BASAL GANGLIA VI Edited by Ann M. Graybiel, Mahlon R. Delong, and Stephen T. Kitai Volume 55 KINDLING 6 Edited by Michael E. Corcoran and Solomon L. Moshé

A Continuation Order Plan is available for this series. A continuation order will bring delivery of each new volume immediately upon publication. Volumes are billed only upon actual shipment. For further information please contact the publisher. THE BASAL GANGLIA VIII

Edited by

J. Paul Bolam MRC Anatomical Neuropharmacology Unit University of Oxford UK

Cali A. Ingham Division of Veterinary Biomedical Science University of Edinburgh UK and

Peter J. Magill MRC Anatomical Neuropharmacology Unit University of Oxford UK J.P. Bolam C.A. Ingham MRC Anatomical Neuropharmacology Unit University of Edinburgh Oxford Edinburgh United Kingdom United Kingdom

P.J. Magill MRC Anatomical Neuropharmacology Unit Oxford United Kingdom

Library of Congress Control Number: 2005931829

ISBN-10: 0-387-28065-0 e-ISBN 0-387-28066-9 ISBN-13: 978-0387-28065-3

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987654321 springeronline.com INTERNATIONAL BASAL GANGLIA SOCIETY OFFICERS (2001–2004)

President J. Paul Bolam (England)

Past President Richard L.M. Faull (New Zealand)

President Elect Henk J. Groenewegen (The Netherlands)

Secretary Cali A. Ingham (Scotland)

Secretary Elect Henk Berendse (The Netherlands)

Treasurer Yoland Smith (USA)

Council Marianne Amalric (France) Gordon Arbuthnott (Scotland) Alan Crossman (England) Gaetano Di Chiara (Italy) Glenda Halliday (Australia) Katsuma Nakano (Japan) Louise F.B. Nicholson (New Zealand) Charles J Wilson (USA) IBAGS VIII The 8th Triennial Meeting of the International Basal Ganglia Society was held at the Crieff Hydro Hotel, Crieff, Scotland 5th–9th September 2004

President J. Paul Bolam Secretary Cali A. Ingham

Local Committee J. Paul Bolam Cali A. Ingham Peter J. Magill Gordon Arbuthnott

Scientific organising committee

J.P. Bolam C.A. Ingham G. Arbuthnott P. Emson P.J. Magill W. Schultz A. Crossman J. Tepper E. Abercrombie Y. Smith D. Brooks P. Redgrave T. Aziz

The following organisations are gratefully acknowledged for their financial assistance

AFFINITI Research Products, Kenneth and Ellen Aidekman, Alpha Omega Egineering, British Neuroscience Association, Cambridge Electronic Design Ltd, Crieff Hydro Hotel, Dalwhinnie Distillery, Eli Lilly & Co, Elsevier Ireland, Elsevier Life Science Marketing, GlaxoSmithKline, International Brain Research Organization, Medtronic Ltd, Novartis Institute for Biomedical Research Inc, Parkinson’s Disease Society (UK), PGRD Groton Laboratories, The Wellcome Trust. PREFACE

This volume, The Basal Ganglia VIII, is derived from the proceedings of the Eighth Triennial Meeting of the International Basal Ganglia Society (IBAGS). The meeting was held from 5th–9th September 2004 at the Crieff Hydro Hotel, Crieff, Scotland. Over 270 delegates from 16 countries (Argentina, Australia, Austria, Canada, Hong Kong, France, Germany, Israel, Italy, Japan, The Netherlands, New Zealand, Spain, Sweden, United Kingdom and USA) attended the meeting, and there were over 54 oral presentations and 186 poster presentations. In keeping with the traditions of IBAGS meetings inclusion of chapters in this book was open to all presenters. In the event, we have 59 contributions. The Scientific Organising Committee of the meeting had identified several themes of out- standing interest to the basal ganglia researcher and we are pleased to say that three of them, ‘Oscillations in the basal ganglia: The good, the bad and the unexpected’, ‘The ventral/dorsal divide: To integrate or separate’ and ‘Cholinergic mechanisms in the stria- tum’, are featured here. The remaining sections of the book do not necessarily reflect the sessions organised for the meeting, but rather, the chapters have been grouped according to more general research topics. Timed to coincide with the meeting were two special issues of Trends in Neurosciences, ‘Current Thinking in Basal Ganglia Research’, designed to highlight key issues in contemporary basal ganglia research. The triennial meetings of IBAGS are traditionally organised to enable young and (more) senior scientists to interact at both scientific and social levels, and we hope that the eighth meeting fulfilled this role. The beautiful Scottish setting of the meeting presented the ideal opportunity for delegates to exchange ideas on an informal basis, which variously included bracing countryside walks, ferocious ceilidh dancing, and plenty of whisky! A particularly pleasing event was the ‘opening lecture’ given by Oleh Hornykiewicz, who took us through forty years of dopamine research, thus enabling the younger scientists to put their work in an historical perspective. For his contributions to neuroscience, and in particular to dopamine research, he was elected as an Honorary Member of the society, as were Ann Graybiel and Anne Young for their long and continuing contributions to basal ganglia research. They join John McKenzie and Gerard Percheron, both long-standing honorary members. The next meeting will take place in The Netherlands in 2007 under the watchful eyes of ‘The Henks’, Henk Groenewegen and Henk Berendse. We all look forward to the ninth meeting with eager anticipation.

Paul Bolam, Cali Ingham and Pete Magill

vii Photos from the 8th Triennial Meeting of IBAGS (5th–9th September 2004, Crieff, Scotland). Upper left, one of the poster sessions. Top middle, lunch-time discussions. Top right, Oleh Hornykiewicz gives the “Opening Lecture”. Bottom left, Anne Young introduces Oleh Hornykiewicz. Bottom middle, the conference dinner. Bottom right, piping in the haggis. CONTENTS

SECTION I Oscillations in the Basal Ganglia

Oscillations in the Basal Ganglia: The Good, the Bad, and the Unexpected 3 Thomas Boraud, Peter Brown, Joshua A. Goldberg, Ann M. Graybiel, and Peter J. Magill

Participation of Striatal Neurons in Large-Scale Oscillatory Networks 25 Joshua D. Berke

Do Local Field Potentials Reflect Synchronized Spiking Activity of Neuronal Populations in the Basal Ganglia? Studies in a Rodent Model of Parkinson’s Disease 37 Judith R. Walters, Dan Hu, Christy A. Itoga, Louise C. Parr-Brownlie, and Debra A. Bergstrom

A Partial Spectra Method for Predicting Spike Correlations from Local Field Potentials: Application to MPTP Induced Synchronization 47 Joshua A. Goldberg and Hagai Bergman

Propagation of Cortical Paroxysms in Basal Ganglia Circuits During Absence Seizures 55 Jeanne T. Paz, Pierre-Olivier Polack, Seán J. Slaght, Jean-Michel Deniau, and Stéphane Charpier

Limitations of the Isolated GP-STN Network 65 Ian M. Stanford, Krim C. Loucif, Claire L. Wilson, Diana Cash, and Michael G. Lacey

ix x CONTENTS

SECTION II Cholinergic Mechanisms in the Striatum

Convergence and Plasticity of Inputs to Striatal Cholinergic Interneurons: The Generation of Synchronised Pauses 77 John N.J. Reynolds

Short and Long-Term Modulation of Synaptic Activity in Striatal Cholinergic Interneurons 91 Paola Bonsi, Massimo Tolu, Franco Lavaroni, Giorgio Bernardi, Paolo Calabresi, and Antonio Pisani

Striatal Acetylcholine Control of Reward-Related Dopamine Signalling 99 Stephanie J. Cragg, Richard Exley, and Michael A. Clements

Changes of Glutamatergic Control of Striatal Acetylcholine Release in Experimental Parkinsonism 109 Flora Mela, Matteo Marti, Clementina Bianchi, and Michele Morari

Peptidergic Regulation of Cholinergic Transmission in the Dorsal Striatum: Peptides and Acetylcholine in the Striatum 119 Marie-Louise Kemel, Maritza Jabourian, Sylvie Pérez, and Jacques Glowinski

SECTION III Pharmacological and Receptor Studies of the Basal Ganglia

Localization and Functions of Kainate Receptors in the Rat Globus Pallidus 131 Xiao-Tao Jin and Yoland Smith

Oligomerization of Dopamine D1 and Glutamate NMDA Receptors: A New Mechanism Regulating Striatal Function 141 Chiara Fiorentini, Chiara Busi, Sandra Bontempi, PierFranco Spano, and Cristina Missale

Modulatory Role of NK1 Receptors in the Basal Ganglia. Studies in NK1-/- Mice 151 Laura Turpín, Jorge Boronat, Carlos Barcia, María Gómez, Francisco Ros, Virginia García, Stephen P. Hunt, Carmen de Felipe, and María-Trinidad Herrero

Trace Amines Cause More Than One Effect on Dopaminergic Neurons 161 Raffaella Geracitano, Mauro Federici, Alessandro Tozzi, Patrizia Longone, Giorgio Bernardi, and Nicola B. Mercuri CONTENTS xi

Regulation of Dopamine Release and Dopamine Cell Activity by

Endogenous H2O2: Implications for Basal Ganglia Function 177 Margaret E. Rice, Jyoti Patel, Li Bao, Zsuzsanna S. Pearson, Pullani Shashidharan, Ruth H. Walker, Billy T. Chen, and Marat V.Avshalumov

Nociceptin/Orphanin FQ Modulates Neurotransmitter Release in the Substantia Nigra: Biochemical and Behavioural Outcome 187 Matteo Marti, Massimiliano Manzalini, Clementina Bianchi, Christian Heidbreder, Michele Morari, and Francesco Crespi

Motor Learning-Related Gene Regulation in the Striatum: Effects of Cocaine 197 Ingo Willuhn and Heinz Steiner

Opposing Short-Term and Long-Term Effects of Amphetamine Sensitization on Operant Responding For a Food Reinforcer 209 Rebecca E. Nordquist, Pieter Voorn, J.G. de Mooij-van Malsen, R.N.J.M.A. Joosten, Cyriel M.A. Pennartz, and Louk J.M.J. Vanderschuren

Anterograde Trophic Mechanisms Participate in Pattern Formation in the Striatum: A Role For BDNF in Glutamatergic Afferents 219 Abbas F. Sadikot, Kenneth Leung, Sandeep Mittal, Vladimir V. Rymar, Mario Alonso-Vanegas, and Kelvin C. Luk

Developmental Assembly of GABA Receptors in the Rat Substantia Nigra 229 Wai K. Lau, Wing H. Yung, Ying-Shing Chan, and Ken K.L. Yung

SECTION IV Disorders of Basal Ganglia Function I: Studies in Animal Models

High Frequency Stimulation of the Subthalamic Nucleus: Electrophysiological and Neurochemical Aspects 243 Nicolas Maurice, Jean-Michel Deniau, Bertrand Degos, François Windels, Carole Carcenac, Annie Poupard, and Marc Savasta

Downregulation of a Metabotropic Glutamate Receptor in the Parkinsonian Basal Ganglia 255 Masahiko Takada, Katsuyuki Kaneda, Yoshihisa Tachibana, Michiko Imanishi, Hitoshi Kita, Ryuichi Shigemoto, and Atsushi Nambu

Pitx3 is Necessary for Survival of Midbrain Dopaminergic Neuron Subsets Relevant to Parkinson’s Disease 265 Abbas F. Sadikot, Kelvin C. Luk, Pepijn van den Munckhof, Vladimir V. Rymar, Kenneth Leung, Rina Gandhi, and Jacques Drouin xii CONTENTS

D1-Dopamine Receptor Supersensitivity in the Dopamine-Depleted Striatum Involves a Novel Activation of Erk1/2 275 Charles R. Gerfen

Do Systemically Administered Glutamate Antagonists Affect Subthalamic Nucleus Activity? Relevance to Pharmacotherapy of Parkinson’s Disease 285 Kelly A. Allers, Debra A. Bergstrom, Leyla J. Ghazi, Deborah S. Kreiss, and Judith R. Walters

Striatopallidal Changes in Early Parkinson’s Disease: Partial Dopamine Depletions 295 Anne E. Grissell and Marjorie A. Ariano

Dynamic Model of Basal Ganglia Functions and Parkinson’s Disease 307 Atsushi Nambu, Yoshihisa Tachibana, Katsuyuki Kaneda, Hironobu Tokuno, and Masahiko Takada

Striatal Grafts and Synaptic Plasticity 313 David Mazzocchi-Jones, Máté Döbrössy, and Stephen Dunnett

Spontaneous Formation of Lewy Bodies in a Rodent 321 J. Nunan, A. Tsiotis-Vais, S. George, C.L. Parish, D.K. Grandy, D.I. Finkelstein, J. Drago, and M.K. Horne

Intralaminar Thalamic Nuclei are Main Regulators of Basal Ganglia Possible Involvement in the Pathophysiology of Parkinson’s Disease 331 Lydia Kerkerian-Le Goff, Jean-Jacques Bacci, Pascal Salin, Maria S. Aymerich, Pedro Barroso-Chinea, José A. Obeso, and José L. Lanciego

Activated Microglia Persist in the Substantia Nigra of a Chronic MPTP Mouse Model of Parkinson’s Disease 341 Gloria E. Meredith, Adrian G. Dervan, and Susan Totterdell

Early Behavioral Phenotypes in Mouse Models of Huntington’s and Parkinson’s Diseases 349 Marie-Francoise Chesselet, Miriam A. Hickey, Sheila M. Fleming, and Pierre-Olivier Fernagut

Synaptic Alterations in Genetic Mouse Models of Huntington’s and Parkinson’s Diseases: Is there a Common Thread? 361 Carlos Cepeda, Nanping Wu, Véronique M. André, and Michael S. Levine

Changes in the Expression of Tonic and Phasic Neurochemical Markers of Activity in a Rat Model of L-DOPA Induced Dyskinesia 371 Anna R. Carta, Annalisa Pinna, Elisabetta Tronci, and Micaela Morelli CONTENTS xiii

SECTION V Disorders of Basal Ganglia Function II: Clinical Studies

Bilateral Somatosensory Responses of Pallidal Neurons in Humans Studied with Microrecording 381 Chihiro Ohye, Tohru Shibazaki, and Sumito Sato

Alterations in Globus Pallidus Internus Firing Patterns are Associated with Different Movement Disorders 389 Joyce K.H. Tang, Neil Mahant, William D. Hutchison, Elena Moro, Andres M. Lozano, Anthony E. Lang, and Jonathan O. Dostrovsky

Biochemical Markers of DBS-Induced Transition from “Off” to “On” State in Parkinsonian Patients 397 Salvatore Galati, Antonio Pisani, Alessandro Stefani, Ernesto Fedele, Maurizio Raiteri, Olimpia Pepicelli, Giuseppe Gattoni, Giorgio Bernardi, Paolo Mazzone, and Paolo Stanzione

Effect of Deep Brain Stimulation on Tremor 407 Fusako Yokochi, Ryoichi Okiyama, Makoto Taniguchi, Hiroshi Takahashi, and Ikuma Hamada

Thalamic and Cortical Changes in Parkinsonian Disorders 415 Jasmine M. Henderson, Virginia Macdonald, and Glenda M. Halliday

Neurogenesis in the Basal Ganglia in Huntington’s Disease in the Human Brain and in an Animal Model 425 Maurice A. Curtis, Andrew S. Tattersfield, Monica Kam, Ellen B. Penney, Ryan J. Croon, Yin Wai Liu, Michael Dragunow, Richard L.M. Faull, and Bronwen Connor

SECTION VI Physiological and Anatomical Studies of the Functional Organisation of the Basal Ganglia

The Ventral/Dorsal Divide: To Integrate or Separate 437 Suzanne N. Haber, Jean-Michel Deniau, Henk J. Groenewegen, Patricio O’Donnell, Jacqueline F. McGinty, and Christelle Baunez

Feedforward and Feedback Inhibition in the Neostriatum 457 James M. Tepper, Tibor Koós, and Charles J. Wilson

Dopaminergic Modulation of Cortical and Striatal Up States 467 Kuei Y. Tseng and Patricio O’Donnell

Integration of Cortical Activity by Striatal Medium Spiny Neurons 475 Fernando Kasanetz and M. Gustavo Murer xiv CONTENTS

Activation of NOS Interneurones in Striatum after Excitotoxic Lesions of Rat Globus Pallidus 485 Matilde Lombardero Fernandez, Ann K. Wright, and Gordon W. Arbuthnott

Electrical Synapses between Output Neurones of the Striatum and between Neurones of the Substantia Nigra Pars Compacta 493 Marie Vandecasteele, Jean-Michel Deniau, Christian Giaume, Jacques Glowinski, and Laurent Venance

Nitric Oxide Signaling Modulates the Responsiveness of Striatal Medium Spiny Neurons to Electrical Stimulation of the Substantia Nigra: Striatal Nitrergic Signaling 503 Danting Liu, Stephen Sammut, and Anthony R. West

Chandelier Neuron Cartridges in the Rat Prefrontal Cortex Contact Pyramidal Neurons Which Project to the Nucleus Accumbens 513 Claire Hardwick, Sarah J. French, and Susan Totterdell

The Pedunculopontine and Reinforcement 523 Helen L. Alderson and Philip Winn

The Pedunculopontine Nucleus: Towards a Functional Integration with the Basal Ganglia 533 Juan Mena-Segovia, Hana M. Ross, Peter J. Magill, and J. Paul Bolam

Glutamatergic and GABAergic Control of Pallidal Activity in Monkeys 545 Hitoshi Kita, Yoshihisa Tachibana, and Atsushi Nambu

Combined Modeling and Extracellular Recording Studies of Up and Down Transitions of Neurons in Awake or Behaving Monkeys 555 Hiroshi Okamoto, Yoshikazu Isomura, Masahiko Takada, and Tomoki Fukai

Sequential Motor Behavior and the Basal Ganglia: Evidence from a Serial Reaction Time Task in Monkeys 563 Robert S. Turner, Kevin McCairn, Donn Simmons, and Izhar Bar-Gad

GABAergic and Dopaminergic Modulation of Basal Ganglia Output in Primates 575 Adriana Galvan, Michele A. Kliem, Yoland Smith, and Thomas Wichmann

The Basal Ganglia-Thalamocortical Circuit Originating in the Ventral Premotor Area (PMv) of the Macaque Monkey 585 K. Nakano, T. Kayahara, and E. Nagaoka CONTENTS xv

The Subthalamic Region of the Sheep 593 John S. McKenzie and Michael J. McKinley

Differential Localization of Vesicular Glutamate Transporters 1 and 2 in the Rat Striatum 601 Dinesh V. Raju and Yoland Smith

Local Connectivity between Neurons of the Rat Globus Pallidus 611 Ahmed-Ramadan Sadek, Peter J. Magill, and J. Paul Bolam

AUTHOR INDEX 621

SUBJECT INDEX 625