Memory Mechanisms in Health and Disease Downloaded from www.worldscientific.com by 37.44.207.67 on 01/28/17. For personal use only.

Memory Mechanisms in Health and Disease Mechanistic Basis of Memory

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Memory Mechanisms in Health and Disease Mechanistic Basis of Memory

Editor

Karl Peter Giese King’s College London, UK

World Scientific NEW JERSEY

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UK office: 57 Shelton Street, Covent Garden, London WC2H 9HE

British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library.

MEMORY MECHANISMS IN HEALTH AND DISEASE Mechanistic Basis of Memory Copyright © 2012 by World Scientific Publishing Co. Pte. Ltd. All rights reserved. This book, or parts thereof, may not be reproduced in any form or by any means, electronic or mechanical, including photocopying, recording or any information storage and retrieval system now known or to be invented, without written permission from the Publisher.

For photocopying of material in this volume, please pay a copying fee through the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, USA. In this case permission to photocopy is not required from the publisher.

ISBN-13 978-981-4366-69-4 ISBN-10 981-4366-69-2

Typeset by Stallion Press Email: [email protected]

Printed in Singapore.

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Contents

Contributing Authors

vii

Introduction Karl Peter Giese

xiii

Chapter 1:

Long-term Potentiation and Memory Karl Peter Giese

Chapter 2:

Structural Synaptic and Dendritic Spine Plasticity in the Hippocampus Michael G. Stewart, and Victor I. Popov

Chapter 3:

Memory Beyond Synaptic Plasticity: The Role of Intrinsic Neuronal Excitability Athanasia Papoutsi, Kyriaki Sidiropoulou and Panayiota Poirazi

Chapter 4:

Adult Hippocampal Neurogenesis and Memory Scellig S.D. Stone and Paul W. Frankland

Chapter 5:

Memory Consolidation and Its Underlying Mechanisms Cristina M. Alberini, Dhananjay Bambah-Mukku, and Dillon Y. Chen

Chapter 6:

The Role of CREB and CREB Co-activators in Memory Formation Melanie J. Sekeres, Derya Sargin, P. Joel Ross, and Sheena A. Josselyn

Chapter 7:

Sex Differences in Memory Formation Keiko Mizuno and Karl Peter Giese

Chapter 8

Neocortical Learning, Memory and Experience-dependent Plasticity Giorgia Albieri and Gerald T. Finnerty

Chapter 9:

Mechanisms of Memory Storage Kimberly Lackenby and Karl Peter Giese

1

19

53

81 147

171

195

213 235

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Memory Mechanisms in Health and Disease

Contents

Chapter 10:

Memory Reconsolidation and Extinction Satoshi Kida

249

Chapter 11:

Memory Circuits in Drosophila Katsuo Furukubo-Tokunaga, Zoe N. Ludlow and Frank Hirth

269

Chapter 12:

Memory Circuits in the Hippocampus Thomas J. McHugh

307

Chapter 13:

Impaired Memory Mechanisms in Mouse Models of Alzheimer’s Disease Masuo Ohno

Chapter 14:

Restoring Memory Deficits in Cognitive Diseases Andre Fischer

Chapter 15:

The Impact of Studies of Memory Mechanisms for Psychiatry Shahid H. Zaman

Index

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343 381

397

431

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Contributing Authors

Cristina M. Alberini Department of Neuroscience Department of Psychiatry Mount Sinai School of Medicine New York, NY 10029, USA E-mail: [email protected] Giorgia Albieri MRC Centre for Neurodegeneration Research King’s College London De Crespigny Park, London SE5 8AF, UK Dhananjay Bambah-Mukku Department of Neuroscience Mount Sinai School of Medicine New York, NY 10029, USA Dillon Y. Chen Department of Neuroscience Mount Sinai School of Medicine New York, NY 10029, USA Gerald T. Finnerty MRC Centre for Neurodegeneration Research King’s College London De Crespigny Park, London SE5 8AF, UK E-mail: [email protected] Andre Fischer Laboratory for Aging and Cognitive Diseases European Neuroscience Institute Grisebach Str. 5, D-37077 Goettingen, Germany E-mail: [email protected] vii

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Contributing Authors

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Paul W. Frankland Neurosciences & Mental Health The Hospital for Sick Children 555 University Ave., 6018 McMaster Building Toronto, Ontario, M5G 1X8, Canada E-mail: [email protected] Katsuo Furukubo-Tokunaga Department of Life and Environmental Sciences University of Tsukuba, Japan E-mail: [email protected] Karl Peter Giese Department of Neuroscience, Institute of Psychiatry King’s College London 125 Coldharbour Lane, London, SE5 9NU, UK E-mail: [email protected] Frank Hirth Department of Neuroscience MRC Centre for Neurodegeneration Research Institute of Psychiatry King’s College London De Crespigny Park, London SE5 8AF, UK Sheena A. Josselyn Program in Neurosciences & Mental Health Hospital for Sick Children 555 University Ave. Department of Physiology Institute of Medical Sciences University of Toronto Toronto, ON, M5G 1X8, Canada E-mail: [email protected]

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Contributing Authors

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Satoshi Kida Department of Bioscience Faculty of Applied Bioscience, Tokyo University of Agriculture 1-1-1 Sakuragaoka, Setagaya-ku, Tokyo 156-8502, Japan E-mail: [email protected] Kimberly Lackenby Department of Neuroscience Institute of Psychiatry,King’s College London 125 Coldharbour Lane, London, SE5 9NU, UK Zoe N. Ludlow Department of Neuroscience MRC Centre for Neurodegeneration Research Institute of Psychiatry King’s College London De Crespigny Park, London SE5 8AF, UK Thomas J. McHugh Laboratory for Circuit and Behavioural Physiology RIKEN Brain Science Institute 2-1 Hirosawa, Wako City, Saitama, 351-0198 Japan E-mail: [email protected] Keiko Mizuno Department of Neuroscience Institute of Psychiatry, King’s College London 125 Coldharbour Lane, London, SE5 9NU, UK E-mail: [email protected] Masuo Ohno Center for Dementia Research Nathan Kline Institute New York University School of Medicine Orangeburg, New York, USA E-mail: [email protected]

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Contributing Authors

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Athanasia Papoutsi Institute of Molecular Biology and Biotechnology (IMBB) Foundation for Research and Technology (FORTH) Department of Biology University of Crete Heraklion, Crete, Greece Panayiota Poirazi Institute of Molecular Biology and Biotechnology (IMBB) Foundation for Research and Technology (FORTH) Heraklion, Crete, Greece E-mail: [email protected] Victor I. Popov Institute of Cell Biophysics Russian Academy of Sciences Pushchino, Russia P. Joel Ross Program in Neurosciences & Mental Health Hospital for Sick Children 555 University Ave. Toronto, ON, M5G 1X8, Canada Derya Sargin Program in Neurosciences & Mental Health Hospital for Sick Children 555 University Ave. Toronto, ON, M5G 1X8, Canada Melanie J. Sekeres Program in Neurosciences & Mental Health Hospital for Sick Children 555 University Ave. Department of Physiology University of Toronto Toronto, ON, M5G 1X8, Canada

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Kyriaki Sidiropoulou Institute of Molecular Biology and Biotechnology (IMBB) Foundation for Research and Technology (FORTH) Department of Biology University of Crete Heraklion, Crete, Greece Michael G. Stewart Department of Life Sciences The Open University Milton Keynes, UK E-mail: [email protected] Scellig S.D. Stone Neurosciences & Mental Health The Hospital for Sick Children 555 University Ave., 6018 McMaster Building Toronto, Ontario, M5G 1X8, Canada Shahid H. Zaman Cambridge Intellectual & Developmental Disabilities Research Group Department of Developmental Psychiatry University of Cambridge Cambridge CB2 8AH, UK E-mail: shz10medschl.cam.ac.uk

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Introduction

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Karl Peter Giese*

Learning and memory are of fundamental importance for the survival of animals. Thus, it should be of no surprise that highly evolved animals, such as mammals, have very sophisticated memory mechanisms. Biomedical research in the last 40 years has provided many insights into memory mechanisms in normal, healthy conditions. More recent research has also begun to address how memory mechanisms are affected in memory disorders, such as Alzheimer’s disease. However, much more research is needed to develop a satisfactory understanding of memory mechanisms in health and disease. It is hoped that such mechanistic insights will ultimately lead to the development of “memory pills” to treat memory dysfunction. This book provides an overview of current highlights of mechanistic studies of memory and it addresses the clinical application of contemporary memory research. The book is suitable not only for final-year BSc Neuroscience, MSc Neuroscience and PhD students, but it also provides critical reviews for postdocs and PIs. Learning and memory are properties of a living brain and they are defined operationally at the behavioural level. Consequently, learning and memory cannot be studied in cell culture or brain slices. Such reduced preparations are suitable for the investigation of cellular mechanisms, which may or may not be relevant for learning and memory. Candidate mechanisms must be studied in behaving animals. Various behavioural tasks have been designed to study learning and memory. For example, the hidden-platform version of the Morris water maze (Morris, 1982, Nature 297, 681–683) and contextual fear conditioning (see Chapter 14) are widely used for studies of mechanisms in the hippocampus. Most learning and memory tasks are well explained in basic textbooks, so they are not described in detail in this book. For the mechanistic analysis of learning and memory, it is important to distinguish between processes. The following processes can be distinguished:

* King’s College London, Institute of Psychiatry, Department of Neuroscience, 125 Coldharbour Lane, London, SE5 9NU, UK. xiii

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Introduction

memory formation, memory storage, and memory retrieval. Memory formation consists of acquisition and consolidation. Furthermore, it is useful to distinguish between memory formation after one training trial and memory formation after repeated training trials, as the underlying mechanisms seem to differ (e.g. Irvine et al., 2006, Trends Neurosci 29, 459–465). Additionally, there are retrievalinduced processes, such as memory reconsolidation and memory extinction. The current mechanistic understanding is most advanced for memory formation,whilst not much is known about mechanisms underlying memory retrieval. Accordingly, in this book, we cover mainly mechanisms underlying memory formation (Chapters 1–8, 13, 14), but mechanisms of memory storage (Chapter 9) and retrieval-induced processes (Chapter 10) are also considered. In mammals, there are independent memory systems that require distinct brain areas. For example, memories for places require the hippocampus whilst motor skill memories are not affected by hippocampal loss. Thus, to develop an understanding of memory mechanisms, it is important to know what brain regions are relevant. The identification of relevant brain regions involves studies of engagement (e.g. using imaging approaches) and inactivation/lesion experiments to establish that the area of interest is required for memory formation and/or storage and/ or retrieval. This anatomical knowledge helps to define the neuronal circuitry which forms and stores particular memories. However, molecular and cellular studies are needed to address how these memories are formed and stored. Basic textbooks sufficiently describe distinct memory systems and their underlying anatomy so that this information is not presented much in this book here. However, Chapters 11 and 12 address contemporary ideas about memory circuits. The most widely investigated cellular mechanisms underlying memory formation is long-term potentiation (LTP), a long-lasting enhancement of transmission at a given synapse. Hence, the first chapter in this book is dedicated to the role of LTP in memory formation. This chapter aims to provide critical insights into studies of the role of LTP. Further chapters in this book are dedicated to other cellular mechanisms of memory that are less widely discussed, but that are still very important. These mechanisms include synaptogenesis (Chapter 2), rewiring of the connections between neurons (Chapter 8), changes in neuronal excitability (Chapter 3), and adult neurogenesis (Chapter 4). We discuss extensively molecular mechanisms underlying memory consolidation, some of which are sexdependent (Chapters 5–7). The molecular basis of memory storage is considered in Chapter 9. Learning and memory are not only impaired in Alzheimer’s disease, but are also affected in autism, bipolar disorder, depression, mental retardation, posttraumatic stress disorder and schizophrenia. The nature of these impairments

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Introduction

xv

is unclear. However, there are some insights into memory dysfunction in Alzheimer’s disease. This research is discussed in Chapter 13; Chapter 14 illustrates how these insights might be useful to develop treatments for patients with Alzheimer’s disease. Finally, Chapter 15 explains in more detail what impact knowledge of memory mechanisms is expected to have for psychiatry. I want to thank the following scientists who gave invaluable feedback that helped to shape this book: Drs. Ted Abel (Penn University, USA), Sam Cooke (MIT, USA), John Disterhoft (Northwestern University, USA), Diane Hanger (King’s College London, UK), Jonathan Lee (University of Birmingham, UK), Anna Need (Duke University, USA), Matthew Nolan (Edinburgh University, UK), Marco Peters (Darts Neuroscience, USA), Claire Rampon (University of Toulouse, France), Emilie Rissman (University of Virginia, USA), Todd Sacktor (SUNY Downstate Medical Center, USA), Miao-Kun Sun (Blanchette Rockefeller Neuroscience Institute, USA), Jeffrey Vernon (University College London, UK), and Marcelo Wood (University of California Irvine, USA).

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