Science of Memory Concepts, 1st Edition

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Science of Memory:
Concepts
Edited by

Henry L. Roediger III

James S. McDonnell Distinguished University Professor
at Washington University in St. Louis

Yadin Dudai
Sela Professor of Neurobiology at the Weizmann Institute
of Science, Rehovot, Israel

and

Susan M. Fitzpatrick
Vice President of the James S. McDonnell Foundation

1
1
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Copyright (©) 2007 by Henry L. Roediger III,
Yadin Dudai, and Susan M. Fitzpatrick.
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All rights reserved. No part of this publication may be reproduced,
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Library of Congress Cataloging-in-Publication Data
Science of memory: concepts / [edited by] Henry L. Roediger III, Yadin Dudai, and Susan M. Fitzpatrick.
p. cm. -- (Science of memory)
Includes bibliographical references and index.
ISBN-13: 978-0-19-531044-3 (pbk.)
1. Memory. I. Roediger, Henry L. II. Dudai, Yadin. III. Fitzpatrick, Susan M., 1956-
BF371.S45 2007
153.1′2--dc22
2006029621
Typeset in Minion by
Cepha Imaging Private Ltd., Bangalore, India
Printed in Great Britain
on acid-free paper by Ashford Colour Press Ltd., Gosport, Hampshire
10 9 8 7 6 5 4 3 2 1
 Contents

Preface xi
Acknowledgments xiii
Contributors xv

1 Memory concepts 1
Yadin Dudai, Henry L. Roediger III and Endel Tulving

1. Memory
2 Memory: It’s all about representations 13
Yadin Dudai
3 Memory: Why the engram is elusive 17
Morris Moscovitch
4 Memory: Delineating the core 23
Daniel L. Schacter
5 Integrative comments:
Memory: Distinctions and dilemmas 29
Richard G.M. Morris

2. Learning
6 Learning: A pre-theoretical concept 37
Robert A. Rescorla
7 Learning: The need for a hybrid theory 41
Anthony Dickinson
8 Learning: Challanges in the merging of levels 45
Elizabeth A. Phelps
9 Integrative comments:
Learning: Multiplicity of mechanisms 49
Steve E. Petersen
vi CONTENTS

3. Coding and representation

10 Coding and representation: Time, space, history and beyond 55
Alessandro Treves
11 Coding and representation: The importance of mesoscale
dynamics 59
Anthony R. McIntosh
12 Coding and representation: Searching for a home in
the brain 65
Endel Tulving
13 Integrative comments:
Coding and representation: On appealing beliefs and
paucity of data 69
Misha Tsodyks

4. Plasticity
14 Plasticity: New concepts, new challenges 77
John H. Byrne
15 Plasticity: A pragmatic compromise 83
Chris I. De Zeeuw
16 Plasticity: On the level 87
John T. Bruer
17 Integrative comments:
Plasticity: More than memory 93
Edvard I. Moser

5. Context
18 Context: What’s so special about it? 101
Michael S. Fanselow
19 Context: Mood, memory, and the concept of context 107
Eric Eich
20 Context: A reference for focal experience 111
Steven M. Smith
21 Integrative comments:
Context: The concept in the human and animal memory
domains 115
Mark E. Bouton
 CONTENTS vii

6. Encoding
22 Encoding: Models linking neural mechanisms to behavior 123
Michael E. Hasselmo
23 Encoding: A cognitive perspective 129
Fergus I.M. Craik
24 Integrative comments:
Encoding: The proof is still required 137
Lila Davachi

7. Working memory
25 Working memory: Signals in the brain 147
Wendy A. Suzuki
26 Working memory: Multiple models, multiple mechanisms 151
Alan Baddeley
27 Working memory: What it is, and what it is not 155
Susan E. Gathercole
28 Integrative comments:
Working memory: The mind is richer than the models 159
Randall W. Engle

8. Consolidation
29 Consolidation: Molecular restlessness 167
Alcino J. Silva
30 Consolidation: Challenging the traditional view 171
Joseph E. LeDoux
31 Consolidation: The demise of the fixed trace 177
Lynn Nadel
32 Integrative comments:
Consolidation: From hypothesis to paradigm to concept 183
Susan J. Sara

9. Persistence
33 Persistence: Necessary, but not sufficient 193
Howard Eichenbaum
34 Persistence: Discrepancies between behaviors and brains 199
Richard F. Thompson
viii CONTENTS

35 Integrative comments:
Persistence: In search of molecular persistence 203
John E. Lisman

10. Retrieval
36 Retrieval: Molecular mechanisms 209
J. David Sweatt
37 Retrieval: Properties and effects 215
Norman E. Spear
38 Retrieval: On its essence and related concepts 221
John M. Gardiner
39 Integrative comments:
Retrieval: Varieties and puzzles 225
Kathleen B. McDermott

11. Remembering
40 Remembering: Defining and measuring 233
Andrew P. Yonelinas
41 Remembering: A process and a state 237
Martin A. Conway
42 Remembering: Metacognitive monitoring and control processes 243
Asher Koriat
43 Integrative comments:
Remembering: A controversy and a challenge 247
Suparna Rajaram

12. Transfer
44 Transfer: Its transfer into neurobiology 255
Yadin Dudai
45 Transfer: Analysis in rats and other species 261
E.J. Capaldi
46 Transfer: Rediscovering a central concept 267
Mark A. McDaniel
47 Transfer: Specificity and generality 271
Alice F. Healy
48 Integrative comments:
Transfer: The ubiquitous concept 277
Henry L. Roediger III
 CONTENTS ix

13. Inhibition
49 Inhibition: Diversity of cortical functions 285
György Buzsáki
50 Inhibition: Attentional regulation of cognition 291
Lynn Hasher
51 Inhibition: Manifestations in long-term memory 295
Michael C. Anderson
52 Inhibition: Elusive or illusion? 301
Colin M. MacLeod
53 Integrative comments:
Inhibition: An essential and contentious concept 307
Robert A. Bjork

14. Forgetting
54 Forgetting: Once again, it’s all about representations 317
Michael Davis
55 Forgetting: The fate of once learned, but “forgotten”, material 321
Elizabeth F. Loftus
56 Forgetting: Its role in the science of memory 325
David C. Rubin
57 Integrative comments:
Forgetting: It’s not just the opposite of remembering 329
John T. Wixted

15. Memory systems

58 Memory systems: A biological concept 339
Larry R. Squire
59 Memory systems: Multiple systems in the brain and their
interactions 345
Edmund T. Rolls
60 Memory systems: A cognitive construct for analysis
and synthesis 353
Marcia K. Johnson
61 Integrative comments:
Memory systems: An incentive, not an endpoint 359
Randy L. Buckner
x CONTENTS

16. Phylogeny and evolution

62 Phylogeny and evolution: It takes two to tango 367
Nicola S. Clayton
63 Phylogeny and evolution: On comparing species at multiple levels
371
Randolf Menzel
64 Phylogeny and evolution: Implications for understanding the
nature of a memory system 377
Stanley B. Klein
65 Integrative comments:
Phylogeny and evolution: Ecology, evolutionary biology, and the
science of memory 383
Sara J. Shettleworth

Epilogue
66 Remember the future 391
Susan M. Fitzpatrick
References 397
Author index 431
Subject index 437
 Preface

Memory is a single term, but with manifold referents. A huge variety of adjec-
tives has been used to modify this noun, so that scholars discuss everything
from abstract memory to zebrafish memory. Many different approaches to
studying memory have arisen, both humanistic and scientific. Even among
scientists who study memory, various methods and lines of attack are used:
there are fields devoted to the biochemical, neurobiological, systems neuro-
scientific, computational and cognitive psychological approaches to studying
memory, among others. Each field has its own techniques, methods, experi-
mental preparations and special theories. What, if anything, holds the entire
enterprise together? Can we develop a unified science of memory? The Science
of Memory: Concepts is based on the assumption that the answer to the second
question is yes. Further, we assume that at least part of the answer to the first
question is concepts. That is, we believe that cross-disciplinary understanding
of key concepts represent a critical element in developing a unified science of
memory.
This volume was developed around 16 core concepts of the science of mem-
ory, those listed in the Table of Contents on the preceding pages. Each of these
concepts was selected for a particular reason and the choices were difficult.
Other perfectly plausible candidate concepts exist that we did not include (e.g.
reinforcement). The introductory chapter by Dudai, Roediger and Tulving on
Memory concepts explains and defends our choices. In her concluding chapter,
Remember the future, Fitzpatrick explains the origin of the enterprise repre-
sented in this volume.
Following the introductory chapter on Memory concepts, the book is divided
into 16 sections, one for each concept. Each section is organized so that a brief
defining statement about a concept appears on the first page and then
2–4 short essays about the concept occur next. Authors of each essay were
instructed to provide their perspectives on the topic at hand; the essays were
their personal testaments, without worrying about satisfying all points of view.
The essays are brief, so authors get to the point. We tried to get researchers
from different corners of the field to write about the same topic, so even essays
on the same subject are heterogeneous. At the end of each section, an integrator
was given a bit more space to write an essay assimilating the various viewpoints.
xii PREFACE

As much as possible, the integrator provided a capstone summary of current

understanding of the particular concept for the science of memory.
One primary purpose of this volume is to inform scientists in the various
scientific subdisciplines studying memory of the many valid (if multifarious)
approaches to their topic. The hope is for all of us to think across our tradi-
tional disciplinary boundaries, under the assumption that doing so will enrich
the research we conduct within our own traditions.
We hope this book will be read by all researchers interested in scientific
approaches to memory. We believe it should be especially useful to graduate
students, postdoctoral fellows and young professors getting their start. Many
great new discoveries in science have come from a melding of methods or
viewpoints, by combining across fields. If this volume leads to some new dis-
coveries of this ilk, the book will be a success.
Henry L. Roediger III
Yadin Dudai
Susan M. Fitzpatrick
 Acknowledgments

This volume represents the work of many more people than the three listed on
the title page as editors. Endel Tulving was a guiding force throughout, from
the initial conception to the final product, and his spirit moved the enterprise
along at critical steps over the past several years. The editors thank him for his
inspiration, insight and sage advice. The James S. McDonnell Foundation gen-
erously provided funding for discussion of the issues covered in this volume at
a conference in Palisades, New York. The present book in no way presents a
‘conference proceedings’ volume, but the conference did enlighten and guide
authors of the essays contained in this volume. We would especially like to
thank Alene Roth and Brent Dolezalek of the McDonnell Foundation for their
enthusiastic and dedicated efforts that kept all the bits and pieces of the project
moving forward toward timely completion. Alene took on a lioness’s share of
the logistical tasks including the all important reminding, prodding and cajoling
that authors require to get essays submitted in a timely fashion. Brent, the JSMF
web-master, worked quietly behind the scenes so that all web-based electronic
transfer of information occurred seamlessly. This volume could not have met
its ambitious publication deadlines without his help. Jane McConnell of
Washington University provided many services at various points along the
way. Catherine Carlin of Oxford University Press first believed in our project
and helped us get started. Angela Burke copyedited the entire manuscript
and helped to even out style differences among contributors. We also thank
Jane Ashley for providing the subject and author indexes, and Helen Hill for
shepherding us through the production process. Finally, we thank all the
authors whose essays are contained here. Some thought our guidelines and
deadlines were impossible to meet, but almost everyone cooperated in a spirit
of adventure for this new kind of project. We thank everyone for helping to
produce this book.
Henry L. Roediger III
Yadin Dudai
Susan M. Fitzpatrick
The art on the cover is a painting by Ruth Tulving entitled HERA #2 and was
completed in 1994. HERA stands for Hemispheric Encoding and Retrieval
Asymmetry, a theroy of Endel Tulving and his collaborators on neural bases of
memory encoding and retrieval.
 Contributors

Michael C. Anderson Nicola S. Clayton

Department of Psychology, Department of Experimental
University of Oregon, USA Psychology, University of
Alan Baddeley Cambridge, UK
Department of Psychology, Martin A. Conway
University of York, UK Institute of Psychological Sciences,
Robert A. Bjork University of Leeds, UK
Department of Psychology, Fergus I.M. Craik
University of California, Rotman Research Institute–Baycrest
Los Angeles, USA Centre, University of Toronto, Canada
Mark E. Bouton Lila Davachi
Department of Psychology, Department of Psychology and
University of Vermont, USA Center for Neural Science, New York
John T. Bruer University, USA
James S. McDonnell Foundation, Michael Davis
USA Department of Psychiatry and
Randy L. Buckner Behavioral Sciences, Emory
Department of Psychology, University, USA
Harvard University, USA Chris I. De Zeeuw
György Buzsáki Department of Neuroscience, Erasmus
Center for Molecular and Medical Center, The Netherlands
Behavioral Neuroscience, Anthony Dickinson
Rutgers University, USA Department of Experimental
John H. Byrne Psychology, University of
Department of Neurobiology Cambridge, UK
and Anatomy, The University of Yadin Dudai
Texas Medical School at Houston, Department of Neurobiology,
USA Weizmann Institute, Israel
E.J. Capaldi Eric Eich
Department of Psychological Department of Psychology, University
Sciences, Purdue University, USA of British Columbia, Canada
xvi CONTRIBUTORS

Howard Eichenbaum Asher Koriat

Department of Psychology, Boston Department of Psychology,
University, USA University of Haifa, Israel
Randall W. Engle Joseph E. LeDoux
School of Psychology, Georgia Center for Neural Science,
Institute of Technology, USA New York University, USA
Michael S. Fanselow John E. Lisman
Department of Psychology, Biology Department & The
University of California, Benjamin and Mae Volen National
Los Angeles, USA Center for Complex Systems,
Susan M. Fitzpatrick Brandeis University, USA
James S. McDonnell Foundation, Elizabeth F. Loftus
USA Department of Psychology & Social
John M. Gardiner Behavior, University of California,
Department of Psychology, Irvine, USA
University of Sussex, UK Mark A. McDaniel
Susan E. Gathercole Department of Psychology,
Department of Psychology, Washington University in St. Louis,
University of York, UK USA

Lynn Hasher Kathleen B. McDermott

Department of Psychology, Department of Psychology,
University of Toronto, Canada Washington University in St. Louis,
USA
Michael E. Hasselmo
Department of Psychology, Anthony R. McIntosh
Boston University, USA Rotman Research Institute–Baycrest
Centre, University of Toronto, Canada
Alice F. Healy
Department of Psychology, Colin M. MacLeod
University of Colorado at Boulder Department of Psychology,
USA University of Waterloo, Canada

Marcia K. Johnson Randolf Menzel

Department of Psychology, Institute for Biology–Neurobiology,
Yale University, USA Free University of Berlin, Germany

Stanley B. Klein Richard G.M. Morris

Department of Psychology, College of Medicine and
University of California, Santa Veterinary Medicine,
Barbara, USA University of Edinburgh, UK
 CONTRIBUTORS xvii

Morris Moscovitch Daniel L. Schacter

Department of Psychology, Department of Psychology,
University of Toronto, Canada Harvard University, USA
Edvard I. Moser Sara J. Shettleworth
Center for the Biology of Memory, Department of Psychology,
Norwegian University of Science and University of Toronto, Canada
Technology, Norway Alcino J. Silva
Lynn Nadel Department of Neurobiology,
Department of Psychology, Psychiatry and Psychology and Brain
University of Arizona, USA Research Institute, University of
Steve E. Petersen California, Los Angeles, USA
Department of Neurology and Steven M. Smith
Neurological Surgery, Washington Department of Psychology,
University School of Medicine, USA Texas A&M University, USA
Elizabeth A. Phelps Norman E. Spear
Department of Psychology, Department of Psychology,
New York University, USA Binghamton University–SUNY, USA
Suparna Rajaram Larry R. Squire
Department of Psychology, Veterans Affairs Medical Center
Stony Brook University, USA and University of California,
Robert A. Rescorla San Diego, USA
Department of Psychology, Wendy A. Suzuki
University of Pennsylvania, USA Center for Neural Science,
Henry L. Roediger III New York University, USA
Department of Psychology, J. David Sweatt
Washington University in St. Louis, Department of Neurobiology,
USA University of Alabama,
Edmund T. Rolls Birmingham–Evelyn F. McKnight
Department of Experimental Brain Institute, USA
Psychology, University of Oxford, UK Richard F. Thompson
David C. Rubin Neuroscience Program, University
Department of Psychology and of Southern California, USA
Neuroscience, Duke University, USA Alessandro Treves
Susan J. Sara Sector of Cognitive Neuroscience,
Neuromodulation, Neural Plasticity International School for Advanced
and Cognition, Pierre & Marie Curie Studies, Italy
University, France
xviii CONTRIBUTORS

Misha Tsodyks John T. Wixted

Department of Neurobiology, Department of Psychology, University
Weizmann Institute, Israel of California, San Diego, USA
Endel Tulving Andrew P. Yonelinas
Rotman Research Institute, Department of Psychology,
University of Toronto, Canada University of California, Davis, USA