cognitive neuroscience of memory

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Cambridge University Press 978-1-107-08435-3 — Cognitive Neuroscience of Memory Scott D. Slotnick Frontmatter More Information www.cambridge.org © in this web service Cambridge University Press Cognitive Neuroscience of Memory Within the last two decades, the eld of cognitive neuroscience has begun to thrive with technological advances that non-invasively measure human brain activity. This is the rst book to provide a comprehensive and up-to-date treatment on the cognitive neuroscience of memory. Topics include cognitive neuroscience techniques and human brain mechanisms underlying long-term memory success, long-term memory failure, working memory, implicit mem- ory, and memory and disease. Cognitive Neuroscience of Memory highlights both spatial and temporal aspects of the functioning human brain during memory. Each chapter is written in an accessible style and includes background information and many gures. In his analysis, Scott Slotnick questions popular views, rather than simply assuming they are correct. In this way, science is depicted as open to question, evolving, and exciting. Scott D. Slotnick is an Associate Professor of Psychology at Boston College, Editor-in-Chief of the journal Cognitive Neuroscience, and author of the book Controversies in Cognitive Neuroscience. He employs multiple cogni- tive neuroscience techniques to investigate the brain mechanisms underlying memory including functional magnetic resonance imaging (fMRI), electro- encephalography (EEG), and transcranial magnetic stimulation (TMS).

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Page 1: Cognitive Neuroscience of Memory

Cambridge University Press978-1-107-08435-3 — Cognitive Neuroscience of MemoryScott D. Slotnick FrontmatterMore Information

www.cambridge.org© in this web service Cambridge University Press

Cognitive Neuroscience of Memory

Within the last two decades, the field of cognitive neuroscience has begun to

thrive with technological advances that non-invasively measure human brain

activity. This is the first book to provide a comprehensive and up-to-date

treatment on the cognitive neuroscience of memory. Topics include cognitive

neuroscience techniques and human brain mechanisms underlying long-term

memory success, long-term memory failure, working memory, implicit mem-

ory, and memory and disease. Cognitive Neuroscience of Memory highlights

both spatial and temporal aspects of the functioning human brain during

memory. Each chapter is written in an accessible style and includes background

information and many figures. In his analysis, Scott Slotnick questions popular

views, rather than simply assuming they are correct. In this way, science is

depicted as open to question, evolving, and exciting.

Scott D. Slotnick is an Associate Professor of Psychology at Boston College,

Editor-in-Chief of the journal Cognitive Neuroscience, and author of the

book Controversies in Cognitive Neuroscience. He employs multiple cogni-

tive neuroscience techniques to investigate the brain mechanisms underlying

memory including functional magnetic resonance imaging (fMRI), electro-

encephalography (EEG), and transcranial magnetic stimulation (TMS).

Page 2: Cognitive Neuroscience of Memory

Cambridge University Press978-1-107-08435-3 — Cognitive Neuroscience of MemoryScott D. Slotnick FrontmatterMore Information

www.cambridge.org© in this web service Cambridge University Press

Cambridge Fundamentals of Neuroscience in Psychology

Developed in response to a growing need to make neuroscience acces-sible to students and other non-specialist readers, the Cambridge

Fundamentals of Neuroscience in Psychology series provides brief intro-ductions to key areas of neuroscience research across major domains ofpsychology. Written by experts in cognitive, social, affective, develop-mental, clinical, and applied neuroscience, these books will serve as idealprimers for students and other readers seeking an entry point to thechallenging world of neuroscience.

Forthcoming Titles in the Series

The Neuroscience of Intelligence, by Richard J. HaierThe Neuroscience of Expertise, by Merim BilalićThe Neuroscience of Adolescence, by Adriana GalvánThe Neuroscience of Aging, by Angela GutchessThe Neuroscience of Addiction, by Francesca Filbey

Page 3: Cognitive Neuroscience of Memory

Cambridge University Press978-1-107-08435-3 — Cognitive Neuroscience of MemoryScott D. Slotnick FrontmatterMore Information

www.cambridge.org© in this web service Cambridge University Press

Cognitive Neuroscience

of Memory

Scott D. SlotnickBoston College

Page 4: Cognitive Neuroscience of Memory

Cambridge University Press978-1-107-08435-3 — Cognitive Neuroscience of MemoryScott D. Slotnick FrontmatterMore Information

www.cambridge.org© in this web service Cambridge University Press

University Printing House, Cambridge CB2 8BS, United Kingdom

One Liberty Plaza, 20th Floor, New York, NY 10006, USA

477 Williamstown Road, Port Melbourne, VIC 3207, Australia

4843/24, 2nd Floor, Ansari Road, Daryaganj, Delhi – 110002, India

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Cambridge University Press is part of the University of Cambridge.

It furthers the University’s mission by disseminating knowledge in the pursuit ofeducation, learning, and research at the highest international levels of excellence.

www.cambridge.orgInformation on this title: www.cambridge.org/978110708435310.1017/9781316026687

© Scott D. Slotnick 2017

This publication is in copyright. Subject to statutory exceptionand to the provisions of relevant collective licensing agreements,no reproduction of any part may take place without the writtenpermission of Cambridge University Press.

First published 2017

Printed in the United States of America by Sheridan Books, Inc.

A catalogue record for this publication is available from the British Library.

Library of Congress Cataloging in Publication DataNames: Slotnick, Scott D.Title: Cognitive neuroscience of memory / Scott D. Slotnick, Boston College.Description: Cambridge : Cambridge University Press, 2016. | Includes index.Identifiers: LCCN 2016049342 | ISBN 9781107084353Subjects: LCSH:Memory. | Memory – Physiological aspects. | Cognitive neuroscience.Classification: LCC QP406 .S5945 2016 | DDC 612.8/23312–dc23LC record available at https://lccn.loc.gov/2016049342

ISBN 978-1-107-08435-3 HardbackISBN 978-1-107-44626-7 Paperback

Cambridge University Press has no responsibility for the persistence or accuracy ofURLs for external or third-party internet websites referred to in this publicationand does not guarantee that any content on such websites is, or will remain,accurate or appropriate.

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Cambridge University Press978-1-107-08435-3 — Cognitive Neuroscience of MemoryScott D. Slotnick FrontmatterMore Information

www.cambridge.org© in this web service Cambridge University Press

This book is dedicated to my incredible daughter Sonya, fordominating my hippocampal sharp-wave ripples these pasttwelve years

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Cambridge University Press978-1-107-08435-3 — Cognitive Neuroscience of MemoryScott D. Slotnick FrontmatterMore Information

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As regards the question . . . what memory or remembering is . . . it is the state of

a presentation, related as a likeness to that of which it is a presentation; and as to the

question of which of the faculties within us memory is a function . . . it is a function of the

primary faculty of sense-perception, i.e. of that faculty whereby we perceive time.

(Aristotle, [350 BCE] 1941, p. 611)

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Contents

List of Figures page xPreface xxi

1 Types of Memory and Brain Regions of Interest 1

1.1 Cognitive Neuroscience 2

1.2 Memory Types 3

1.3 Brain Anatomy 8

1.4 The Hippocampus and Long-Term Memory 12

1.5 Sensory Regions 13

1.6 Control Regions 18

1.7 The Organization of This Book 21

2 The Tools of Cognitive Neuroscience 24

2.1 Behavioral Measures 25

2.2 High Spatial Resolution Techniques 25

2.3 High Temporal Resolution Techniques 30

2.4 High Spatial and Temporal Resolution Techniques 34

2.5 Lesions and Temporary Cortical Disruption

Techniques 37

2.6 Method Comparisons 43

3 Brain Regions Associated with Long-Term Memory 46

3.1 Episodic Memory 47

3.2 Semantic Memory 51

3.3 Memory Consolidation 53

3.4 Consolidation and Sleep 56

3.5 Memory Encoding 59

3.6 Sex Differences 61

3.7 Superior Memory 64

4 Brain Timing Associated with Long-Term Memory 71

4.1 Timing of Activity 72

4.2 The FN400 Debate 76

4.3 Phase and Frequency of Activity 79

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5 Long-Term Memory Failure 88

5.1 Typical Forgetting 89

5.2 Retrieval-Induced Forgetting 92

5.3 Motivated Forgetting 96

5.4 False Memories 97

5.5 Flashbulb Memories 103

6 Working Memory 108

6.1 The Contents of Working Memory 109

6.2 Working Memory and the Hippocampus 114

6.3 Working Memory and Brain Frequencies 119

6.4 Brain Plasticity and Working Memory Training 122

7 Implicit Memory 129

7.1 Brain Regions Associated with Implicit Memory 130

7.2 Brain Timing Associated with Implicit Memory 135

7.3 Models of Implicit Memory 138

7.4 Implicit Memory and the Hippocampus 141

7.5 Skill Learning 146

8 Memory and Other Cognitive Processes 150

8.1 Attention and Memory 151

8.2 Imagery and Memory 159

8.3 Language and Memory 164

8.4 Emotion and Memory 166

9 Explicit Memory and Disease 171

9.1 Amnestic Mild Cognitive Impairment 172

9.2 Alzheimer’s Disease 177

9.3 Mild Traumatic Brain Injury 179

9.4 Medial Temporal Lobe Epilepsy 186

9.5 Transient Global Amnesia 190

10 Long-Term Memory in Animals 196

10.1 The Medial Temporal Lobe 197

10.2 Long-Term Potentiation 200

10.3 Memory Replay 203

10.4 Time Cells 205

10.5 Episodic Memory 210

viii Contents

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11 The Future of Memory Research 219

11.1 Phrenology and fMRI 220

11.2 fMRI versus ERPs 225

11.3 Brain Region Interactions 227

11.4 The Future of Cognitive Neuroscience 232

11.5 A Spotlight on the Fourth Dimension 234

Glossary 238References 248Author Index 270Subject Index 276

Color plates are to be found between pp. 170 and 171

Contents ix

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Figures

1.1 The relationships between the fields of cognitive psychology,cognitive neuroscience, and behavioral neuroscience. page 2

1.2 Organization of memory types. 31.3 Probability of “remember” or “know” responses as a function

of confidence judgments. 81.4 Brain regions associated with memory. 91.5 Gyri and sulci in brain regions of interest. 101.6 Brodmann map. 111.7 Depiction of medial temporal lobe resection in patient H. M.

Reproduced from Journal of Neurology, Neurosurgery, &

Psychiatry, Loss of recent memory after bilateral hippocampallesions, William Beecher Scoville and Brenda Milner, Volume20, Pages 11–21, Copyright (1957), with permission from BMJPublishing Group Ltd. 13

1.8 Sensory brain regions of interest. 141.9 Sensory fMRI activity associated with perception andmemory. 17

1.10 Item memory and source memory paradigm and fMRI results.Reprinted from Cognitive Brain Research, Volume 17, ScottD. Slotnick, Lauren R. Moo, Jessica B. Segal, and John Hart,Jr., Distinct prefrontal cortex activity associated with itemmemory and source memory for visual shapes, Pages 75–82,Copyright (2003), with permission from Elsevier. 19

2.1 MRI scanner and fMRI results. (A) Photo courtesy of PrestonThakral. (B, C) Reprinted from Proceedings of the National

Academy of Sciences of the United States of America,Volume 93, Randy L. Buckner, Peter A. Bandettini,Kathleen M. O’Craven, Robert L. Savoy, Steven E. Petersen,Marcus E. Raichle, and Bruce R. Rosen, Detection of corticalactivation during averaged single trials of a cognitive task usingfunctional magnetic resonance imaging, Pages 14878–14883,Copyright (1996) National Academy of Sciences, USA. 27

2.2 ERP setup and results. (A) Photo courtesy of Scott Slotnick.Reprinted from NeuroImage, Volume 39, Jeffrey D. Johnson,Brian R. Minton, and Michael D. Rugg, Content dependence

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of the electrophysiological correlates of recollection, Pages406–416, Copyright (2008), with permission from Elsevier. 31

2.3 MEG setup. Photo courtesy of CTFMEG/MEG InternationalServices Ltd., Canada. 33

2.4 Hippocampal depth electrode placement and results.Reprinted from Proceedings of the National Academy of

Sciences of the United States of America, Volume 112, NanthiaA. Suthana, Neelroop N. Parikshak, Arne D. Ekstrom, MatiasJ. Ison, Barbara J. Knowlton, Susan Y. Bookheimer, andItzhak Fried, Specific responses of human hippocampalneurons are associated with better memory, Pages10503–10508, Copyright (2015) National Academy of Sciences,USA. 36

2.5 Hippocampal lesion and recognition memory results.Reprinted from Neuron, Volume 37, Joseph R. Manns,Ramona O. Hopkins, Jonathan M. Reed, Erin G. Kitchener,and Larry R. Squire, Recognition memory and the humanhippocampus, Pages 171–180, Copyright (2003), withpermission from Elsevier. 38

2.6 TMS setup and fMRI guided TMS results. (A, B) Photoscourtesy of Scott Slotnick. Reprinted from NeuroImage,Volume 55, Scott D. Slotnick and Preston P. Thakral, Memoryformotion and spatial location is mediated by contralateral andipsiliateral motion processing cortex, Pages 794–800, Copyright(2011), with permission from Elsevier. 40

2.7 tDCS setup. Photo courtesy of Bryan Coppede. 422.8 Spatial resolution and temporal resolution for different

methods. 433.1 Regions of the brain associated with episodic memory.

Reprinted from Current Opinion in Neurobiology,Volume 23(2), Michael D. Rugg and Kaia L. Vilberg, Brainnetworks underlying episodic memory retrieval, Pages255–260, Copyright (2013), with permission from Elsevier. 48

3.2 Model of medial temporal lobe sub-region function. Reprintedfrom NeuroReport, Volume 24(12), Scott D. Slotnick,The nature of recollection in behavior and the brain, Pages663–670, Copyright (2013), with permission from WoltersKluwer. 49

3.3 Regions of the brain associatedwith semanticmemory.Reprintedfrom Neuroimage, Volume 63(1), Kimiko Domoto-Reilly, DaisySapolsky, Michael Brickhouse, and Bradford C. Dickerson,

List of Figures xi

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Naming Impairment in Alzheimer’s disease is associatedwith left anterior temporal lobe atrophy, Pages 348–355,Copyright (2012), with permission from Elsevier. 52

3.4 Autobiographical memory disruption for recent and remoteevents in patients with hippocampal lesions. Reprinted fromProceedings of the National Academy of Sciences of the United

States of America, Volume 108, Thorsten Bartsch, JulianeDöhring, Axel Rohr, Olav Jansen, and Günther Deuschl, CA1neurons in the human hippocampus are critical forautobiographical memory, mental time travel, and autonoeticconsciousness, Pages 17562–17567, Copyright (2011) NationalAcademy of Sciences, USA. 55

3.5 Sleep stages and brain oscillations associated with slow wavesleep and long-term memory consolidation. (A) Reprintedfrom Trends in Neurosciences, Volume 28(8), Robert Stickgoldand Matthew P. Walker, Memory consolidation andreconsolidation: What is the role of sleep, Pages 408–415,Copyright (2005), with permission fromElsevier. (B)Reprintedfrom Psychological Research, Volume 76(2), Jan Born andInes Wilhelm, System consolidation of memory during sleep,Pages 192–203, Copyright (2012), with permission fromSpringer. 57

3.6 Regions of the brain associated with subsequent memoryeffects. Reprinted from NeuroImage, Volume 54(3),Hongkeun Kim, Neural activity that predicts subsequentmemory and forgetting: A meta-analysis of 74 fMRI studies,Pages 2446–2461, Copyright (2011), with permission fromElsevier. 60

3.7 Object–location virtual environment and hippocampallaterality results. Reprinted from NeuroReport, Volume 17(4),Lars Frings, Kathrin Wagner, Josef Unterrainer, JoachimSpreer, Ulrike Halsband, and Andreas Schulze-Bonhage,Gender-related differences in lateralization of hippocampalactivation and cognitive strategy, Pages 417–421, Copyright(2006), with permission from Wolters Kluwer. 63

3.8 Change in the size of the posterior hippocampus as a functionof time as a London taxi driver. Reprinted from Proceedings of

the National Academy of Sciences of the United States of

America, Volume 97, Eleanor A. Maguire, David G. Gadian,Ingrid S. Johnsrude, Catriona D. Good, John Ashburner,Richard S. J. Frackowiak, and Christopher D. Frith,

xii List of Figures

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Navigation-related structural change in the hippocampi of taxidrivers, Pages 4398–4403, Copyright (2000) National Academyof Sciences, USA. 65

4.1 ERP activity associated with recollection and familiarity.Reprinted from Brain Research, Volume 1122(1), KaiaL. Vilberg, Rana F. Moosavi, and Michael D. Rugg,The relationship between electrophysiological correlates ofrecollection and amount of information retrieved, Pages161–170, Copyright (2006), with permission from Elsevier. 73

4.2 ERP activity associated with conceptual repetition priming.Reprinted from NeuroImage, Volume 49(3), Joel L. Voss,Haline E. Schendan, and Ken A. Paller, Finding meaning innovel geometric shapes influences electrophysiologicalcorrelates of repetition and dissociates perceptual andconceptual priming, Pages 2879–2889, Copyright (2010), withpermission from Elsevier. 77

4.3 Topographic maps illustrating the conceptual priming effectand the mid-frontal old–new effect. Reprinted fromNeuroImage, Volume 63(3), Emma K. Bridger, Regine Bader,Olga Kriukova, Kerstin Unger, and Axel Mecklinger,The FN400 is functionally distinct from the N400, Pages1334–1342, Copyright (2012), with permission from Elsevier. 78

4.4 Topographic maps and activation timecourses illustratingspatial memory effects. Reprinted from Brain Research,Volume 1330, Scott D. Slotnick, Synchronous retinotopicfrontal-temporal activity during long-term memory for spatiallocation, Pages 89–100, Copyright (2010), with permission fromElsevier. 81

4.5 EEG frequency band activity associated with subsequentlyremembered and forgotten items. Reprinted from NeuroImage,Volume 66, Uwe Friese, Moritz Köster, Uwe Hassler, UllaMartens, Nelson Trujillo-Barreto, and Thomas Gruber,Successful memory encoding is associated with increased cross-frequency coupling between frontal theta and posterior gammaoscillations in human scalp-recorded EEG, Pages 642–647,Copyright (2013), with permission from Elsevier. 83

5.1 Subsequent forgetting fMRI activity and default network fMRIactivity. (A) Reprinted from NeuroImage, Volume 54(3),Hongkeun Kim, Neural activity that predicts subsequentmemory and forgetting: A meta-analysis of 74 fMRI studies,Pages 2446–2461, Copyright (2011), with permission from

List of Figures xiii

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Elsevier. (B)Reprinted fromAnnals of the NewYorkAcademy

of Sciences, Volume 1124, Randy L. Buckner, JessicaR. Andrews-Hanna, and Daniel L. Schacter, The Brain’sDefault Network, Pages 1–38, Copyright (2008), withpermission from John Wiley and Sons. 91

5.2 Retrieval-inducted forgetting paradigm, behavioralperformance, and fMRI activity. Reprinted fromWimber et al.,The Journal of Neuroscience: The official journal of the Society

for Neuroscience, Copyright (2008), Reproduced withpermission of the Society for Neuroscience. 93

5.3 Retrieval-induced forgetting EEG activity. Reprinted fromStaudigl et al.,The Journal of Neuroscience: The official journal

of the Society for Neuroscience, Copyright (2010), Reproducedwith permission of the Society for Neuroscience. 95

5.4 Regions of the brain commonly and differentially associatedwith true memory and related false memory. Reprinted fromNature Neuroscience, Volume 7(6), Scott D. Slotnick andDaniel L. Schacter, A sensory signature that distinguishes truefrom false memories, Pages 664–672, Copyright (2004). 99

5.5 Brain activity associated with unrelated false memory. RachelJ. Garoff-Eaton, Scott D. Slotnick, andDaniel L. Schacter, Notall false memories are created equal: The neural basis of falserecognition, Cerebral Cortex, 2006, 16(11), 1645–1652, bypermission of Oxford University Press. 102

6.1 Object or location working memory paradigm and fMRIresults. Reprinted from Neuropsychologia, Volume 41(3),Joseph B. Sala, Pia Rämä, and Susan M. Courtney, Functionaltopography of a distributed neural system for spatial andnonspatial information maintenance in working memory,Pages 341–356, Copyright (2003), with permission fromElsevier. 110

6.2 Sustained working memory fMRI activity in the dorsolateralprefrontal cortex. Reprinted fromTrends in Cognitive Sciences,Volume 7(9), Clayton E. Curtis and Mark D’Esposito,Persistent activity in the prefrontal cortex during workingmemory, Pages 415–423, Copyright (2003), with permissionfrom Elsevier. 111

6.3 Color and/or location working memory paradigms and medialtemporal lobe lesion results. Reprinted fromNeuropsychologia, Volume 46(2), Carsten Finke, MischaBraun, Florian Ostendorf, Thomas-Nicolas Lehmann, Karl-

xiv List of Figures

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Titus Hoffiman, Ute Kopp, and Christoph J. Ploner,The human hippocampal formation mediates short-termmemory of colour-location associations, Pages 614–623,Copyright (2008), with permission from Elsevier. 118

6.4 Color working memory paradigm and EEG results. ReprintedfromCurrent Biology, Volume 19(21), Paul Sauseng,WolfgangKlimesch, Kirstin F. Heise, Walter R. Gruber, Elisa Holz,Ahmed A. Karim, Mark Glennon, Christian Gerloff, NielsBirbaumer, and Friedhelm C. Hummel, Brain oscillatorysubstrates of visual short-term memory capacity, Pages1846–1852, Copyright (2009), with permission from Elsevier. 120

6.5 Behavioral effects and brain effects of working memorytraining. Reprinted from NeuroImage, Volume 52(2), DietsjeD. Jolles, Meike J. Grol, Mark A. Van Buchem, SergeA. R. B. Rombouts, and Eveline A. Crone, Practice effects inthe brain: Changes in cerebral activation after workingmemory practice depends on task demands, Pages 658–668,Copyright (2010), with permission from Elsevier. 124

7.1 Repetition priming paradigm and fMRI results. Reprintedfrom Neuropsychologia, Volume 39(2), Wilma Koutstaal,Anthony D. Wagner, Michael Rotte, Anat Maril, RandyL. Buckner, and Daniel L. Schacter, Perceptual specificity invisual object priming: Functional magnetic resonance imagingevidence for a laterality difference in fusiform cortex, Pages184–199, Copyright (2001), with permission from Elsevier. 132

7.2 Review of cortical repetition priming effects. Reprinted fromCurrent Opinion in Neurobiology, Volume 17(2), DanielL. Schacter, Gagan S.Wig, andW. Dale Stevens, Reductions incortical activity during priming, Pages 171–176, Copyright(2007), with permission from Elsevier. 134

7.3 Repetition priming EEG and MEG results. (A) Reprintedfrom Fiebach et al., The Journal of Neuroscience: The official

journal of the Society for Neuroscience, Copyright (2005),Reproduced with permission of the Society for Neuroscience.(B) Reprinted from Frontiers in Human Neuroscience, 2010,Volume 4, Article 30, Jessica R. Gilbert, Stephen J. Gotts,Frederick W. Carver, and Alex Martin, Object repetition leadsto local increases in the temporal coordination of neuralresponses. 137

7.4 Models of repetition priming. Reprinted from Trends in

Cognitive Sciences, Volume 10(1), Kalanit Grill-Spector,

List of Figures xv

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Richard Henson, and Alex Martin, Repetition and the brain:Neural models of stimulus-specific effects, Pages 14–23,Copyright (2006), with permission from Elsevier. 139

7.5 Contextual cuing stimulus display. 1437.6 Skill learning behavioral results and fMRI results. Reprinted

from Brain Research, Volume 1318, Liangsuo Ma, BinquanWang, Shalini Narayana, EliotHazeltine, Xiying Chen,DonaldA. Robin, Peter T. Fox, Jinhu Xiong, Changes in regionalactivity are accompanied with changes in inter-regionalconnectivity during 4 weeks motor learning, Pages 64–76,Copyright (2010), with permission from Elsevier. 146

8.1 Spatial attention paradigm and fMRI results. (B) Reprintedfrom Neuropsychologia, Volume 39(12), Joseph B. Hopfinger,Marty G.Woldorff, EvanM. Fletcher, andGeorge R.Mangun,Dissociating top-down attentional control from selectiveperception and action, Pages 1277–1291, Copyright (2001),with permission from Elsevier. (C) Reprinted from Brain

Research, Volume 1302, Preston P. Thakral and ScottD. Slotnick, The role of parietal cortex during sustained visualspatial attention, Pages 157–166, Copyright (2009), withpermission from Elsevier. 153

8.2 Spatial memory fMRI and ERP results. Reprinted from Brain

Research, Volume 1268, Scott D. Slotnick, Rapid retinotopicreactivation during spatial memory, Pages 97–111, Copyright(2009), with permission from Elsevier. 156

8.3 Meta-analysis of control region activity associated withattention, working memory, and episodic memory retrieval.Reprinted from Consciousness and Cognition, Volume 14(2),Hamid R. Naghavi and Lars Nyberg, Common fronto-parietalactivity in attention, memory, and consciousness: Shareddemands on integration? Pages 390–425, Copyright (2005),with permission from Elsevier. 158

8.4 Visual perception, imagery, and attention paradigms and fMRIresults. Scott D. Slotnick, William L. Thompson, andStephen M. Kosslyn, Visual mental imagery inducesretinotopically organized activation of early visual areas,Cerebral Cortex, 2005, 15(10), 1570–1583, by permission ofOxford University Press. 160

8.5 Language processing regions. Reprinted from Journal of

Anatomy, Volume 197, Cathy J. Price, The anatomy oflanguage: Contributions from functional neuroimaging, Pages

xvi List of Figures

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335–359, Copyright (2000), with permission fromJohn Wiley & Sons, Inc. 164

8.6 The amygdala and the hippocampus. Reprinted from Current

Opinion in Neurobiology, Volume 14(2), Elizabeth A. Phelps,Human emotion and memory: Interactions of the amygdalaand hippocampal complex, Pages 198–202, Copyright (2004),with permission from Elsevier. 167

9.1 Hippocampus and entorhinal cortex segmentation andvolumes of these regions in control participants and amnesticmild cognitive impairment patients. Reprinted fromProceedings of the National Academy of Sciences of the United

States of America, Volume 103, Travis R. Stoub, LeyladeToledo-Morrell, Glenn T. Stebbins, Sue Leurgans, DavidA. Bennett, and Raj C. Shah, Hippocampal disconnectioncontributes to memory dysfunction in individuals at risk forAlzheimer’s disease, Pages 10041–10045, Copyright (2006)National Academy of Sciences, USA. 173

9.2 Pattern separation paradigm, behavioral results, and fMRIresults for control participants and aMCI patients. Reprintedfrom NeuroImage, Volume 51(3), Michael A. Yassa,Shauna M. Stark, Arnold Bakker, Marilyn S. Albert, MichelaGallagher, and Craig E. L. Stark, High-resolution structuraland functional MRI of hippocampal CA3 and dentate gyrus inpatients with amnestic mild cognitive impairment, Pages1242–1252, Copyright (2010), with permission from Elsevier. 175

9.3 Relationship between exercise engagement and Alzeimer’sdisease biomarkers in older adults. Reprinted from Annals of

Neurology, Volume 68, Kelvin Y. Liang, Mark A. Mintun,Anne M. Fagan, Alison M. Goate, Julie M. Bugg,David M. Holtzman, John C. Morris, and Denise Head,Exercise and Alzheimer’s disease biomarkers in cognitivenormal older adults, Pages 311–318, Copyright (2010), withpermission from John Wiley & Sons, Inc. 180

9.4 N-back paradigm, behavioral results, and fMRI results for mildtraumatic brain injury patients and control participants.Reprinted from NeuroImage, Volume 14(5), ThomasW.McAllister, Molly B. Sparling, Laura A. Flashman, StephenJ. Guerin, Alexander C. Mamourian, and Andrew J. Saykin,Differential working memory load effects after mild traumaticbrain injury, Pages 1004–1012, Copyright (2001), withpermission from Elsevier. 182

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9.5 Stimuli and behavioral results for control participants andmedial temporal lobe epilepsy patients following removal ofleft or right medial temporal lobe regions. Reprinted fromNeuropsychologia, Volume 24(5), Marilyn Jones-Gotman,Right hippocampal excision impairs learning and recall of a listof abstract designs, Pages 659–670, Copyright (1986), withpermission from Elsevier. 188

9.6 Brain images of transient global amnesia patients. Reprintedfrom the Journal of Clinical Neurology, Volume 4(2),YoungSoon Yang, SangYun Kim, and Jae Hyoung Kim,Ischemic evidence of transient global amnesia: Location ofthe lesion in the hippocampus, Pages 59–66, Copyright (2008). 192

10.1 Spontaneous object recognition task. Reprinted fromNeuroscience and Biobehavioral Reviews, Volume 32, BoyerD. Winters, Lisa M. Saksida, and Timothy J. Bussey, Objectrecognition memory: Neurobiological mechanisms ofencoding, consolidation and retrieval, Pages 1055–1070,Copyright (2008), with permission from Elsevier. 198

10.2 Medial temporal lobe organization and phylogenic tree ofmammals. Reprinted from Hippocampus, Volume 16, JosephR. Manns and Howard Eichenbaum, Evolution of declarativememory, Pages 795–808, Copyright (2006), with permissionfrom John Wiley & Sons, Inc. 200

10.3 Long-term potentiation experimental setup and results.Reprinted from The Journal of Physiology, Volume 232,T. V. P. Bliss and T. Lømo, Long-lasting potentiation ofsynaptic transmission in the dentate area of the anaesthetizedrabbit following stimulation of the perforant path, Pages331–356, Copyright (1973), with permission fromJohn Wiley & Sons, Inc. 202

10.4 Memory replay in the rat. Reprinted from Current Opinion

in Neurobiology, Volume 21, Gabrielle Girardeau andMichaëlZugaro, Hippocampal ripples and memory consolidation,Pages 452–459, Copyright (2011), with permission fromElsevier. 204

10.5 Time cell behavioral apparatus and neural activity. Reprintedfrom Neuron, Volume 78, Benjamin J. Kraus, RobertJ. Robinson II, John A. White, Howard Eichenbaum, andMichael E. Hasselmo, Hippocampal “time cells”: Time versuspath integration, Pages 1090–1101, Copyright (2013), withpermission from Elsevier. 207

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10.6 Time delay memory task and behavioral results. Reprintedfrom Current Biology, Volume 16, Stephanie J. Babb andJonathan D. Crystal, Episodic-like memory in the rat, Pages1317–1321, Copyright (2006), with permission from Elsevier. 211

10.7 Hippocampal anatomy in mammals. (A) Reprinted fromHippocampus, Volume 16, J. R. Manns and H. Eichenbaum,Evolution of declarative memory, Pages 795–808, Copyright(2006), with permission from JohnWiley & Sons, Inc. (B)Withkind permission from Springer Science + Business Media:Brain Structure and Function, Organization and chemicalneuroanatomy of the African elephant (Loxodonta africana)hippocampus, 219(5), 2014, 1587–1601, Nina Patzke,Olatunbosun Olaleye, Mark Haagensen, Patrick R. Hof,Amadi O. Ihunwo, and Paul R. Manger, Figure 2. 214

11.1 Past phrenology map and present brain map. Reprinted fromProceedings of the National Academy of Sciences of the

United States of America, Volume 107, Nancy Kanwisher,Functional specificity in the human brain: A window into thefunctional architecture of the mind, Pages 11163–11170,Copyright (2010) National Academy of Sciences, USA. 221

11.2 Face processing and shape processing fMRI activity.Reprinted from NeuroImage, Volume 83, Scott D. Slotnickand Rachel C. White, The fusiform face area respondsequivalently to faces and abstract shapes in the left andcentral visual fields, Pages 408–417, Copyright (2013), withpermission from Elsevier. 223

11.3 Number of fMRI and ERP articles in the highest-impactcognitive neuroscience journals. 225

11.4 Brain region interaction TMS target sites and fMRI visualsensory effects during perception. Reprinted from Current

Biology, Volume 16, Christian C. Ruff, FelixBlankenburg, Otto Bjoertomt, Sven Bestmann, ElliotFreeman, John-Dylan Haynes, Geraint Rees, Oliver Josephs,Ralf Deichmann, and John Driver, Concurrent TMS-fMRIand psychophysics reveal frontal influences on humanretinotopic visual cortex, Pages 1479–1488, Copyright (2006),with permission from Elsevier. 228

11.5 Brain region interaction TMS target site, visual sensory regionsof interest, and fMRI effects during working memory.Reprinted from Proceedings of the National Academy of

Sciences of the United States of America, Volume 108, Eva

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Feredoes, KlaartjeHeinen, NikolausWeiskopf, ChristianRuff,and John Driver, Causal evidence for frontal involvement inmemory target maintenance by posterior brain areas duringdistractor interference of visual working memory, Pages17510–17515, Copyright (2011) National Academy ofSciences, USA. 230

11.6 The relationships between the fields of cognitive psychology,cognitive neuroscience, and behavioral neuroscience in thepast and in the future. 233

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Preface

The human brain and memory are two of the most complex andfascinating systems in existence. Within the last two decades, the cogni-tive neuroscience of memory has begun to thrive with the advent oftechniques that can non-invasively measure human brain activity withhigh spatial resolution and high temporal resolution.

This is the first book to provide a comprehensive treatment of thecognitive neuroscience of memory. It is related to three classes of otherbooks. First, textbooks on cognitive psychology or cognition providebroad overviews of the cognitive psychology of memory and thereforeonly consider a small fraction of the work on the cognitive neuroscienceof memory. Second, textbooks on cognitive neuroscience providebroad overviews of the entire field and also consider only a small frac-tion of the work on memory. Third, more specialized books on memoryfocus on the cognitive psychology, the behavioral neuroscience, or thecomputational modeling of memory rather than the cognitive neu-roscience of memory.

This book highlights temporal processing in the brain. Cognitiveneuroscientists predominantly use functional magnetic resonance ima-ging (fMRI) to identify the brain regions associated with a cognitiveprocess. Although fMRI has excellent spatial resolution, this methodprovides little if any information about the time at which brain regionsare active or the way in which different brain regions interact.By emphasizing both spatial and temporal aspects of brain processing,this book provides a complete overview of the cognitive neuroscience ofmemory and aims to guide the future of memory research.

Each chapter is written in an accessible style and includes backgroundinformation and many figures. Debated topics are discussed throughoutthe text. The most popular view is routinely questioned rather thansimply assumed to be correct, as is done in the vast majority of textbooks.In this way, science is depicted as open to question, evolving, andexciting.

The audience for this book is educated lay people interested in thecognitive neuroscience of memory and undergraduate students, graduatestudents, and scientists who are interested in a comprehensive up-to-datetreatment of this topic. Each chapter includes learning objectives, anintroduction, sections on key topics, a summary, review questions, and

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recommended scientific articles. At a college or university, this bookcould serve as a supplemental textbook in lower-level courses (forinstructors who desire a comprehensive treatment on this topic) or asa main text in an intermediate-level undergraduate course, an advanced-level undergraduate course, or a graduate seminar (with instructorlectures, student presentations, and discussions of the recommendedscientific articles).

Many individuals significantly improved the quality of this book. Firstand foremost, I thank Matthew Bennet, my editor. Without his vision,guidance, and support, this book would not exist. I am grateful to JessicaKaranian, Brittany Jeye, and two anonymous reviewers for providinginvaluable comments and suggestions on the entire book. I thankElizabeth Chua for her expert comments on the transcranial directcurrent stimulation section (and for providing a photograph illustratingthis technique) and Lauren Moo for her insightful comments on theexplicit memory and disease chapter. Finally, I thank Jacqueline Frenchfor her skilled copy editing and appreciate all of the professionals atCambridge University Press, including Valerie Appleby, BriandaReyes, Srilakshmi Gobidass, and Maree Williams-Smith, who made theproduction of this book a smooth process.

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