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STEVENS’ HANDBOOK OFEXPERIMENTAL PSYCHOLOGYAND COGNITIVE NEUROSCIENCE

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STEVENS’ HANDBOOK OFEXPERIMENTAL PSYCHOLOGYAND COGNITIVE NEUROSCIENCEFOURTH EDITION

Volume 1Learning & Memory

Editor-in-Chief

JOHN T. WIXTED

Volume Editors

ELIZABETH A. PHELPS AND LILA DAVACHI

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This book is printed on acid-free paper. ∞

Designations used by companies to distinguish their products are often claimed astrademarks. In all instances where John Wiley & Sons, Inc., is aware of a claim,the product names appear in initial capital or all capital letters. Readers, however,should contact the appropriate companies for more complete informationregarding trademarks and registration.

Copyright © 2018 by John Wiley & Sons, Inc., New York. All rights reserved.

Published by John Wiley & Sons, Inc.Published simultaneously in Canada.

No part of this publication may be reproduced, stored in a retrieval system ortransmitted in any form or by any means, electronic or mechanical, includinguploading, downloading, printing, decompiling, recording or otherwise, except aspermitted under Sections 107 or 108 of the 1976 United States Copyright Act,without the prior written permission of the Publisher. Requests to the Publisher forpermission should be addressed to the Permissions Department, John Wiley &Sons, Inc., 605 Third Avenue, New York, NY 10158–0012, (212) 850–6011, fax(212) 850–6008, E-Mail: [email protected].

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Library of Congress Cataloging-in-Publication Data

The Library of Congress has cataloged the combined volume as follows:

Name: Wixted, John T., editor.Title: Stevens’ handbook of experimental psychology and cognitive

neuroscience / by John T. Wixted (Editor-in-chief).Other titles: Handbook of experimental psychology.Description: Fourth edition. | New York : John Wiley & Sons, Inc., [2018] |

Includes index. Contents: Volume 1. Learning and memory – Volume 2.Sensation, perception, and attention – Volume 3. Language & thought –Volume 4. Developmental & social psychology – Volume 5. Methodology.

Identifiers: LCCN 2017032691 | ISBN 9781119170013 (cloth : vol. 1) |ISBN 9781119170037 (epdf : vol. 1) | ISBN 9781119170020 (epub : vol. 1) |ISBN 9781119170044 (cloth : vol. 2) | ISBN 9781119174158 (epdf : vol. 2) |ISBN 9781119174073 (epub : vol. 2) | ISBN 9781119170693 (cloth : vol. 3) |ISBN 9781119170730 (epdf : vol. 3) | ISBN 9781119170716 (epub : vol. 3) |ISBN 9781119170051 (cloth : vol. 4) | ISBN 9781119170068 (epdf : vol. 4) |ISBN 9781119170082 (epub : vol. 4) | ISBN 9781119170129 (cloth : vol. 5) |ISBN 9781119170150 (epdf : vol. 5) | ISBN 9781119170143 (epub : vol. 5)Subjects: LCSH: Psychology, Experimental. | Cognitive neuroscience.Classification: LCC BF181 .H336 2018 | DDC 150—dc23 LC record available athttps://lccn.loc.gov/2017032691

Wiley also publishes its books in a variety of electronic formats. Some content thatappears in print may not be available in electronic books. For more informationabout Wiley products, visit our web site at www.wiley.com.

Printed in the United States of America.10 9 8 7 6 5 4 3 2 1

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Contributors

R. Alison AdcockDuke University

Sara E. AlgerUniversity of Notre Dame

Michael J. ArmsonRotman Research Institute, Universityof Toronto

Agnes BacopulosRotman Research Institute

Marlene BehrmannCarnegie Mellon University

Marvin M. ChunYale University

Deborah DavisUniversity of Nevada Reno

Nancy A. DennisPennsylvania State University

Mark D’EspositoUniversity of California, Berkeley

Nicholas B. DiamondRotman Research Institute, Universityof Toronto

Rachel A. DianaVirginia Polytechnic Institute and StateUniversity

Kathryn C. DickersonDuke University

Keisuke FukudaVanderbilt University

Sarah M. KarkBoston College

Elizabeth A. KensingerBoston College

Tadeusz W. KononowiczFrench National Institute of Healthand Medical Research (Inserm)

Brice A. KuhlUniversity of Oregon

Kevin S. LaBarDuke University

Brian LevineRotman Research Institute, Universityof Toronto

Elizabeth F. LoftusUniversity of California, Irvine

Nicole M. LongUniversity of Oregon

John M. McCormick-HuhnPennsylvania State University

Warren H. MeckDuke University

Derek Evan NeeFlorida State University

Daniela J. PalomboBoston University

Jessica D. PayneUniversity of Notre Dame

Adam L. PutnamCarleton College

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vi Contributors

Jeroen G. W. RaaijmakersUniversity of Amsterdam

Henry L. Roediger IIIWashington University in St. Louis

Kristoffer RomeroRotman Research Institute

Daniel L. SchacterHarvard University

Dhawal SelarkaRotman Research Institute

Signy SheldonMcGill University

Daniel StjepanovicDuke University

Karl K. SzpunarUniversity of Illinois at Chicago

Hedderik van RijnUniversity of Groningen

Mark VidaCarnegie Mellon University

Fang WangVirginia Polytechnic Institute and StateUniversity

Geoffrey F. WoodmanVanderbilt University

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Contents

PREFACE ix

1 EMOTION AND MEMORY 1Elizabeth A. Kensinger and Sarah M. Kark

2 THE COGNITIVE NEUROSCIENCE OF FEAR LEARNING 27Daniel Stjepanovic and Kevin S. LaBar

3 EPISODIC MEMORY 67Rachel A. Diana and Fang Wang

4 SLEEP AND MEMORY 101Sara E. Alger and Jessica D. Payne

5 MEMORY AND FUTURE IMAGINING 145Karl K. Szpunar and Daniel L. Schacter

6 EDUCATION AND MEMORY: SEVEN WAYS THE SCIENCEOF MEMORY CAN IMPROVE CLASSROOM LEARNING 169Adam L. Putnam and Henry L. Roediger III

7 MOTIVATION AND MEMORY 215Kathryn C. Dickerson and R. Alison Adcock

8 INHIBITION IN MEMORY 251Jeroen G. W. Raaijmakers

9 MEMORY AND ATTENTION 285Nicole M. Long, Brice A. Kuhl, and Marvin M. Chun

10 ITEM AND ASSOCIATIVE MEMORY DECLINE IN HEALTHY AGING 323Nancy A. Dennis and John M. McCormick-Huhn

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viii Contents

11 ASSESSING AUTOBIOGRAPHICAL MEMORY: IMPLICATIONSFOR UNDERSTANDING THE UNDERLYING NEUROCOGNITIVEMECHANISMS 363Signy Sheldon, Nicholas B. Diamond, Michael J. Armson, Daniela J. Palombo,Dhawal Selarka, Kristoffer Romero, Agnes Bacopulos, and Brian Levine

12 WORKING MEMORY: AN EVOLVING CONCEPT 397Derek Evan Nee and Mark D’Esposito

13 VISUAL COGNITION AND WORKING MEMORY 423Geoffrey F. Woodman and Keisuke Fukuda

14 TIMING AND TIME PERCEPTION: A CRITICAL REVIEWOF NEURAL TIMING SIGNATURES BEFORE, DURING,AND AFTER THE TO-BE-TIMED INTERVAL 453Tadeusz W. Kononowicz, Hedderik van Rijn, and Warren H. Meck

15 VISUAL OBJECT RECOGNITION 491Marlene Behrmann and Mark Vida

16 EYEWITNESS SCIENCE IN THE 21ST CENTURY: WHAT DO WEKNOW AND WHERE DO WE GO FROM HERE? 529Deborah Davis and Elizabeth F. Loftus

Author Index 567

Subject Index 599

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Preface

Since the first edition was published in 1951,The Stevens’ Handbook of Experimental Psy-chology has been recognized as the standardreference in the experimental psychologyfield. The most recent (third) edition of thehandbook was published in 2004, and it wasa success by any measure. But the field ofexperimental psychology has changed in dra-matic ways since then. Throughout the firstthree editions of the handbook, the changes inthe field were mainly quantitative in nature.That is, the size and scope of the field grewsteadily from 1951 to 2004, a trend that wasreflected in the growing size of the handbookitself: the one-volume first edition (1951) wassucceeded by a two-volume second edition(1988) and then by a four-volume third edi-tion (2004). Since 2004, however, this still-growing field has also changed qualitativelyin the sense that, in virtually every subdomainof experimental psychology, theories of themind have evolved to include theories ofthe brain. Research methods in experimen-tal psychology have changed accordinglyand now include not only venerable EEGrecordings (long a staple of research in psy-cholinguistics) but also MEG, fMRI, TMS,and single-unit recording. The trend towardneuroscience is an absolutely dramatic,worldwide phenomenon that is unlikely everto be reversed. Thus, the era of purely behav-ioral experimental psychology is already longgone, even though not everyone has noticed.

Experimental psychology and cognitiveneuroscience (an umbrella term that, asused here, includes behavioral neuroscience,social neuroscience, and developmental neu-roscience) are now inextricably intertwined.Nearly every major psychology departmentin the country has added cognitive neurosci-entists to its ranks in recent years, and thattrend is still growing. A viable handbook ofexperimental psychology should reflect thenew reality on the ground.

There is no handbook in existence todaythat combines basic experimental psychol-ogy and cognitive neuroscience, despite thefact that the two fields are interrelated—andeven interdependent—because they are con-cerned with the same issues (e.g., memory,perception, language, development, etc.).Almost all neuroscience-oriented researchtakes as its starting point what has beenlearned using behavioral methods in exper-imental psychology. In addition, nowadays,psychological theories increasingly take intoaccount what has been learned about thebrain (e.g., psychological models increas-ingly need to be neurologically plausible).These considerations explain why I chosea new title for the handbook: The Stevens’Handbook of Experimental Psychology andCognitive Neuroscience. This title serves asa reminder that the two fields go togetherand as an announcement that the Stevens’Handbook now covers it all.

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x Preface

The fourth edition of the Stevens’ Hand-book is a five-volume set structured asfollows:

1. Learning & Memory: Elizabeth A.Phelps and Lila Davachi (volume editors)

Topics include fear learning, time per-ception, working memory, visual objectrecognition, memory and future imag-ining, sleep and memory, emotion andmemory, attention and memory, motiva-tion and memory, inhibition in memory,education and memory, aging and mem-ory, autobiographical memory, eyewitnessmemory, and category learning.

2. Sensation, Perception, & Attention:John T. Serences (volume editor)

Topics include attention; vision; colorvision; visual search; depth perception;taste; touch; olfaction; motor control; per-ceptual learning; audition; music percep-tion; multisensory integration; vestibular,proprioceptive, and haptic contributionsto spatial orientation; motion perception;perceptual rhythms; the interface theoryof perception; perceptual organization;perception and interactive technology;and perception for action.

3. Language & Thought: Sharon L.Thompson-Schill (volume editor)

Topics include reading, discourse anddialogue, speech production, sentenceprocessing, bilingualism, concepts andcategorization, culture and cognition,embodied cognition, creativity, reasoning,speech perception, spatial cognition, wordprocessing, semantic memory, and moralreasoning.

4. Developmental & Social Psychology:Simona Ghetti (volume editor)

Topics include development of visualattention, self-evaluation, moral devel-

opment, emotion-cognition interactions,person perception, memory, implicitsocial cognition, motivation group pro-cesses, development of scientific thinking,language acquisition, category and con-ceptual development, development ofmathematical reasoning, emotion regula-tion, emotional development, developmentof theory of mind, attitudes, and executivefunction.

5. Methodology: Eric-Jan Wagenmakers(volume editor)

Topics include hypothesis testing andstatistical inference, model comparisonin psychology, mathematical modelingin cognition and cognitive neuroscience,methods and models in categorization,serial versus parallel processing, theoriesfor discriminating signal from noise,Bayesian cognitive modeling, responsetime modeling, neural networks andneurocomputational modeling, methodsin psychophysics analyzing neural timeseries data, convergent methods ofmemory research, models and methodsfor reinforcement learning, culturalconsensus theory, network models forclinical psychology, the stop-signalparadigm, fMRI, neural recordings, andopen science.

How the field of experimental psychologywill evolve in the years to come is anyone’sguess, but the Stevens’ Handbook providesa comprehensive overview of where itstands today. For anyone in search ofinteresting and important topics to pursuein future research, this is the place to start.After all, you have to figure out the direc-tion in which the river of knowledge iscurrently flowing to have any hope of everchanging it.

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CHAPTER 1

Emotion and Memory

ELIZABETH A. KENSINGER AND SARAH M. KARK

INTRODUCTION

Although more than a decade has passedsince September 11, 2001, most adults willhave no problem remembering what hap-pened on that date; by contrast, most of thosesame adults will have no memory of whathappened on the previous day. It is wellestablished that we are less likely to forgetemotional events than we are to forget moremundane experiences. Yet, despite this con-sensus, there continues to be active researchand debate about fundamental questionsregarding the links between emotion andmemory: How does the nature of the emo-tional reaction affect memory? Which detailsof an emotional experience are most likelyto be retained? What neural processes enablethese interactions between emotion andmemory, and over what time course do theyoperate?

In this chapter, we first focus on how twodifferent aspects of an emotional reaction—its valence and arousal—affect the way thatthe events are remembered. We then turnto a discussion of the time course of thoseeffects, describing how emotion can affectthe sequence of processes engaged duringencoding and retrieval as well as the pro-cesses that unfold over time as memoriesare consolidated. In each of these sections,we review findings from behavioral, neu-roimaging, and psychophysiological studies,

because it is from the combination of thesemethods that many of the key insights regard-ing emotion and memory have been revealed.We conclude with a brief discussion of threedebates that are ongoing in the field: therole of the amygdala in emotional memory,the effects of emotion on memory accuracy,and the effects of emotional appraisals andreappraisals on memory.

HOW VALENCE AND AROUSALAFFECT MEMORY

Often when we think about an emotional re-action, we think about the physiologicalreactions elicited, such as our sweaty palmsand pounding heart as we are about to makeour way onstage in front of an audience.Indeed, much of the research examining theeffects of emotion on memory has focusedon the influences of this arousal dimension(Mather & Sutherland, 2011; Yonelinas &Ritchey, 2015), building on decades ofresearch using animal models to reveal theneural circuitry implicated in arousal-basedmodulation of memory (see McGaugh, 2015,for a review). Yet the pleasure or displea-sure stemming from an event also can be apowerful predictor of how that event will beremembered. In this section, we describe theinfluences of these dimensions of arousal(physiological and subjective reactivity) and

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2 Emotion and Memory

valence (pleasure or displeasure; see Lang,Greenwald, Bradley, & Hamm, 1993; Russell,1980, for discussion of these dimensions).

Separable Influences of Valenceand Arousal

The emotional events that we experienceoften elicit shifts in valence and arousal.In other words, as compared to a neutralstate, emotional events tend to evoke plea-sure or displeasure as well as subjective andphysiological arousal. Although shifts inboth dimensions often occur when emotion iselicited in real-world contexts, in laboratorysettings the influences of these dimensionscan be distinguished. Most commonly, this isachieved by selecting stimuli that elicit shiftsin one primary dimension or by matchingstimuli on one dimension (e.g., valence) andthen examining how a change in the otherdimension (e.g., arousal) affects memory.

In a series of studies, Kensinger andCorkin (2003, 2004; see Kensinger, 2004,for a review) demonstrated that the presenceof either the valence or the arousal dimen-sion (i.e., a change from neutral in eitherdirection) was sufficient to elicit memoryenhancements (Kensinger & Corkin, 2003):Words that evoked changes in arousal butnot valence (“high-arousal stimuli”) wereremembered better than words that elicitedneither changes in arousal nor valence, and asimilar memory benefit also was revealed forwords that evoked changes in valence but notarousal (“valence-only stimuli”). A memoryadvantage for valenced stimuli, regardlessof their arousal, has also been demonstratedusing a large corpus of linguistic stimuli(Adelman & Estes, 2013), confirming thatshifts in the valence dimension are suffi-cient to elicit memory benefits. Importantly,however, the mechanisms underlying thevalence-only and high-arousal enhancementsappear to differ: Kensinger and Corkin

(2004) noted that high-arousal stimuli wereremembered well even when attention wasdivided during encoding, whereas memoryfor the valence-only stimuli was dramaticallyreduced when attention was divided. In fact,under conditions of divided attention, mem-ory for the valence-only stimuli was no longergreater than memory for neutral words, andthe memory enhancement for high-arousalstimuli remained intact (Kensinger & Corkin,2004).

These behavioral results pointed to disso-ciable mechanisms supporting the memorybenefits for high-arousal and valence-onlystimuli and suggested that the memory ben-efits for the former may occur relativelyautomatically and the memory benefits forthe latter may be linked to more controlledencoding processes. This conclusion is gen-erally consistent with evidence from event-related potentials (ERPs), which suggestsarousal is processed faster than valence(Jhean-Larose, Leveau, & Denhière, 2014;Recio, Conrad, Hansen, & Jacobs, 2014;Styliadis, Ioannides, Bamidis, & Papadelis,2015). In terms of memory encoding, acrossa range of paradigms, arousing stimuli havebeen remembered well even when attention isdivided (Kern, Libkuman, Otani, & Holmes,2005; Steinmetz, Waring, & Kensinger,2014), although the effect may be strongerfor negative stimuli than for positive stim-uli (Kang, Wang, Surina, & Lü, 2014).Moreover, associations between pairs ofhigh-arousal stimuli can be formed rapidly(Murray & Kensinger, 2013b) and remem-bered better than neutral stimuli even whenattention is divided (Maddox, Naveh-Benjamin, Old, & Kilb, 2012). Debatescontinue about whether these memoryenhancements for high-arousal informationoccur automatically or whether the process-ing of that information may be prioritizedat the expense of other concurrent processes(Pottage & Schaefer, 2012). But importantly,


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How Valence and Arousal Affect Memory 3

even if a prioritization explanation is correct,it still appears that the prioritization itselfoccurs relatively automatically. For instance,high-arousal stimuli typically attract atten-tion and resources (see Bröckelmann et al.,2011; Schmidt, Belopolsky, & Theeuwes,2015) even when participants are instructedto attend to other concurrent tasks or to ignorethose stimuli (see Iordan, Dolcos, & Dolcos,2013, for a review). Memory enhancementsfor valence-only stimuli, by contrast, appearto be linked to additional engagement of thesame types of controlled, elaborative pro-cesses that typically support memory. Thus,when attention is divided, these benefitsdisappear (Kang et al., 2014; Kensinger &Corkin, 2004), and older adults, who havedifficulty engaging elaborative encodingprocesses show less memory enhancementfor valence-only stimuli than for high-arousalstimuli (Kensinger, 2008).

Neuroimaging (functional magnetic reso-nance imaging; fMRI) studies have providedfurther evidence of this dissociation. Mem-ory for high-arousal stimuli is linked toengagement of the amygdala at encoding(Kensinger & Corkin, 2004; Mickley &Kensinger, 2008; Steinmetz, Schmidt,Zucker, & Kensinger, 2012) and to correla-tions between amygdala and hippocampalactivity (Fastenrath et al., 2014; Kensinger &Corkin, 2004; Leal, Tighe, Jones, & Yassa,2014; Richardson, Strange, & Dolan, 2004).By contrast, memory for valence-only stim-uli are linked to additional engagement ofthe same prefrontal cortex (PFC) and hip-pocampal processes that support memory forneutral information (Kensinger & Corkin,2004; Steinmetz & Kensinger, 2009).

Combined Influences of Valenceand Arousal Dimensions

Although these prior studies demonstratethat the presence of either valence or arousal

is sufficient to elicit memory enhancements,in everyday life, these dimensions tend toco-occur. Events that are highly valenced arealso arousing, and vice-versa (see Bradley& Lang, 1991; Lang, Bradley, & Cuthbert,2008, for distribution of stimuli in thistwo-dimensional space). Extensive researchhas therefore focused on the combinedinfluences of valence and arousal on mem-ory: How is memory affected when eventsare highly arousing and also pleasant orunpleasant?

Decades of research has confirmed thatthese emotional events are more likely to beremembered than neutral ones and can havea shallower forgetting curve than emotionalitems. Among the first demonstrations of thismemory enhancement were demonstrationsof “flashbulb memories,” the subjectivelyvivid memories formed when events are sur-prising and emotionally evocative (Brown &Kulik, 1977; see Holland & Kensinger, 2010,for a review of emotion and autobiographicalmemory). Indeed, everyday memories andflashbulb memories may be similarly detailedat first, but over time, confidence for memoryaccuracy remains high for flashbulb memo-ries whereas confidence decreases over timefor everyday memories (Talarico & Rubin,2007). In other words, people tend to be over-confident in the accuracy of their flashbulbmemories, but objective accuracy itself is notenhanced over everyday memories. Despitethe term flashbulb memory, the authors rec-ognized that “a flashbulb memory is onlysomewhat indiscriminate and is very far fromcomplete. In these respects, it is unlike a pho-tograph” (Brown & Kulik, 1977, p. 75). Thisconjecture has been upheld by myriad stud-ies, revealing that valence and arousal do notresult in memory enhancement for all eventdetails. Rather, some details are rememberedbetter when events elicit shifts in valenceand arousal, but many other details are not.There continue to be debates about the best


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way to characterize the types of details thatare remembered best (e.g., Bennion, Ford,Murray, & Kensinger, 2013; Levine &Edelstein, 2009; Mather & Sutherland, 2011;Yonelinas & Ritchey, 2015), but in a generalsense, the effects of arousal on memoryappear to be best described as selectiveenhancements.

Many of these selective enhancementshave been attributed to amygdala engage-ment. Individuals with damage to theamygdala show neither the enhancing northe impairing effects of arousal on mem-ory (e.g., Adolphs, Tranel, & Buchanan,2005; Strange, Hurlemann, & Dolan, 2003).Many fMRI studies have confirmed a linkbetween amygdala engagement and suc-cessful encoding of emotional events (for ameta-analysis see Murty, Ritchey, Adcock,& LaBar, 2010). The amygdala is activatedas attention is drawn toward salient, novelstimuli, and amygdala activity is greaterduring the processing of emotional items thatare subsequently remembered than duringthe processing of items that are subsequentlyforgotten (reviewed by Hamann, 2001; LaBar& Cabeza, 2006). Amygdala activity doesnot correspond with subsequent memory forall details of an arousing event, however,consistent with the idea of selective enhance-ments (Kensinger, Addis, & Atapattu, 2011;Kensinger & Schacter, 2006). For instance,increased amygdala activity at encoding isassociated with an increasingly vivid mem-ory at retrieval but not with retention ofan increasing number of contextual details(Kensinger et al., 2011; Waring & Kensinger,2011).

These selective enhancements can occurrelatively automatically (Steinmetz et al.,2014) and are not dependent on howovert attention is focused (Steinmetz &Kensinger, 2013). In fact, the use of con-trolled, PFC-based encoding strategies cansometimes help to broaden the types of details

that are remembered about emotional events(e.g., Kensinger, Garoff-Eaton, & Schacter,2007; Steinberger, Payne, & Kensinger,2011; Waring & Kensinger, 2011; Waring,Payne, Schacter, & Kensinger, 2010). Theseresults are consistent with the proposal thatsome of the arousal- and amygdala-mediatedeffects on memory may occur relativelyautomatically.

Separable Influences of Positiveand Negative Valence

So far, this chapter has defined the effects ofvalence as those that occur when there is achange from neutral valence. But research hasdemonstrated that it is not just the magnitudeof the change that matters but also the direc-tion of the change: Many of the mnemoniceffects of valence depend on whether thatchange is in the direction of pleasantnessor in the direction of unpleasantness. Neg-ative events often are remembered with agreater subjective vividness than positiveevents, whereas positive memories oftenare associated with a feeling of familiarity(Dewhurst & Parry, 2000; Ochsner, 2000).In the laboratory, participants are better ableto remember the visual details of negativestimuli (e.g., which weapon they saw), butthey have a harder time remembering thevisual details of positive stimuli (e.g., whichcake they saw; Kensinger, Garoff-Eaton,et al., 2007). This difference extends toautobiographical memories: Individuals havean easier time remembering the details ofgames or elections that were associatedwith a negative outcome (preferred teamor candidate lost) than with a positive out-come (preferred team or candidate won;Holland & Kensinger, 2012; Kensinger &Schacter, 2006).

These valence differences likely relate tothe fact that, even when items are equatedfor arousal, different sets of neural regions


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How Valence and Arousal Affect Memory 5

are recruited during the processing andencoding of negative compared to positivestimuli. Although converging evidence sug-gests that the amygdala is engaged for allsalient stimuli, regardless of valence (e.g.,Blackford, Buckholtz, Avery, & Zald, 2000;Liberzon, Phan, Decker, & Taylor, 2003;Sander, Grafman, & Zalla, 2003), negativevalence may lead to greater recruitment ofsensory regions, and positive valence maylead to greater recruitment of PFC regions(reviewed by Kensinger, 2009) and mid-line regions (Ritchey, Bessette-Symons,Hayes, & Cabeza, 2011). More specifically,the encoding of negative images tends tobe associated with greater fusiform activityand with greater connectivity between thefusiform and amygdala (Kark & Kensinger,2015) than does the encoding of neutral orpositive images (reviewed by Kensinger,2009). Conversely, the processing of positiveitems often is associated with greater recruit-ment of medial and lateral PFC regions andparietal regions than negative items (reviewedby Kensinger, 2009; see also Ritchey et al.,2011). These findings have been corroboratedin a number of fMRI studies, and a recentrepetitive transcranial magnetic stimulation(rTMS) study also provided partial supportfor this distinction, revealing that facilitationof left dorsolateral PFC processes improvedmemory for positive, but not for negative,stimuli (Balconi & Cobelli, 2015).

Why might these processing differencesexist? There are multiple levels at whichthis question can be answered. At one levelare theories regarding the adaptive nature ofbrain function (Friston, 2010), which couldsuggest that different types of emotionsprepare the person for different forms ofaction and thus bias different modes of cog-nitive processing (Schwarz & Clore, 1996;Storbeck, 2012; Storbeck & Clore, 2005).Indeed, another level of evidence reveals thatpositive and negative emotions are associated

with different forms of processing: Positiveaffect supports gist-based and relationalprocessing (our ability to connect incominginformation with what we know already),whereas negative affect leads to a reductionin relational processing and instead enablesitem-specific or referential processing(Storbeck & Clore, 2005), which can becomeintensified under conditions of high arousal(Storbeck & Clore, 2008). Importantly,although much of this research has examinedthe effects of sustained moods on cognitiveprocessing, the literature reviewed in thissection has highlighted similar effects withrelatively short-lived emotional reactions tospecific stimuli. Thus, valence may be ableto rapidly bias the way in which incominginformation that is arousing is processed andstored in the brain (see Figure 1.1).

Future Directions: Interactive Effectsof Valence and Arousal

There is still relatively little research exam-ining the interactive effects of valence andarousal, yet the extant research suggests thatthese interactions are important to consider.A number of studies have revealed that theeffects of arousal on memory can differ wheninformation is of positive valence ratherthan of negative valence (Ford, Addis, &Giovanello, 2012; Mickley Steinmetz, Addis,& Kensinger, 2010). Moreover, there is sug-gestive evidence for distinct neural processessupporting the interaction of valence andarousal (Styliadis et al., 2015; Wang et al.,2015). The effects of pleasant or unpleasantvalence can also be affected by the arousalof the information (Greene, Flannery, &Soto, 2014; Simola, Le Fevre, Torniainen,& Baccino, 2015). Although the literature isinsufficient to create a systematic explanationfor these interactive effects, these studiesdemonstrate the importance of consideringboth dimensions together in future research.


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emotionalevent

amygdala

moreautomaticbenefits

selectivebenefits

sensorycortices

neg valenced?

memory w/ morespecificity

memory w/ gist &familiarity

PFC/parietal

attention &elaboration

benefit memory

yes arousing? PFC

no

pos

Figure 1.1 Overview of the modulatory influences of arousal and valence at encoding.

TIME COURSE OF THE EFFECTSOF VALENCE AND AROUSALON MEMORY

Valence and arousal influence memory fromthe moment stimuli are perceived, influ-encing the way they are encoded, stored,and retrieved. In this section, we examinethe effects of valence and arousal on emo-tional memory across various time courses.We begin by zooming in to examine howvalence and arousal affect the rapid pro-cessing of information during encoding andretrieval. Then, we gradually zoom out intime. We review evidence for effects ofemotion on memory retrieval during an ini-tial search phase—during which a memoryis accessed—and a subsequent elabora-tion phase—during which the informationretrieved during the initial search is expandedon in further detail. We explore how theeffects of arousal and valence unfold as thetime between an encoding event and latermemory retrieval progresses from minutes toyears. Last, we examine encoding-to-retrieval

interactions; we highlight that what happensduring encoding can affect downstreamretrieval processes and present evidence forthe flexibility of when emotion can prioritizeinformation.

Valence and Arousal by the Millisecond:Effects at Encoding and Retrieval

When stimuli elicit valence or arousal, pro-cessing differences are noticeable withina few milliseconds of their presentation.Word processing studies have suggestedthat arousal effects might serve as an early“alert system” that precedes the evaluationof valence (Jhean-Larose et al., 2014, Recioet al., 2014). The presence of arousal alsoleads to earlier memory-related signatures:Dolcos and Cabeza (2002) demonstrated thatpositive and negative high-arousal stimuli(relative to neutral stimuli) were associatedwith earlier subsequent-memory effects (seePaller & Wagner, 2002; Wagner, Koutstaal, &Schacter, 1999, for discussion of theseeffects). Specifically, over centro-parietal


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Time Course of the Effects of Valence and Arousal on Memory 7

electrodes, subsequent-memory effects foremotionally arousing stimuli were greaterthan for neutral stimuli at a relatively earlyepoch (400 ms–600 ms).

Although Dolcos and Cabeza (2002)focused on memory for high-arousal stimuli,a recent ERP study assessed subsequent-memory effects for high-arousal and low-arousal negative stimuli. Yick, Burrato, andSchaefer (2015) reported that high- and low-arousal negative images were associatedwith enhanced subsequent-memory effectsas compared to neutral stimuli, but the high-arousal stimuli elicited enhanced effectsearlier in the encoding time course. Theseresults are generally consistent with thoseof Dolcos and Cabeza (2002) and suggestrapid, preferential processing of high-arousalnegative stimuli. Interestingly, Yick andcolleagues noted that the emotion-enhancedsubsequent-memory effects occurred basedon item memory and regardless of whetherthe source (context) memory was accuratebut that the effect was even stronger when theitem and source were remembered. This pat-tern is generally consistent with the selectivememory enhancements conveyed by emotion,discussed later in the section “Time Courseof Memory Retrieval: Effects of Emotion onMemory Search and Elaboration.” In Dolcosand Cabeza (2002) and Yick et al. (2015), theeffects of emotion on subsequent-memorysignatures co-occurred with behavioral mem-ory enhancement for the emotional stimuli.In fact, Yick et al. (2015) interpreted theirresults within a hybrid model for attention(Pottage & Schaefer, 2012), whereby higharousal enhances pre-attentive processes,sustained attention, early and late percep-tual processing, and sensory informationintegration, whereas low-arousal negativeemotion enhances more controlled processes.By contrast, when behavioral enhancementsof memory have not been present, ERPstudies have not always revealed effects of

emotion on subsequent-memory signatures(Galli, Wolpe, & Otten, 2011; Koenig &Mecklinger, 2008). This pattern of resultssuggests that the modulation of early mem-ory signatures may reflect the preferentialprocessing and encoding of emotional infor-mation so that emotional enhancements occurwhen those early signatures are modulatedby emotion.

Arousal and valence affect the timing notonly of encoding processes, as just described,but also of retrieval processes. In order toavoid confounds between the emotionalityof a retrieval cue and the emotionality ofthe memory target, many paradigms haveused neutral prompts to cue memories ofemotional events (e.g., Maratos, Allan, &Rugg, 2000). In one such study, Righi et al.(2012) presented participants with imagesof faces with happy, fearful, and neutralexpressions at study. During the test, partic-ipants were presented with the same faces,but this time all of them conveyed a neutralexpression. The novel aspect of this studywas that there were no emotional stimulipresented at retrieval (all expressions wereneutral), so any ERP effects that differedbased on study history (i.e., the studied facialexpression) would be because of memoryfor emotional stimuli and not a reaction toan emotional cue. The researchers foundthat, compared to faces studied with a happyor neutral expression, recognition of facespreviously studied with a fearful expres-sion elicited a number of ERP markers ofenhanced perceptual processing and visualattention capture (e.g., a greater early posi-tive [P] component appearing 100 ms afterthe stimulus [P100]; Carretie, Hinojosa,Martin-Loeches, Mercado, & Tapia, 2004;Mangun, 1995), and of implicit memory(e.g., a larger early fronto-central effectand a reduced negative [N] signal appear-ing 170 ms after the stimulus [N170]; seealso Jaeger & Rugg, 2012; Smith, Henson,


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Rugg, & Dolan, 2005, for evidence ofimplicit effects). Because the behavioral datademonstrated faster reaction times duringrecognition of previously fearful faces com-pared to previously happy or neutral faces,these effects were interpreted to reflect rapiddecoding of threat-related retrieval cues.Another study (Jaeger, Johnson, Corona, &Rugg, 2009) also reported early modulationof ERP effects during recognition of neutralobjects previously shown on an emotionalbackground compared to a neutral back-ground; after a 10-minute and a 24-hourstudy-test delay, effects of the emotionalcontext were apparent within 200 ms of thepresentation of the retrieval cue. Interest-ingly, the polarity and spatial distributionof the emotion effects reversed between theshorter and longer delay, which could reflectchanges in the memory trace because ofconsolidation processes.

Together, these electrophysiological stud-ies highlight the spatiotemporal dynamics ofthe effects of valence and arousal on encodingand retrieval processes and suggest that stim-uli with high intrinsic motivational salience(i.e., high-arousal negative or threat-relatedstimuli) appear to have rapid and privilegedaccess to encoding and retrieval processes.As we describe next, however, the effects ofvalence and arousal are not circumscribedto these earliest phases of retrieval. Rather,the effects appear to begin early but to havedownstream effects on the way the retrievedinformation is monitored and elaborated.Figure 1.2 summarizes the time course ofemotional memory effects across multiplephases of memory.

Time Course of Memory Retrieval:Effects of Emotion on Memory Searchand Elaboration

Memory retrieval has been demarcated intoat least two phases: an initial search phase

during which a memory is accessed and alater event elaboration phase during which theretrieved memory is maintained in mind andthe details of the event are further expandedon (Conway, Pleydell-Pearce, & Whitecross,2001). Specifically, the information retrievedduring the initial search phase serves as aretrieval cue to bring further informationand fine-grained details to mind during elab-oration. For instance, try to remember thelast time you went to the movie theater. Onhearing the cue movie theater, a controlledsearch process can use your world knowledge(e.g., nearby movie theaters) and personalsemantic knowledge (e.g., favorite moviegenre) to narrow the search space. Then,on selecting the content (e.g., saw the latestPixar film Inside Out with Kat and Coreyat the Cineplex), an elaboration process canexpand on the internal details (e.g., you criedduring the movie) and external details ofthe events (e.g., it was a going-away partyfor Kat; you downed a bucket of popcornbefore the previews were even finished).Monitoring processes also come online todetect erroneous details (e.g., you actuallysaw the movie at the Odeon because it wascloser to Kat’s house). Search and elaborationprocesses can repeat iteratively as additionaldetails are recovered and expounded on(St Jacques, Kragel, & Rubin, 2011).

The distinction between these phases hasbeen corroborated in neuroimaging stud-ies (Daselaar et al., 2008; Ford, Morris, &Kensinger, 2014; St Jacques et al., 2011;see Cabeza & St Jacques, 2007; Holland &Kensinger, 2010, for reviews). In thesestudies, the search phase is triggered bythe presentation of a retrieval cue, whereasthe elaboration phase begins once partici-pants have accessed the memory. Consistentwith the ERP studies, there has been com-pelling fMRI evidence to indicate thatemotion affects the memory search pro-cess. For example, Daselaar et al. (2008)


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9

Encoding/Initial Learning Consolidation

Time

Shorter Delay Longer Delay

Me

mo

ry P

erf

orm

an

ce

ERP effects (ms)

ERP effects (ms)

fMRI effects(s)

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Arousal(early,

subsequentmemoryeffects)

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Neutral Stim

Heart rate, skin conductanceImmediate,minutes

Hours, days, months, years••

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Consolidation processesLikely includes sleep-dependent memoryenhancement

Usually no sleep

EncodingStrategy

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Retrieval/Recognition

Search

Rapid decoding ofthreat-related stim

Greater influence of emotionon neural activity during

search (amygdala engagedacross both phases)

Elaboration

Goals Intentions Emotion Regulation

Figure 1.2 Overview of time course of arousal and valence emotion effects on memory, including factors that could influence the effects of emotion at one phase(e.g., encoding strategy or attention allocation during encoding) or across multiple phases (e.g., goals, intentions, and emotion regulation strategies).


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Ventral viewCut out view from left hemisphere

y

x

z

x

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x = +11

Key Brain Regions:

1. Dorsomedial PFC (ofsuperior frontal gyrus)

5. Dorsolateral PFC (ofmiddle frontal gyrus)

2. Ventromedial PFC

3. Parietal lobe

4. Amygdala

6. Hippocampus

7. Fusiform gyrus

x = +26

x = +33

Figure 1.3 Visualizations of key brain regions discussed in this chapter. Color version of this figure isavailable at http://onlinelibrary.wiley.com/book/10.1002/9781119170174.Source: 3D maximum probability atlas overlays from Gousias et al. (2008) and Hammers et al. (2003).

distinguished the search from the elaborationphase of autobiographical memory retrievaland provided evidence that emotion had agreater effect on amygdala engagement dur-ing the search phase, before people retrievedthe memory in full (see Figure 1.3 fordepiction of brain regions discussed in thischapter). Similar conclusions were reachedby Ford et al. (2014), using an episodic mem-ory retrieval task; even when all retrieval

cues were neutral, the emotionality of thememory target had a greater influence onneural activity during search than elabo-ration. These results suggest that emotionaffects, or even guides, the way that details ofan experience are retrieved or reassembled inorder to reconstruct the past event in memory.

Emotion is also likely to affect the way thatmemories are elaborated. Memory for emo-tions themselves is a central and useful part of

http://onlinelibrary.wiley.com/book/10.1002/9781119170174


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most emotional memories (Levine & Pizarro,2004; Wirtz, Kruger, Napa Scollon, & Diener,2003), and there is evidence that amygdalaand medial temporal lobe (MTL) activa-tion may relate to the intensity with whichthese emotions are reexperienced (Addis,Moscovitch, Crawley, & McAndrews, 2004;Ford & Kensinger, 2016). A study in patientswith MTL damage supported the con-clusion that the amygdala is involved inmemory search and in the elaboration ofemotional details of past events. In thatstudy (Buchanan, Tranel, & Adolphs, 2006),patients with MTL damage that spared theamygdala were compared to those whosedamage affected the amygdala. Importantly,memories were assessed for events that hadoccurred when the individuals still had intactmedial temporal lobes; thus, anything atyp-ical about their memories could be ascribedto the role of the MTL during retrieval ratherthan to the encoding or initial consolidationphases. This study revealed that the subsetof patients with amygdala damage were lesslikely to retrieve memories of unpleasantevents than were the other patients, corrob-orating a role for the amygdala in the searchand recovery of emotional events. But inaddition, when these patients did retrieveunpleasant events, they rated them as lessintense than did the other patients. Thislatter finding suggests that the amygdalamay also participate in the reexperience andreconstruction of emotion during retrieval(see Buchanan, 2007, for a review of effectsof emotion at retrieval).

Although relatively little research hasassessed the effects of valence on memoryretrieval, across a few studies, frontal regionshave been more active during retrievalof positive memories compared to neg-ative memories. This pattern has beendemonstrated in studies of autobiographicalmemory (Piefke, Weiss, Zilles, Markow-itsch, & Fink, 2003) and, more recently, in

a study of episodic memory (Ford et al.,2014). This distinction could be tied to theeffects of valence discussed previously, withpositive memories associated with a morethematic and heuristic form of recall (Monin,2003; Schwarz & Clore, 1996) and oftenwith a broadening of attention associatedwith broaden-and-build theories of positiveemotions (Fredrickson, 2001). Interestingly,relative to healthy participants, patients withpost-traumatic stress disorder (PTSD) haveshown greater hippocampus and amyg-dala activation during the search phase fornegative memories compared to positivememories, which might reflect exaggeratedearly-threat detection to non-traumatic nega-tive memories and less sensitivity to positiveautobiographical memories in the PTSDpopulation (St Jacques, Botzung, Miles, &Rubin, 2011). Together, these neuroimagingstudies demonstrate that effects of emotionbegin during the search for a memory andcan vary with the valence of the event.

The Passage of Time Between Encodingand Retrieval: Effects of Consolidation

William James wrote, “An experience maybe so exciting emotionally as almost to leavea scar on the cerebral tissue” (James, 1890,p. 670). Indeed, the durability of emotionalmemories is one of their most compellingfeatures. Although not all details are retainedaccurately, in the longest test-retest study todate, Hirst et al. (2015) assessed memoryup to 10 years after the terrorist attacksof September 11, 2001. They reportedmaintained consistency and high levels ofconfidence for canonical features of thememory (e.g., where participants were whenthey learned of the attack, what they werewearing) between 3 and 10 years after theattacks. These findings corroborate numer-ous studies of flashbulb memories (Brown& Kulik, 1977) for highly emotional public


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events, which typically find a decline inconsistency and confidence over the first yearbut stabilization in memory thereafter (Hirstet al., 2015).

It does not take decades to see the selec-tively beneficial effects of emotion on mem-ory. The neural and behavioral enhancementof memory by emotion can be present evenminutes after an event has occurred (Dolcos,LaBar, & Cabeza, 2004; Kensinger &Corkin, 2004; Talmi & McGarry, 2012).However, the beneficial effects of emotionon recollection memory do tend to increaseover time (Sharot, Verfaellie, & Yonelinas,2007; Sharot & Yonelinas, 2008). This delaydependence was first noted by Kleinsmith andKaplan (1963) and has been corroborated by anumber of studies. For instance, Wang (2014)revealed a shallower forgetting curve for neg-ative images compared to neutral and positiveimages between a 24-hour and 1-week study-test delay, and Quevedo et al. (2003) foundenhanced memory for an emotionally arous-ing slide-show narrative compared to aneutral narrative after a 1 week—but not1 hour—delay. Similarly, Anderson, Yam-aguchi, Grabski, and Lacka (2006) foundenhanced memory for negatively arous-ing scenes (relative to neutral scenes)after a 2-week delay but not at earliertime points.

Often, this delay-dependent effect ofemotion arises because memory for neu-tral items decays at a faster rate over timethan does memory for emotional items(LaBar & Phelps, 1998; Sharot & Phelps,2004). The most likely explanation for theslower forgetting of emotional stimuli is thatcritical neurobiological consolidation pro-cesses take place shortly after learning tostabilize memory for long-term storage(McGaugh, 2000). For example, sleep-basedconsolidation processes when sleep is initi-ated shortly after learning—as compared tosleeping after 16 hours post-learning—have

been shown to enhance memory for emo-tional objects after a 24-hour delay (Payne,Chambers, & Kensinger, 2012). These datasupport a consolidation account, as opposedto an interference account, for emotionallyenhanced memory, because all participantswere awake for a similar amount of time(for more on the interference hypothesis andsleep-based consolidation see Chapter 4 inthis volume).

This slower forgetting curve for emo-tional items appears to depend on amygdalafunction (Phelps et al., 1998) coupled withpsychophysiological arousal (Andersonet al., 2006; Onoda, Okamoto, & Yamawaki,2009; Segal, Stark, Kattan, Stark, & Yassa,2012). For instance, Claire, Sophie, Claudia,Phillippe, and Eliane (2015) reported that, ascompared to control participants, a patientwith amygdala damage was impaired inthe recognition of emotional words after a1-week—but not 1-hour—delay (see alsoPhelps et al., 1998).

The amygdala-mediated effects on mem-ory consolidation have been extensivelyinvestigated, sparked by the pioneering workby Gallagher and Kapp (1981); Ellis andKesner (1983); Ledoux, Iwata, Cicchetti,and Reis (1988); and Cahill and McGaugh(1990, 1991). In animals and humans,arousal influences many forms of learningvia time-dependent effects of the adrenergic-noradrenergic, cholinergic, and opioid pep-tide systems—and their interactions—on theamygdala (see McGaugh, 2015, for a recentreview).

Electrophysiological studies have shownthat stimulation of the amygdala can inducelong-term potentiation—patterns of activ-ity that reflect synaptic plasticity relatedto learning—in the hippocampus (Ikegaya,Saito, & Abe, 1994, 1995) and vice versa(Maren & Fanselow, 1995). Recent worksuggests region-specific encoding of theemotional and contextual aspects of fear


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memory (a form of associative learningresulting from Pavlovian fear conditioning)in the amygdala and hippocampus, respec-tively, with the medial PFC integratingthese emotional and contextual components(Zelikowsky, Hersman, Chawla, Barnes, &Fanselow, 2014). However, although the hip-pocampus is a clear target for amygdalamodulation of memory storage, the amyg-dala also projects to many different brainregions (Young, 1993) and clearly is notacting in isolation to modulate the durabilityof emotional memories.

Hints as to the network of regions involvedhave come from neuroimaging studies exam-ining the processes needed for the creation ofdurable memories (see Murty et al., 2010, fora quantitative meta-analysis), which revealnot only the engagement of the amygdala butalso of PFC and sensory regions. For instance,Steinmetz et al. (2012) revealed activity inthe ventromedial PFC, fusiform gyrus, andhippocampus was an equally strong—orstronger—predictor of subsequent memoryfor emotionally arousing stimuli followinga retention delay of 24 hours comparedto 30 minutes. By contrast, these regions’ability to predict memory for neutral itemsdissipated with the longer retention inter-val. Parallel findings have been revealed atretrieval, with neuroimaging studies showingenhanced recollection ERP effects (Weymar,Low, & Hamm, 2011) and more amyg-dala and hippocampal engagement (Dolcos,LaBar, & Cabeza, 2005; Kalpouzos, Fischer,Rieckmann, Macdonald, & Backman, 2012)during delayed retrieval of negative eventscompared to neutral events. Although therole of these regions during encoding andretrieval continues to be debated (see “WhatIs the Role of the Amygdala in EmotionalMemory?”), together these studies begin tosuggest mechanisms to support the increasedlikelihood of retaining emotional memoriesover time.

Effects of Sleep on Emotional MemoryConsolidation

It is not just the amount of time that affectsthe likelihood of memory retention but alsowhether high-quality sleep was includedwithin the retention interval. An extensivebody of research has shown that the emo-tional memory advantage is boosted if thestudy-test interval includes a period of sleep(see Chapter 4 in this volume and also Alger,Chambers, Cunningham, & Payne, 2015;Diekelmann, Wilhelm, & Born, 2009). Thatboost may be particularly large if the sleepfollows soon after the occurrence of theemotional event (Payne et al., 2012).

Because sleep is thought to selectivelypreserve memories that have been “tagged”as relevant for the future during encoding (seeBennion, Mickley Steinmetz, Kensinger, &Payne, 2015; Payne & Kensinger, 2011),it makes sense that emotional informationmay be prioritized over periods of sleep.Indeed, this tagging process may be optimalwhen arousal levels are high during encoding(Bennion et al., 2015; Cunningham, Cham-bers, & Payne, 2014). At a neural level,sleep has been shown to facilitate plasticityin the amygdala, hippocampus, PFC, andsensory regions. Although the nature ofthis facilitation continues to be discussed(Bennion et al., 2015; Cairney, Durrant,Power, & Lewis, 2015; Sterpenich et al.,2014; van Marle, Hermans, Qin, Overeem,& Fernandez, 2013), it seems clear thatsleep can alter amygdala connectivity andaffect the likelihood of amygdala reactivationduring memory retrieval.

To date, most studies examining the effectof sleep on emotional memory have focusedon the role of rapid eye movement (REM)sleep (Groch, Wilhelm, Diekelmann, &Born, 2013; Wagner, Gais, & Born, 2001;Wiesner et al., 2015; see Walker, 2010, foran outline of the REM-sleep hypothesis;see van der Helm and Walker, 2011; and


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for comprehensive reviews, see Alger et al.,2015; Diekelmann et al., 2009). However,enhancing effects of slow-wave sleep (SWS)on memory consolidation are also frequentlyreported (Ackermann & Rasch, 2014) andhave been revealed for emotionally enhancedmemories as well as neutral ones (Cair-ney, Durrant, Hulleman, & Lewis, 2014;Eschenko & Sara, 2008; Groch et al., 2011;Kaestner, Wixted, & Mednick, 2013; Payneet al., 2015). It has recently been suggestedthat a parsimonious explanation might be thatSWS and REM sleep serve complementaryfunctions during sleep-dependent consolida-tion of emotional memories (Cairney et al.,2015; Payne et al., 2015). In alignment withthe sequential hypothesis for the effects ofsleep on memory (Giuditta, 1977, Giudittaet al., 1995; and for a more-recent reviewsee Giuditta, 2014), SWS might weaken thedependence of negative memories on the hip-pocampus before REM sleep preferentiallytargets negative memories for additional inte-grative and mnemonic processing. Together,SWS and REM sleep might give rise tothe enhancing effects of negative arousalon emotionally enhanced memory (Cairneyet al., 2015).

Although the majority of studies haveexamined the enhancement for negative stim-uli (relative to neutral stimuli), recent workhas also shown superior sleep-dependentmemory consolidation for positive stimuli(i.e., humorous cartoons) (Chambers &Payne, 2014). It will be advantageous forfuture research to examine whether theeffects of sleep on memory unfold similarlyfor all information with future relevanceor whether the emotional memory bene-fit may be related to unique mechanisms(and see Cunningham, Chambers, et al.,2014, for some evidence). Understandingthis issue will be critical for revealing howencoding goals and strategies interact with

emotion and can have downstream effects onretrieval, an issue that we expand on in thenext section.

Encoding-to-Retrieval Interactions

The effect of emotion on memory retrievalcan critically depend on what happened dur-ing encoding or consolidation. For instance,the likelihood of retrieving emotional stimulican be influenced by whether informa-tion was intentionally encoded (Chainay,Michael, Vert-Pre, Landre, & Plasson, 2012;Sakaki, Fryer, & Mather, 2014) and by thefuture relevance of the stimuli (Cunningham,Chambers, et al., 2014). The magnitude ofthe emotional memory benefit conveyed canalso be influenced by the emotion-regulationstrategies employed during encoding (Kim &Hamann, 2012) or by the memory-encodingstrategy (Murray & Kensinger, 2012). Thisinterdependence is perhaps unsurprising,because retrieval is thought to involve thereactivation of processes that are activeduring encoding. Indeed, emotional mem-ories are no exception to this rule; studieshave demonstrated amygdala reengagementduring retrieval of stimuli studied in emo-tional contexts (Smith et al., 2005) and haverevealed that negative valence increases theengagement of ventral visual processingregions during encoding and also the reen-gagement of those processes during retrieval(Kark & Kensinger, 2015).

Importantly, however, the effects of emo-tion at encoding do not always parallel thoseat retrieval. For instance, although there is nodoubt that emotionally arousing informationbenefits from prioritized or facilitated pro-cessing during encoding, this facilitatedprocessing does not always result in enhancedmemory (see Bennion et al., 2013, for furtherdiscussion). As one example, Murray andKensinger (2012) demonstrated that arousing


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Debates and Open Questions 15

content enabled participants to more rapidlyintegrate word pairs (i.e., to form a mentalimage that incorporated two unrelated items).Participants, however, were less likely toremember those arousing pairs over timethan they were to remember the neutral pairs.Murray and Kensinger (2013b) argued thatthe ease of integrating the arousing wordpairs may have circumvented the effortfulprocessing that would have translated into amore durable memory trace (see also Murray& Kensinger, 2013a). A related finding wasreported by Zimmerman and Kelley (2010):They showed that participants were overcon-fident when estimating which negative wordpairs they would remember. It is likely thatparticipants were fooled by the ease withwhich they had bound the items at encodingand were biased to believe that this easewould extend to their ability to retain thepairs in memory.

Another example of the interdependenceof encoding and retrieval comes from a studyby Sakaki et al. (2014), who showed thatmemory for neutral images seen immediatelybefore emotional images was enhanced ifparticipants were instructed to prioritizethe neutral images, but it was impaired ifthose neutral images were not prioritized. Inother words, the encoding orientation influ-enced the likelihood of later retrieval. Theeffects of prioritization exist not only whenthey are apparent at the time of encoding (asin Sakaki et al., 2014) but also when theyare revealed during the consolidation period.In a more-recent study, Dunsmoor, Murty,Davachi, and Phelps (2015) demonstratedthat neutral memories can be made moredurable if conceptually related informationlater becomes emotionally salient. Together,these studies show that goals and prioritiesduring encoding and consolidation can influ-ence the durability of a memory and thelikelihood of later retrieval success.

DEBATES AND OPEN QUESTIONS

The previous sections have noted key con-clusions that have been drawn from decadesof research into the interactions betweenemotion and memory, but there are manyquestions that remain. Here we highlightthree of those questions and the debatesthat have arisen as researchers have tried toanswer them.

What Is the Role of the Amygdalain Emotional Memory?

There have been two primary debates thathave been ongoing regarding the role of theamygdala in emotional memory. The firstrelates to the time course over which theamygdala exerts its effects. It is debatedwhether the amygdala plays a specific rolein the consolidation of emotional memoriesor whether its influence also is related to theinitial encoding or the eventual retrieval ofthose memories. As previously described,there is some evidence to support a consol-idation view, in that amygdala engagementappears to be a stronger predictor of memoryafter longer delays than shorter ones. Indeed,some research has suggested that the amyg-dala may not be necessary for emotionalmemory enhancements if memory is testedafter a short delay (see Talmi & McGarry,2012, for discussion). Yet other researchsuggests that amygdala activation may influ-ence the way that emotional information isprioritized during encoding, biasing atten-tion toward high-priority information (seeMather & Sutherland, 2011). There also areproposals to suggest that the amygdala mayfacilitate retrieval, working in concert withthe hippocampus to support the recollectionof emotional events via recapitulation of rep-resentations stored in neocortical regions (deVanssay-Maigne et al., 2011; Fenker, Schott,


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Richardson-Klavehn, Heinze, & Düzel,2005). Thus, although there is no doubtthat the amygdala is important for the con-solidation of emotional memory, questionsremain about its role during the encoding andretrieval of that information. Future work,possibly harnessing the high spatial and tem-poral resolution of intra-cranial recordings,is needed to disentangle whether amygdalaactivation at the moment of retrieval facili-tates successful retrieval itself or if amygdalaactivation is an emergent property of anemotional reaction to retrieved content. Itis also possible that the amygdala playsboth roles: Early amygdala activation mayguide retrieval and later amygdala activationduring retrieval may reflect an emotionalreaction to the retrieved memory content.

A second debate relates to how the amyg-dala influences the consolidation of memory.The traditional view (i.e., modulatory emo-tional consolidation theory) has been that theamygdala exerts its effects on consolidationthrough interactions with other MTL regionsand specifically the hippocampus (reviewedby Hamann, 2001; LaBar & Cabeza, 2006).This view has been supported by decades ofanimal research and many studies of humanmemory. For instance, amygdala activationhas been shown to lead to changes in synapticplasticity within the hippocampus (Ikegayaet al., 1994, 1995; Roozendaal & McGaugh,1997, 2011), and numerous studies haveshown that correlations between amygdalaand hippocampal activity predict the memoryenhancement for high-arousal stimuli, espe-cially after longer delays (Binder et al., 2012;Fastenrath et al., 2014; Richardson et al.,2004). Yet this view has recently been calledinto question with the proposal that the amyg-dala might—in the absence of interactionwith the hippocampus—create item-emotionbindings that are resistant to forgetting(Yonelinas & Ritchey, 2015). The authorsassert that, if the amygdala were to exert itseffects via modulation of the hippocampus,

evidence should show enhanced item-contextassociations of emotional memory and adisruption of emotional-memory longevityfollowing hippocampal damage. However,emotion appears to selectively enhancememory for items, not for their context, andpatients with hippocampal damage continueto show a time-dependent enhancement ofemotional memory. It is important to notethat this newer view posited by Yonelinasand Ritchey (2015) rests on the assump-tion that the hippocampus does not play arole in item memory but rather functions tobind items and their contexts in support ofstrong recollection over weaker familiarity(Diana, Yonelinas, & Ranganath, 2007). Incontrast with this item-context distinction,other work suggests that the hippocampussupports memory for multi-attribute stimuli,which could include, for example, visual,spatial, and emotional attributes (Wixted &Squire, 2011). Under the latter framework,the hippocampus supports stronger and weakmemory for attributes that may or may notbe construed as an item or a context. Furtherwork is needed to understand when and howhippocampal involvement enhances the var-ied constituent parts of emotional memories.

Clearly, further work is needed to clarifythe role of the amygdala in emotionallyenhanced memory, including the neurochem-ical mechanisms (e.g., Cahill, Gorski, & Le,2003; Mather, Clewett, Sakaki, & Harley,2015; Okuda, Roozendaal, & McGaugh,1997; Roozendaal, & McGaugh, 2004;) thatsupport the enhancement effect as well asthe extent and timing of amygdalae interac-tions with other MTL structures and corticalregions.

What Are the Effects of EmotionalArousal on Memory Accuracy?

As we discussed previously in this chapter,individuals often report high confidencein emotional memories yet show low


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Debates and Open Questions 17

consistency over time (Neisser & Harsch,1992; Schmidt, 2004; Schmolck, Buffalo,& Squire, 2000; Talarico & Rubin, 2003) oronly remember select details (for a review,see Kensinger, 2009). Clearly, emotionalevents do not leave indelible traces. Yetwhether emotional arousal provides anybenefits to memory for detail has continuedto be widely debated.

Some have argued that arousal enhancesonly the feeling of vividness but not theability to retrieve accurate content (reviewedby Phelps & Sharot, 2008). Relatedly, othershave argued that arousal biases individualsto endorse content as having been previouslyexperienced, but it does not enhance theability to discriminate studied from novelcontent (Dougal & Rotello, 2007). It is clearthat there are conditions in which arousingevents are remembered with different quali-tative characteristics (e.g., higher vividness)even when those events are rememberedat the same rates as neutral memories andwith the same, or lesser, objectively mea-surable detail (reviewed by Kensinger,2009). But what remains debated is whetherarousal only enhances these qualitativecharacteristics.

We suggest the need for future researchto attend to two types of factors in orderto resolve this debate. First, research mustcontrol for confounds between the emotionaland nonemotional stimuli. For instance,emotional stimuli are often more interre-lated than neutral stimuli, a factor that caninflate the likelihood that participants endorseemotional lures. When this interrelatednessis controlled, emotion may not enhancefalse memory (Choi, Kensinger, & Rajaram,2013). Other potential confounds to considerinclude attention allocation, distinctive-ness, and affective state of the participant(see Bennion et al., 2013, for elaboration).Second, research would benefit from con-sidering whether unmeasured memorycharacteristics may be affecting retrieval

decisions. It is likely that participants some-times report a vivid memory for an eventnot because they remember its content well,but because they remember their emotionalreactions well. These internal details areoften not measured yet are likely to influencememory decisions. Relatedly, participantsmay report a vivid memory because of theease with which a detail comes to mind ratherthan because of the quantity of details thatcome to mind. In most prior research, onlyone of these factors has been measured, andusually it has been the latter.

How Do Emotional Appraisalsand Reappraisals Affect MemoryPatterns?

Arousal and valence are not static and fixedproperties of an experience. Emotional regu-lation strategies can be used in everyday lifein order increase or decrease affective reac-tions to real-world situations (Gross, 1998).Interestingly, use of emotional strategiesduring the initial experience of an event canhave long-lasting effects on memory (Ahnet al., 2015; Hayes et al., 2010). Knowledgeacquired after an event can frequently changeour feelings toward and appraisal about anevent. As these appraisals change, it can behard for us to remember that we ever felt dif-ferently (reviewed by Levine & Safer, 2002).Although these effects are often described interms of biases and distortions, Levine andSafer (2002) have emphasized the utility ofupdating our memories to reflect our currentconceptions about an event. For instance,if we learn that an argument with a friendwas based on a misunderstanding, it is notadaptive for us to continue to reexperiencethe negative emotions that we felt at thetime of the conversation. More generally,if a main purpose of memory is to help usmake decisions and behave adaptively in thefuture, then it makes sense that our memorystores would serve us best if they contained


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the most up-to-date appraisals of rewards andthreats in our environment.

Despite the well-known ability for emo-tions to change over time, and even to bechanged in the moment of an emotionalexperience (Gross, 1998), relatively little isknown about how memory characteristicsand the neurobiology of memory consoli-dation and retrieval are influenced by thesereappraisals. For instance, if an event wasperceived as negative at the time of its occur-rence, but over time is reappraised as neutral,do the retrieval signatures now parallel thosefor neutral memories, or do some differ-ences remain based on the initial appraisal?The more that we conceive of memory as adynamic process, the more central these sortsof questions become to our understanding ofemotional memory.

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