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Cognitive Neuroscience of Emotional Memory Kevin S. LaBar, Ph.D. Center for Cognitive Neuroscience Duke University Stanford Law 2011 Outline of Talk Enhancing effects of emotion on declarative memory: basic laboratory paradigms encoding, consolidation, and retrieval effects of emotion regulation Enhancing effects of emotion on declarative memory: 'real-world' paradigms emotional memories of a complex sporting event emotional autobiographical memories (A) Psychological Theories of Emotion Categorical (evolutionary) (B) Dimensional (social-motivational) (C) Component Process (cognitive) APPRAISAL CRITERIA Novelty Pleasantness Goal significance: Outcome certainty Conduciveness Urgency Coping potential: Agency Control Power Adjustment JOY high high ANGER high open FEAR high low SADNESS low open high very high high very high conducive obstructive obstructive obstructive low high very high low self/other high high high other high high high other open very low low open very low very low medium Neurobiological theories of emotional memory Memory systems theories Memory modulation theories The amygdala mediates emotional arousal influences on a variety of memory systems LaBar & Cabeza, Nat Rev Neurosci, 2006 Experimental fMRI Encoding Paradigm 9=High Arousal High arousing & Unpleasant High arousing & Pleasant Low arousing & Neutral High Arousing & 1 Unpleasant [N=60] Unpleasant 1=Lo w 5 Neutral 9 Pleasant Valence Study: rate pleasantness Test: cued recall Low Arousing & Neutral [N=60] Dolcos, LaBar, & Cabeza, Neuron, 2004 High Arousing & Pleasant [N=60] Main Effect of Arousal on Amygdala Activation and Memory A. 35 # of pictures recalled 30 Z = -22 B. Left Amygdala Right Amygdala 25 20 15 10 % signal change 5 0.25 0.25 0.15 0.15 0.05 0.05 -0.05 -0.05 0 1 2 Pleasant 3 4 5 TR Pleasant 1 Unpleasant 2 3 4 5 TR Neutral Neutral Unpleasant Subsequent Memory Paradigm Difference Arousal Modulation of Subsequent Memory (Dm) Effect Meta-analysis of emotional encoding success studies Murty , Ritchey, Adcock & LaBar, Neuropsychologia, 2010 Emotion regulation and subsequent memory Encode negative pictures during fMRI under passive view, suppress, and reappraise (reduce personal relevance) conditions, as well as neutral (view) control pictures Test memory in 2-week delayed recognition test Behavioral results * Pannu Hayes et al., Front Human Neurosci, 2010 Emotion regulation and hippocampal subsequent memory effect Pannu Hayes et al., Front Human Neurosci, 2010 Remembering One Year Later: Role of the MTL in Retrieving Emotional Memories Does the MTL also participate in the successful retrieval of emotional items from long-term storage? • Successful Retrieval = Hits vs. Misses • Divide into recollection- and familiarity-based retrieval operations • Compare Emotional Successful Retrieval vs. Neutral Successful Retrieval Emotional Modulation of Retrieval Success Activity in MTL (Remember/Know combined) Dolcos, LaBar, & Cabeza, PNAS, 2005 Recollection- vs. Familiarity-Based Emotional Retrieval Success Activity * * Moving from the lab to the real world… “There should also be more interest in what people actually do (eat, have political views, watch television…), [and] more concern about whether the paradigmatic instances we choose for experimental analysis correspond to real-world events and are both robust and generalizable” Rozin, Perspectives Psychol. Sci., 2009 Retrieving emotional memories for a complex sporting event: The Duke -UNC Basketball Study Features of the experimental design Archived game (@UNC 2000) Valence is determined by opposing fan perspectives Select engaged fans of opposing teams Encoding conditions are controlled Assess memory for specific plays (detailed event memory) each play has an emotional outcome that fluctuates widely across trials Sample retrieval trial fMRI results: Arousal modulation Amygdala and hippocampus fMRI results: Arousal modulation Social cognitive/self-referential network Sensorimotor fMRI results: Valence effects Positive valence effect dorsal frontoparietal network Spatiotemporal dissociation of emotional intensity and reliving in autobiographical memory retrieval maintenance time 24 sec “emotion” “reliving” “cue word” eyes closed 1 2 3 4 MRT = 12.3 s Daselaar et al., Cereb Cortex, 2008 1 2 3 4 Emotion-specific variation Reliving-specific variation Amygdala Visual Cortex 5.00 5.00 T values 3.00 2.00 1.00 3.00 Emotion Reliving 2.00 1.00 0.00 0.00 -1.00 4.00 T values Emotion Reliving 4.00 retriev maint retriev maint phase1 phase2 phase1 phase2 -1.00 retriev maint retriev maint phase1 phase2 phase1 phase2 Early Role of Emotion During Memory Retrieval “When a subject is being asked to remember, very often the first thing that emerges is something of the nature of an attitude. The recall is then a construction, made largely on the basis of this attitude, and its general effect is that of a justification of the attitude,” where for Bartlett attitude is “very largely a matter of feeling, or affect.” Bartlett (1932/1995) Conclusions Emotional memory is a multidimensional construct Amygdala-MTL interactions are important for long-term encoding and retrieval of emotionally intense episodes, with additional support from frontoparietal and sensory regions Emotion regulation strategies modify activity in this network These interactions extend to more complex, real-world memories where emotion has a broader reach over social cognitive and sensorimotor networks Emerging VR technologies may be beneficial to reveal how real-world contexts regulate the expression of emotional memories Acknowledgements Research support: NIH R01 DA14094, R01 AG023123; NSF CAREER Award Collaborators: Alison Adcock, Anne Botzung, Rachael Brady, Roberto Cabeza, Sander Daselaar, Florin Dolcos, Daniel Greenberg, Amanda Miles, Gregory McCarthy, Rajendra Morey, Jasmeet Pannu Hayes, Heather Rice, David Rubin, Moria Smoski, Holton Thompson, David Zielinski LaBaratory: Jose Alba Hernandez, Matthew Fecteau, Nicole Huff, Phil Kragel, Vishnu Murty, Maureen Ritchey No conflicts of interest to report Future directions: Virtual emotional memories Duke immersive Virtual Environment (DiVE) MTL Activation During Retrieval of Emotional Autobiographical Memories • Pre-scan cue generation method • Compare autobiographical vs. semantic retrieval AM SM Anterior Posterior Anterior Posterior Greenberg, Rice, Cooper, Cabeza, Rubin & LaBar, Neuropsychologia, 2005 How Can Cognitive Neuroscience Contribute? Two central issues in emotional memory research (Schooler & Eich, 2000) 1. Whether emotion enhances or diminishes the strength of memory for an event 2. Whether special mechanisms are required to account for the effects of emotion on memory 3. Whether emotion affects the subjective experience of remembering Historical interest: Emotion and memory Francis Bacon: Facts connected with strong feelings were easier remembered than indifferent facts Descartes: Emergence of memories is brought about by the passions Rappaport, Emotions and Memory, 1950 S.P. Arousal-Mediated Memory Consolidation Deficits Following Bilateral Amygdala Damage # words recalled LaBar & Phelps, Psychol Sci, 1998 R L