UNC 2013

Cognitive neuroscience of emotional memory

Kevin S. LaBar, Ph.D.

Center for Cognitive Neuroscience Department of Psychology & Neuroscience

Department of Psychiatry & Behavioral Sciences

Duke University Durham, NC USA

The problem space: Defining the intersection of emotion and memory

- Cognitive/Social - Evolutionary/Developmental

- Neurobiological

Theories of Emotion - Cognitive/Social

- Evolutionary/Developmental - Neurobiological

Theories of Memory

Psychological theories of emotion

(A)

(B)

APPRAISAL CRITERIA JOY ANGER FEAR SADNESS Novelty high high high low Pleasantness high open low open Goal significance: Outcome certainty high very high high very high Conduciveness conducive obstructive obstructive obstructive Urgency low high very high low Coping potential: Agency self/other other other open Control high high open very low Power high high very low very low Adjustment high high low medium

(C)

Categorical (evolutionary)

Dimensional (social-motivational)

Component Process (cognitive)

Memory systems theories

Squire & Zola, 1996

Memory processing stages

Encoding Storage Retrieval

Consolidation Reconsolidation

Are there neurobiological 'laws' of emotional memory ?

1. The amygdala forms conditioned fear associations between predictive cues and aversive reinforcers (LeDoux, 1996)

2. The amygdala modulates the consolidation of memories of emotionally arousing experiences (McGaugh, 2004)

Memory modulation theories

Eichenbaum & Cohen, 2001

Memory systems theories

Squire & Zola, 1996

Neurobiological 'laws' of emotional memory

Outline of Talk

Role of the amygdala in fear conditioning

The memory modulation hypothesis Foundational studies "Beyond the MMH": Retrieval, phenomenology & real-

world events

Outline of Talk

Role of the amygdala in fear conditioning

The memory modulation hypothesis Foundational studies Beyond the MMH: Retrieval, phenomenology & real-

world events

Human fear conditioning paradigm

LaBar & LeDoux, Understanding Autism, 2006

Impaired fear conditioning in amygdala-lesioned patients

Bechara et al., Science, 1995 Phelps et al., Neurocase, 1998

R

S.P. Control

SP

Functional neuroimaging studies reveal thalamo-amygdalo-cingulate network for acquiring fear

LaBar & Cabeza, Nat Rev Neurosci, 2006

Büchel et al., Neuron, 1998

Amygdala

Cor

rela

tion

coe

ffic

ient

Cheng et al., Behav Neurosci, 2003

Furmark et al., NeuroReport, 1997 LaBar et al., Neuron, 1998

Amygdala activity correlates with SCR indices of fear learning

SCR

Outline of Talk

Role of the amygdala in fear conditioning

The memory modulation hypothesis Foundational studies Beyond the MMH: Retrieval, phenomenology & real-

world events

The memory modulation hypothesis

Roozendaal & McGaugh, Behav Neurosci, 2011

Peripheral

Central

Evidence for amygdala involvement and stress hormone modulation

Adapted from Cahill et al., 1994, 1995

Memory consolidation for arousing words following amygdala damage

Phelps et al., Neurocase, 1998; LaBar & Phelps, Psychol Sci, 1998

reca

ll

R

*

Subsequent Memory Paradigm

Difference

Experimental Paradigm

ValenceUnpleasant Neutral Pleasant1 5 9

1=Low

9=High

Aro

usal

High arousing & Unpleasant

High arousing & Pleasant

Low arousing & Neutral

ValenceUnpleasant Neutral Pleasant1 5 9

1=Low

9=High

Aro

usal

ValenceUnpleasant Neutral Pleasant1 5 9

1=Low

9=High

Aro

usal

High arousing & Unpleasant

High arousing & Pleasant

High arousing & Unpleasant

High arousing & Pleasant

Low arousing & Neutral

High Arousing & Pleasant [N=60]

High Arousing & Unpleasant [N=60]

Low Arousing & Neutral [N=60]

Study: rate pleasantness Test: cued recall

Dolcos et al., Neuron, 2004

Left Amygdala Right Amygdala B.

A.

Pleasant Neutral Unpleasant

-0.05

0.05

0.15

0.25

1 2 3 4 5-0.05

0.05

0.15

0.25

1 2 3 4 5 TR TR

% s

igna

l cha

nge

Z = -22

0

5

10

15

20

25

30

35

# of

pic

ture

s re

calle

d

Pleasant Neutral Unpleasant0

5

10

15

20

25

30

35

# of

pic

ture

s re

calle

d

Pleasant Neutral Unpleasant

Main Effect of Arousal on Amygdala Activation and Memory

Amygdala-MTL Interactions

Predict Successful Emotional

Memory Encoding

Meta-analysis of emotional encoding success studies

Murty et al., Neuropsychologia, 2010 P < .05, FDR-corrected

Beyond the Memory Modulation Hypothesis: Role of the MTL in retrieving emotional memories

• Successful Retrieval = Hits vs. Misses

• Compare Emotional Successful Retrieval vs. Neutral Successful Retrieval

• Minimize contribution of emotional perception-related activation

Does the MTL also participate in the successful retrieval of emotional items from long-term storage?

Emotional modulation of retrieval success activity in MTL

Dolcos et al., PNAS, 2005

Emotion selectively enhances memories accompanied by a sense of recollection

*

Participants performed remember/know judgment

Recollection- vs. familiarity-based emotional retrieval success activity

* *

“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

Moving from the lab to the real world…

Recollection of autobiographical memories engages MTL

Greenberg et al., Neuropsychologia, 2005

Anterior Anterior Posterior Posterior

Autobiographical Retrieval Category Generation

Emotional arousal predicts autobiographical memory experience

BASIC COMPLEX

Arousal Valence Arousal Valence

Autobiographical Memory-specific

reliving .50* .08 .57* .29*

remember vs. know .32 -.02 .44* .07

own eyes vs. observer .32 -.05 .44* .06

specific vs. generic .30 -.12 .29 .03

vividness .57* .03 .55* .10

narrative .29 .08 .53* .12

language .34* -.11 .50* .06

rehearsal .31 -.02 .44* -.05

confidence .29 -.04 .13 .05

Emotion-specific

same intensity .79* .04 .83* .11

same emotion .72* .04 .73* .09

visceral .58* -.01 .62* .04

Talarico et al., Mem. Cognit., 2004

Spatiotemporal dissociation of emotional intensity and reliving in autobiographical memory

“cue word”

time

“emotion” “reliving”

retrieval maintenance

N=80 eyes closed

24 sec

1 2 3 4 1 2 3 4

Memot = 2.3 Mreliv = 2.5 MRT = 12.3 s

Daselaar et al., Cereb Cortex, 2008

-1.00

0.00

1.00

2.00

3.00

4.00

5.00

-1.00

0.00

1.00

2.00

3.00

4.00

5.00

T va

lues

T va

lues

Emotion Reliving

Emotion Reliving

retriev maint retriev maint retriev maint retriev maint

Visual Cortex Emotion-specific variation Reliving-specific variation

Amygdala

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)

Retrieving emotional memories for a complex sporting event: The Duke -UNC Basketball Study

Features of the experimental design

Archived game (@UNC 2000) Encoding conditions are controlled and realistic Valence is determined by opposing fan perspectives Select engaged fans of opposing teams ('fandom') Assess memory for specific plays (detailed event

memory) each play is a narrative element marker within the more

complex event time series need lots of trials for signal averaging requirements each play has an emotional outcome that fluctuates widely

across trials; valence unknown until outcome recalled plays are important to oral tradition and statistics of sport

Sample retrieval trial

fMRI results: Arousal modulation Amygdala and hippocampus

SPM: parametric model FIR model High vs. low SPM contrast

fMRI results: Arousal modulation

Mentalizing/self-referential network Sensorimotor

fMRI results: Valence effects

Positive valence effect Positive valence X Confidence interaction

dorsal frontoparietal network

May 31, 2009 Upon losing in the 4th round of the 2009 French Open after 31 consecutive wins and 4 consecutive titles, Rafael Nadal said "We know that when we walk on the court, we can either win or lose. No one remembers defeats in the long run. People remember victories. So I have to move forward."

Conclusions

Emotional memory is a multidimensional construct

The amygdala is critical for fear conditioning

Amygdala-MTL interactions are critical for the consolidation of emotionally arousing episodes into long-term memory, as well as their retrieval

These interactions extend to complex, real-world memories where emotion has a broader reach over phenomenological aspects of recollection and social cognitive and sensorimotor networks

Valence effects on memory involve frontal and MTL regions but the amygdala is not critical

Funding NIH 2 P01 NS041328 NIH R01 DA027802 NSF 0745919

http://mind.duke.edu

Trainees Fredrik Åhs Nineequa Blanding Joseph Dunsmoor Jose Alba Hernandez Nicole Huff Matt Fecteau Philip Kragel Vishnu Murty Steven Prince Maureen Ritchey

Collaborators Anne Botzung Roberto Cabeza Sander Daselaar Daniel Greenberg Joseph LeDoux Amanda Miles Elizabeth Phelps Heather Rice David Rubin Jennifer Talarico