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Following the Crowd: Brain Substrates of Long-Term Memory Conformity

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Human memory is strikingly susceptible to social influences, yet we know little about the underlying mechanisms. We examined how socially induced memory errors are generated in the brain by studying the memory of individuals exposed to recollections of others. Participants exhibited a strong tendency to conform to erroneous recollections of the group, producing both long-lasting and temporary errors, even when their initial memory was strong and accurate. Functional brain imaging revealed that social influence modified the neuronal representation of memory. Specifically, a particular brain signature of enhanced amygdala activity and enhanced amygdala-hippocampus connectivity predicted long-lasting but not temporary memory alterations. Our findings reveal how social manipulation can alter memory and extend the known functions of the amygdala to encompass socially mediated memory distortions.
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DOI: 10.1126/science.1203557
, 108 (2011);333 Science , et al.Micah Edelson
Conformity
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Following the Crowd: Brain Substrates
of Long-Term Memory Conformity
Micah Edelson,
1
*Tali Sharot,
2
Raymond J. Dolan,
2
Yadin Dudai
1
Human memory is strikingly susceptible to social influences, yet we know little about the
underlying mechanisms. We examined how socially induced memory errors are generated in the
brain by studying the memory of individuals exposed to recollections of others. Participants exhibited a
strong tendency to conform to erroneous recollections of the group, producing both long-lasting
and temporary errors, even when their initial memory was strong and accurate. Functional brain
imaging revealed that social influence modified the neuronal representation of memory. Specifically,
a particular brain signature of enhanced amygdala activity and enhanced amygdala-hippocampus
connectivity predicted long-lasting but not temporary memory alterations. Our findings reveal
how social manipulation can alter memory and extend the known functions of the amygdala to
encompass socially mediated memory distortions.
Our memories are often inaccurate. Ubiq-
uitous sources of false recollection are
social pressure and interpersonal influ-
ence (14). This phenomenon, dubbed memory
conformity(4), is encountered in a variety of
contexts, including social interactions, mass me-
dia exposure, and eyewitness testimony. In such
settings an individual may change veridical re-
collections of past events to match a false ac-
count provided by others (16). Although these
social influences on memory have been exten-
sively demonstrated (15), the underlying neuro-
biology of this process is unknown.
Conformity may present in two forms, which
initially convey similar explicit behavior but are
fundamentally different (7,8). In one type, known
as private conformity, an individuals recollec-
tion may genuinely be altered by social influ-
ence, resulting in long-lasting, persistent memory
errors (1,4,5,7). In such circumstances, even
when social influence is removed, the individ-
uals will persist in claiming an erroneous mem-
ory as part of their own experience (7,9). Private
conformity could hence be considered a bona fide
memory change. In the second type, known as
public conformity, individuals may choose to out-
wardly comply, providing an account that fits
that of others, but inwardly maintain certitude
in their own original memory. Public conformity
can be dispelled when the veracity of the socially
transferred information abates (7,10,11). Thus,
errors induced by public conformity are tran-
sient (7,9) and appear to represent a change in
behavior in the absence of lasting alterations to
a memory engram.
Although private and public memory con-
formity are often behaviorally indistinguishable,
they reflect different cognitive processes (7,8).
These processes are probably mediated by dis-
tinct activation in interconnected brain circuits
previously found to be active in mnemonic func-
tions and social cognition (such as the hippo-
campal complex, amygdala, and frontal regions)
(1218). Here, we set out to characterize the brain
mechanisms that lead to both types of conformity.
Our experimental protocol included four phases
spanning a 2-week period (Fig. 1A). Thirty adult
participants (12 females, age 28.6 T0.8, mean T
SEM) viewed an eyewitness-style documentary
on a large screen in groups of five. Three days
after viewing, participants returned to the lab in-
dividually and completed a memory test (test 1).
Test 1 served to assess the participantsbaseline
accuracy and confidence before the manipulation
stage. Four days later, participants returned to the
lab and answered the same memory questions
while being scanned with functional magnetic
resonance imaging (fMRI) (test 2). On this oc-
casion, a manipulation was introduced in an
attempt to induce conformity.
Before responding during this test, partici-
pants were presented with answers they were
led to believe were given by their four fellow co-
observers, whose photographs were provided
with their corresponding answers (Fig. 1A). In
a subset of trials, for which the target participant
originally had a confident veridical memory (as
identified by test 1), the answers provided by
the four co-observes were all false (manipulation
condition, 80 questions). In matched control trials,
the letter X was presented instead of the co-
observersanswers (no-manipulation condition,
25 questions). Pilot data indicated that the use
of manipulation and no-manipulation conditions
alone would raise suspicion in the participants
minds that the answers given by the co-observers
were fabricated. Therefore we added credibility
trials in which different patterns of co-observer
answers were provided (Fig. 1B).
One week later, the participants returned
to the lab and were informed that the answers
given by the co-observers during the previous
fMRI session were in fact determined random-
ly. This rendered the socially conveyed infor-
mation previously provided as uninformative.
The participants were then requested to com-
plete the memory test again (test 3) based on
their original memory of the movie. Finally, the
participants were debriefed. Participants with
excessive head movements in the scanner or
suspected brain pathology and those that indi-
cated suspicion of the manipulation were ex-
cluded from the analysis, resulting in a final
number of participants (N) = 20.
Our behavioral data revealed that our manip-
ulation induced memory errors (Fig. 2A). Strik-
ingly, participants conformed to the majority
opinion in 68.3 T2.9% of manipulation trials,
giving a false answer to questions they had pre-
viously answered correctly with relatively high
confidence. This was not due to forgetting, be-
cause in the no-manipulation condition, incorrect
answers were given in only 15.5 T1.7% of the
questions [Studentsttest (df 19) = 16.9, P<10
7
].
When social influence was removed (test 3), par-
ticipants reverted to their original correct answer
in 59.2 T2.3% of the previously conformed trials
(transient errors) but maintained erroneous an-
swers in 40.8% (persistent errors). Confidence
ratings in persistent and transient errors did not
differ either before or after the manipulation stage
(Fig. 2B). During the manipulation stage, con-
fidence ratings in transient errors were signifi-
cantly lower than in persistent errors [t(19) = 6.9,
P<10
5
]. Differences in confidence levels were
controlled for in the fMRI analysis by means of a
covariate [supporting online material (SOM)].
Our brain imaging data indicated that at
the time of exposure to social influence, distinct
brain signatures characterized instances of mem-
ory conformity that would result in persistent
and transient errors. We first performed analysis
on a priori anatomically defined regions of in-
terest (ROIs) selected by virtue of being widely
implicated in memory encoding and maintenance
(the bilateral anterior hippocampus, bilateral pos-
terior hippocampus, and bilateral parahippocam-
pal gyrus) and in social-emotional processing
(bilateral amygdala) (1225). Brain activity was
averaged across all voxels in each ROI for the
three conditions of interest (persistent errors, tran-
sient errors, and instances when participants
did not conform to the erroneous information;
i.e., nonconformity). In all regions, except for the
left posterior hippocampus, the blood oxygen
leveldependent (BOLD) signal was greater
during trials that subsequently resulted in persist-
ent memory errors relative to trials that resulted in
transient errors or nonconformity (Fig. 3A). No
significant difference was found between transient
error and nonconformity trials in these regions.
To examine whether other brain regions dif-
ferentiate between persistent and transient errors,
we conducted a whole-brain exploratory analy-
sis. Greater activity during trials resulting in per-
sistent errors versus trials resulting in transient
errors was found in four regions, all in the medial
temporal lobe (MTL, Fig. 3B): the left amygdala
(22,8,10), right hippocampus (28,22,12),
right parahippocampal gyrus (PHG, 36,48,10),
and a region bordering the left PHG and occipital
1
Department of Neurobiology, Weizmann Institute of Science,
Israel.
2
Wellcome Trust Centre for Neuroimaging, Institute of
Neurology, University College London, London, UK.
*To whom correspondence should be addressed. E-mail:
micah.edelson@weizmann.ac.il
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cortex (22,54,10), [P< 0.001, cluster thresh-
old (k) > 10]. In the opposite comparison (transient
versus persistent errors), enhanced activation was
found in the bilateral dorsal anterior cingulate cor-
tex (ACC, Brodmann area 32; 12,22,42; 8,20,46).
A striking activation in both aforementioned
analyses was found in the left amygdala. A be-
havioral control study (SOM) indicated that el-
evated activation in the amygdala during trials
that resulted in persistent errors was not due to
heightened emotional arousal during these trials.
Nor were these errors related to questions asso-
ciated with greater emotional content. Rather,
heightened amygdala activation seemed specific
to socially induced memory change.
The amygdala plays a key role in social and
emotional processing and modulates memory-
related hippocampal activity (1323). It is strate-
gically placed for this function, having rich
anatomical connections with the hippocampal
complex (the anterior hippocampus in particular)
as well as with neocortical areas (1316,23,26).
The amygdala is thus a prime candidate for
mediating social effects on memory, most likely
involving its interactions with other brain re-
gions (13,14). This consideration motivated us
to carry out a functional connectivity analysis,
using a psychophysiological interaction (PPI) ap-
proach (27). This analysis showed heightened
functional connectivity between the left amyg-
dala and bilateral anterior hippocampus within
anatomically defined ROIs, during trials that sub-
sequently resulted in persistent memory errors as
opposed to transient errors and nonconformity
(Fig. 4A).
We also sought to identify which brain re-
gions responded to the information presented
by the co-observers (SOM). To this end, trials in
which misleading information was presented
What did the policeman do?
1) Arrest a child 2) Arrest a man
2 sec
What did the policeman do?
1) Arrest a child 2) Arrest a man
Arrest a
man
Arrest a
man
Arrest a
man
Arrest a
man
2.5 sec
Protocol B Experimental conditions
Co-observer
answers
displayed
2.5 sec
Response
self paced
2 sec
3 sec
Self paced
What did the policeman do?
1) Arrest a child 2) Arrest a man
Arrest a
man
Arrest a
man
Arrest a
man
Arrest a
man
Manipulation
What did the policeman do?
1) Arrest a child 2) Arrest a man
Arrest a
child
Arrest a
child
Arrest a
child
Arrest a
child
Credibility
What did the policeman do?
1) Arrest a child 2) Arrest a man
XX
XX
No-manipulation
(correct answer = arrest a child)
What did the policeman do?
1) Arrest a child 2) Arrest a man
Arrest a
man
Arrest a
man
arrest a
man
How confident are you
in your answer ?
Guess Low
050100
Medium High Absolute
Movie (day 0)
Test 1 (day 3)
Test 2 (day 7)
memory prior to
manipulation
social manipulation
in scanner
Test 3 (day 14)
detection of persistent and
transient errors
in scanner
A
Fig. 1. Experimental outline. (A) Participants viewed the movie in groups
of five and subsequently performed three memory tests individually. Test
1 served to assess the participantsinitial memory and confidence before
the social manipulation administered in test 2. Test 3 served to identify
memory errors that persisted after the social manipulation was removed.
For the test 2 scanning session, the question and possible answers were
presented for 2.5 s, followed by the fabricated co-observersanswers for
2.5 s. Subsequently, a font color change indicated that the participants were
allowed to respond. Finally, confidence ratings were provided. (B)Illustration
of the different experimental conditions: the manipulation condition in which
all co-observersanswers were incorrect, the no-manipulation condition in
which the letter X was displayed instead of co-observersanswers, and the
credibility condition in which variable patterns of co-observersanswers were
displayed (SOM).
www.sciencemag.org SCIENCE VOL 333 1 JULY 2011 109
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(the manipulation condition) were contrasted with
the no-manipulation condition. Five regions (fig.
S1A) were identified in the frontal and occipital
cortex. Further analysis of brain activity in these
regions (fig. S1B) suggests that they are involved
in non-mnemonic processes, such as conflict
monitoring (2831) in the face of competing
memories (3234).
Were our findings driven merely by the pre-
sentation of additional information regardless of
social context? To answer this question, we per-
formed a control fMRI experiment using a non-
social medium to convey misinformation (SOM).
Participants underwent a similar protocol to that
of our main experiment. However, in memory test
2, instead of receiving answers from co-observers,
participants were told that the information origi-
nated from four different computer algorithms,
a common technique used to control for social
effects (30). Conformity in this case was signifi-
cantly lower (45.3 T4.7%) than in the social
manipulation described earlier (68.3 T2.9%) but
significantly higher than with no manipulation
at all (15.0 T2.4%) [t(38) = 4.2 and t(19) = 5.7,
respectively; P< 0.0002)].
Analysis of BOLD signal in the a priori
MTL ROIs revealed an interaction between mem-
ory (persistent errors and transient errors) and
experimental manipulation (social and nonsocial)
in the bilateral amygdala (P< 0.05). This inter-
action was driven by greater activation in trials
resulting in persistent memory errors relative to
transient errors in the social manipulation, but not in
the nonsocial manipulation (Fig. 3A). These re-
sults suggest that enhanced activity in these regions
is related specifically to socially induced persistent
memory errors. In contrast, the right anterior and
posterior hippocampus and left PHG revealed a
main effect of memory (P<0.05),wheretherewas
greater activity during trials resulting in persistent
relative to transient errors regardless of manipu-
lation type (P<0.05)(Fig.3A).Thus,theBOLD
signal in these regions was associated with long-
lasting memory errors irrespective of the medium
by which information was conveyed. Results of
a functional connectivity analysis between the
left amygdala and bilateral anterior hippocam-
pus showed a significant interaction (P<0.05).
Heightened connectivity was seen during trials that
resulted in persistent errors relative to transient
errors, a pattern specific to the social manipulation
(Fig. 4B). Our control experiments results hence
indicate that heightened amygdala activation and
enhanced connectivity with the hippocampus are
specific to socially induced memory changes,
whereas hippocampal complex activation differ-
entiates between persistent and transient errors
regardless of the source of influence.
Our results indicate that memory is highly
susceptible to alteration due to social influence,
creating both transient and persistent errors.After
over a century of intensive behavioral research
into social influences on memory (35), this study
now provides a brain account of this phenome-
non. Our findings suggest a mechanism by which
social influence produces long-lasting alterations
in memory, and they highlight the critical role of
the amygdala in mediating this influence.
Although at the time of social influence on
memory overt behavior was indistinguishable,
transient and persistent errors nevertheless in-
Test 2
manipulation Test Test Test Test
Test 3
post-debrief
Test 1
pre-manip
123 123 123 123
80
40
0
80
40
0
% Error
BA
Non-conformity
No-manipulation
Persistent error
Transient error
No-manipulation
*
*
*
Manipulation
Confidence
Fig. 2. Behavioral results. (A) Conformity level in the social manipulation condition was 68.3% versus 15.5%
in the no-manipulation condition [t(19) = 16.9, P<10
7
]. In test 3, participants reverted back to their original
correct answer in 59.2% of the previously conformed-to events (transient errors) and on 40.8% maintained
their erroneous answer (persistent memory error). The error rate was significantly different in test 3 between the
manipulation and no-manipulation conditions [ t(19) = 3.7, P< 0.002]. The questions included in the
manipulation and no-manipulation trials were those for which participants gave correct answers in test
1 with medium-high confidence. (B) Confidence ratings over time for differential trial types (*P<0.002).
0.15 ** **
-0.15
∆β
∆β
0
0.15 **
-0.15
0
0.15
-0.15
0
0.15 **
-0.15
∆β
∆β
0
0.15 ****
**
-0.15
0
0.3
-0.2
0
0.05
*
*
-0.2
∆β
∆β
0
0.05
*
**
-0.2
0
0.15
-0.2
0
L amyg
R ant hipp L ant hipp
R PHG L PHG
R amyg
R ant hipp
L PHG
Non-social
ABPredetermined ROIs Whole brain
analysis
L amyg
Social
y = -4
L amyg
R hipp
x = 28
PHG
z = -6
Transient errors Persistent errorsNon-conformity
Fig. 3. MTL activation during manipulation predicts long-term socially induced memory errors. (A)BOLD
signal in anatomically a priori defined MTL regions. L, left; R, right; In the social manipulation, enhanced
activation was found during trials that subsequently resulted in persistent errors relative to all other con-
ditions in the bilateral hippocampal complex and amygdala. In the nonsocial manipulation, this pattern was
evident in the hippocampal complex but not in the bilateral amygdala. (B) Whole-brain exploratory analysis
in the social manipulation (P<0.001,k> 10) revealed greater activity in persistent error versus transient
error conditions in the left amygdala, right hippocampus, right PHG, and left PHG bordering on the
occipital lobe. All areas also survived small volume correction for multiple comparisons (familywise
error < 0.05). The baseline in all figures is the no-manipulation condition (*P< 0.05 **P< 0.005).
1 JULY 2011 VOL 333 SCIENCE www.sciencemag.org
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duced distinct brain signatures. Heightened acti-
vation in the hippocampal complex was seen
when false information induced a long-lasting
change in the participantsmemories regardless
of social context. The hippocampal complex ac-
tivation we observed may represent a process
of reconsolidation (36) or encoding of new stable
representations [e.g., gist (37)]. In contrast, tran-
sient changes did not activate areas known to
be crucial for memory processing. Our findings
provide neurobiological evidence for the classic
assertion that private conformity is accompanied
by actual changes in beliefs, whereas public dis-
plays of conformity are not (7,8,10, 38).
Enhanced activation in the bilateral amygdala
and heightened functional connectivity with the
anterior hippocampus were a signature of long-
term memory change induced by the social envi-
ronment. This indicates that the incorporation
of external social information into memory may
involve the amygdalas intercedence, in accord-
ance with its special position at the crossroads
of social cognition and memory (13,14,16).
Multiple formal models have proposed
trace attributes that might contribute to mem-
ory distortion in different false memory protocols
(37, 3941). These postulated attributes refer, for
example, to potential heterogeneity in episodic
content and the persistence of memory trace el-
ements. Our laboratory analog to socially induced
memory distortion was not intended to distinguish
between specific models. However, further ex-
ploitation of our protocol, combined with cross-
fertilization of behavioral and brain data, might
contribute to the refinement of current models
and better understanding of the biological and
cognitive mechanisms of memory conformity.
Altering memory in response to group in-
fluence may produce untoward effects. For ex-
ample, social influence such as false propaganda
can deleteriously affect individualsmemory in
political campaigns and commercial advertising
(1,2,6) and impede justice by influencing eye-
witness testimony (2,4, 5). However, memory
conformity may also serve an adaptive purpose,
because social learning is often more efficient
and accurate than individual learning (42). For
this reason, humans may be predisposed to trust
the judgment of the group, even when it stands
in opposition to their own original beliefs. Such
influences and their long-term effects, the neu-
robiological basis of which we describe here,
may contribute to the extraordinary levels of per-
sistent conformity seen in authoritarian cults and
societies.
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Acknowledgments: M.E. was supported by a Weizmann
InstituteUK Grant. T.S. is supported by a British Academy
Postdoctoral Fellowship. R.J.D is supported by a Wellcome
Trust Program Grant. Y.D. is supported by the Nella and
Leon Benoziyo Center for Neurological Diseases. We thank
A. Ben-Yakov, J. G. Edelson, T. Fitzgerald, O. Furman,
S. Fleming, D. Levi, M. Guitart-Masip, A. Mendelsohn,
U. Nili, A. Pine, J. S. Winston, and N. Wright for helpful
comments and the support teams of the Norman and
Helen Asher Center for Brain Imaging at the Weizmann
Institute and the Imaging Neuroscience & Theoretical
Neurobiology unit in the Wellcome Trust Center for
Neuroimaging.
Supporting Online Material
www.sciencemag.org/cgi/content/full/333/6038/108/DC1
Materials and Methods
Fig. S1
Table S1
References
31 January 2011; accepted 12 May 2011
10.1126/science.1203557
Fig. 4. Amygdala-hippo-
campal functional connec-
tivity during manipulation
predicts long-term social-
ly induced memory errors.
(A) Social manipulation.
Functional connectivity be-
tween the left amygdala
and bilateral anterior hip-
pocampus was heightened
in the persistent error con-
dition relative to all other
conditions. (B)Nonsocial
manipulation. No condition-
dependent difference in
functional connectivity be-
tween the left amygdala
and bilateral anterior hip-
pocampus was found. The
baseline in all figures is the
no-manipulation condition (*P< 0.05). The inset depicts the anatomical ROIs used in the aforementioned
analyses.
0.8 **
-0.4
∆β∆β
0
0.8 **
-0.4
0
L ant hipp & L amyg R ant hipp & L amyg
L ant hipp & L amyg R ant hipp & L amyg
ASocial
BNon-social
0.3
-0.4
0
0.4
0
Transient errors Persistent errorsNon-conformity
www.sciencemag.org SCIENCE VOL 333 1 JULY 2011 111
REPORTS
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... O papel das influências normativa e informacional na conformidade de memória foi demonstrado repetidas vezes. Infere-se que a conformidade ocorreu devido a influência normativa quando um participante segue o confederado de forma pública, mas reverte sua resposta para a resposta original de forma privada (Edelson et al., 2011). Indivíduos com maior medo de avaliação social negativa tendem a mostrar maior conformidade (Wright et al., 2010), enquanto que indivíduos com maior tendência a evitar interações sociais tendem a mostrar menor conformidade , padrão de resultados consistente com a hipótese de influência normativa na magnitude do efeito. ...
... A influência normativa também tende a ser maior quando as consequências de se cometer um erro de memória são baixas (Baron et al., 1996). Em termos neurobiológicos, a conformidade por influência normativa tem sido associada à maior ativação em circuitos cerebrais envolvidos na detecção de conflito de informações (córtex cingulado anterior; Deuker et al., 2013;Edelson et al., 2011) e à ação do hormônio ocitocina (Edelson et al., 2015). ...
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A syndrome consisting of "agnostic" disturbances, strong "oral" tendencies, and marked emotional changes resulted from bilateral temporal lobectomy in 3 rhesus monkeys. The "agnostic" disturbances appeared in the form of hyper-attention to seen objects, with repeated manipulation of all objects irrespective of importance. This manipulation tended to take an "oral" form. Social behavior was markedly decreased, behavior characteristic of anger, fear, etc. largely disappeared, and a persistence of attentive action appeared. The "agnostic" symptoms were primarily visual, but some evidence appeared for the meaninglessness of perceptions in other sensory fields. Slight visual disturbances present after operation could not have accounted for the agnostic disturbances. This report, given as preliminary evidence, is detailed for one animal over a period of 4 months. The data from the other two animals were confirmatory. (PsycINFO Database Record (c) 2012 APA, all rights reserved)