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Hamann SB, Ely TD, Grafton ST, Kilts CD. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nat Neurosci 2: 289-293

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Pleasant or aversive events are better remembered than neutral events. Emotional enhancement of episodic memory has been linked to the amygdala in animal and neuropsychological studies. Using positron emission tomography, we show that bilateral amygdala activity during memory encoding is correlated with enhanced episodic recognition memory for both pleasant and aversive visual stimuli relative to neutral stimuli, and that this relationship is specific to emotional stimuli. Furthermore, data suggest that the amygdala enhances episodic memory in part through modulation of hippocampal activity. The human amygdala seems to modulate the strength of conscious memory for events according to emotional importance, regardless of whether the emotion is pleasant or aversive.
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nature neuroscience • volume 2 no 3 • march 1999 289
Studies with humans
1,2
and experimental animals
3,4
have demon-
strated that memory is better for emotionally arousing stimuli than
for emotionally neutral stimuli. From an evolutionary perspective,
it is clearly adaptive for memory for emotional stimuli to be
enhanced, because emotional stimuli, whether pleasant (for exam-
ple, sexual) or aversive (for example, frightening) are generally
more important than neutral stimuli for reproductive success. Con-
siderable evidence from animal studies indicates that the amyg-
dala has a crucial role in enhancing the strength of long-term
memory for emotional stimuli
3,5,6
through the interaction of
peripheral adrenergic systems with cholinergic, opioid-peptidergic
and GABAergic systems in the amygdala
3
. Two recent single-case
studies of amygdala-damaged human subjects
7,8
suggest that the
amygdala also enhances episodic memory (conscious memory for
events) for aversive stimuli. However, there are no conclusive neu-
roimaging data linking amygdala activity to enhanced episodic
memory for specifically emotional stimuli in humans
9
. The role
of the amygdala in memory for pleasant stimuli is of particular
interest, because there are to date no data linking the amygdala to
memory for pleasant, rewarding stimuli in humans. Here, using
positron emission tomography (PET), we examined the relation-
ship between amygdala activity during memory encoding of pleas-
ant and aversive stimuli and enhanced long-term episodic memory
(recall and recognition) for these stimuli. We tested the hypothesis
that amygdala activity is related to enhanced episodic memory for
pleasant and aversive emotionally arousing stimuli but not for non-
emotional stimuli. Our primary hypothesis is consistent with the
‘memory modulation’ theoretical framework of amygdala func-
tion
3,5,6
from experimental animal data, which predicts that the
amygdala should enhance long-term memory formation through
modulation of hippocampal activity for emotionally arousing stim-
uli but not for emotionally neutral stimuli.
We measured brain activity with PET H
2
15
O studies of region-
al cerebral blood flow (rCBF) while ten healthy male volunteers
Amygdala activity related to
enhanced memory for pleasant and
aversive stimuli
Stephan B. Hamann
1
, Timothy D. Ely
2
, Scott T. Grafton
3
and Clinton D. Kilts
2
1
Department of Psychology, Emory University, Atlanta, Georgia 30322, USA
2
Psychiatry and Behavioral Sciences, Emory University, Atlanta, Georgia 30322, USA
3
Neurology and Center for PET, Emory University, Atlanta, Georgia 30322, USA
Correspondence should be addressed to S. H. (shamann@emory.edu)
Pleasant or aversive events are better remembered than neutral events. Emotional enhancement of
episodic memory has been linked to the amygdala in animal and neuropsychological studies. Using
positron emission tomography, we show that bilateral amygdala activity during memory encoding is
correlated with enhanced episodic recognition memory for both pleasant and aversive visual stimuli
relative to neutral stimuli, and that this relationship is specific to emotional stimuli. Furthermore, data
suggest that the amygdala enhances episodic memory in part through modulation of hippocampal
activity. The human amygdala seems to modulate the strength of conscious memory for events
according to emotional importance, regardless of whether the emotion is pleasant or aversive.
viewed four types of pictures. Representative pleasant pictures
depicted sexually arousing scenes, appealing animals or appetiz-
ing food. Representative aversive pictures depicted mutilated and
diseased bodies, frightening animals or lethal violence. These
conditions were contrasted with two nonemotional control con-
ditions. Representative neutral pictures depicted chess players,
plants and animals or household scenes. Interesting pictures,
such as a chrome rhinoceros, a scene from a surrealistic film or an
exotic parade, were designed to attract interest and attention and
to be highly memorable as a control for these factors in the emo-
tional pictures, yet to be emotionally unarousing. Twelve scans
were done, three each for the four picture types. Skin-conduc-
tance and heart-rate data collected during scanning confirmed
substantial physiological arousal elicited by emotional pictures,
corroborating subjects’ emotion ratings taken after each scan
(Ta b le 1 ). PET data revealed an association of emotional-stim-
ulus pictures with significantly greater amygdala activation than
the neutral pictures, consistent with prior findings
10
(pairwise
comparisons with PET data will be reported separately; S.H, T.E.,
J.H. & C.K.). As expected, interesting pictures were rated as sim-
ilar in interest and attention to the emotional pictures but were
rated relatively unemotional (Ta b l e 1 ). After scanning had ended,
a surprise memory-recall test was given for the pictures. Four
weeks later, subjects were given another unannounced recall test
followed by a recognition-memory test, in which they were asked
to discriminate between pictures seen during the PET session
and similar but previously unseen pictures.
R
ESULTS
We examined correlations between rCBF in the amygdala dur-
ing encoding of pleasant, aversive or interesting pictures and the
corresponding memory enhancement for each picture type rel-
ative to performance in the neutral control condition. The result-
ing difference scores (for example, pleasant-picture recognition
articles
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290 nature neuroscience • volume 2 no 3 • march 1999
minus neutral-picture recognition) isolated
the memory-enhancement effect from indi-
vidual subject differences in general, non-
emotional (neutral) memory ability.
Isolation of the enhancement effect was cru-
cial, as a given subject might exhibit better
memory for pleasant or aversive pictures
than another subject because of superior
general memory ability unrelated to the
amygdala or to greater emotional-memory
enhancement. For each subject, the rCBF
and memory data were averaged across the
three scans for each picture type.
Correlational analyses were done for
recognition data and immediate- and
delayed-recall test data. Long-term episodic
recognition memory was substantially
enhanced for the pleasant, aversive and interesting pictures relative
to the neutral pictures (data for the three memory tests are pre-
sented in Tab le 1). Significant correlations with amygdala rCBF
were observed only for the recognition data; therefore only those
results are presented here. The absence of significant amygdala
correlations for the four-week-delayed-recall test data may have
resulted from a statistical artifact (restriction of range) associat-
ed with the low level of memory performance and consequently,
small variance for enhancement scores in this condition. In con-
trast to the four-week, delayed-recall data, there was substantial
individual subject variance in the four-week recognition and ten-
minute recall memory-enhancement scores. Absence of signifi-
cant amygdala correlations for the ten-minute recall data is
consistent with the memory-modulation theory, which postulates
that a major function of the amygdala is to modulate long-term
memory consolidation
3,5,6
. At short delays, the amygdalas role
may not be detectable because little consolidation has taken place.
Significant correlation was found between individual subjects’
recognition memory enhancement for pleasant pictures and bilat-
eral amygdala activity measured during the pleasant-picture scans
(Fig. 1a). For aversive pictures, recognition-memory enhance-
ment was also correlated with bilateral amygdala activity mea-
sured during the aversive picture scans, though at a slightly more
inferior level and more right-lateralized (Fig. 1b). Three-dimen-
sional coordinates
11
of representative maximally correlated pix-
els for these regions are presented in Table 2. In contrast,
recognition-memory enhancement for interesting pictures was
not correlated with activity in the amygdala or in the periamyg-
daloid cortex, even using liberal statistical thresholds, indicating
that the amygdalas relation to enhanced recognition memory
was specific to emotional stimuli.
This conclusion was corroborated by an analysis that com-
pared strength of correlations between amygdala rCBF at encod-
ing and memory enhancement for pleasant and aversive pictures
(Ta b l e 2 ) with corresponding correlations for interesting pictures
at the same loci. In each case, amygdala rCBF correlations were
significantly greater for the emotional pictures than for the inter-
esting, emotionally neutral pictures, all t (7) > 1.77, p < 0.05, for
the directional t-test of significant difference between two corre-
lations. Indeed, the correlations for interesting pictures at the left
and right amygdala correlation loci for pleasant pictures were neg-
ligible or negative (–0.19 and 0.01, respectively), as were the cor-
relations for the aversive picture loci (–0.21 and 0.11, respectively).
The outcome of the correlational analyses suggests a specific
relationship between enhancement of episodic memory for pleas-
ant and unpleasant emotional stimuli and activity in the amyg-
dala. Subjects who showed the greatest episodic-memory
enhancement associated with emotional stimuli also tended to
have higher levels of activity in the amygdala than subjects who
showed the least enhancement.
Because the amygdala has been hypothesized to influence
episodic memory indirectly, by modulating
3,5,6
the activity of a
hippocampal/medial–temporal lobe memory system
12,13
(accord-
ing to the memory-modulation theory), we did the same corre-
lational analysis for a second region of interest, the
hippocampal/parahippocampal region, which had been defined
a priori. Consistent with this hypothesis, recognition-memory
enhancement for both pleasant and aversive pictures was corre-
lated with bilateral activity in the hippocampal region (Ta b l e 2 ),
although a causal relationship between amygdala and hip-
pocampal activity cannot be inferred from these correlations.
Consistent with the hippocampus’s role in general episodic mem-
ory encoding for novel stimuli
14
, recognition-memory enhance-
ment for interesting pictures was also correlated with
hippocampal activity in the right hemisphere (Ta b le 2 ).
If the amygdala influences memory for emotional stimuli by
modulating activity in the hippocampal/parahippocampal region
as specified by the memory-modulation theory, then activity lev-
els in the amygdala and the hippocampal/parahippocampal
region should be highly correlated across individual subjects.
Conversely, uncorrelated activity in these two regions would sug-
gest that, although activity in each region is independently relat-
articles
Table 1. Behavioral data.
Stimulus type
Measure Pleasant Aversive Interesting Neutral
Emotional arousal 4.2 ± .5 4.9 ± .1 2.5 ± .2 1.3 ± .1
Emotional valence 4.3 ± .2 1.2 ± .1 3.2 ± .1 3.0 ± .1
Interest / attention 4.0 ± .2 4.4 ± .2 3.6 ± .1 1.7 ± .2
Skin-conductance response (µS) 0.65 ± .13 0.71 ± .13 0.59 ± .10 0.24 ± .04
Heart rate change ( bpm) –2.90 ± .34 –3.31 ± .37 –3.21 ± .33 –2.17 ± .20
10-min free recall 0.39 ± .04 0.47 ± .03 0.18 ± .02 0.19 ± .02
4-wk free recall 0.17 ± .03 0.21 ± .02 0.10 ± .02 0.06 ± .01
4-wk recognition (d) 2.06 ± .12 2.41 ± .12 2.39 ± .22 1.56 ± .13
Numbers following the ± sign indicate the standard error of the mean. Recall scores are expressed as
proportion correct recall.
Fig. 1. Brain activity correlated with memory enhancement. Maps of pixels
in which individual subject rCBF was significantly correlated (yellow, p <
0.05, two-tailed test for significant correlations) with individual-subject
episodic-memory enhancement superimposed on an axial magnetic-reso-
nance reference image averaged from a separate group of subjects.
(a) Correlation map for pleasant stimuli at z = –10.5. (b) Correlation map
for aversive stimuli at z = –16.5.
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nature neuroscience • volume 2 no 3 • march 1999 291
ed to enhanced memory, no modulatory relationship exists
between them. Importantly, the memory-modulation theory does
not predict that activity at all loci in the amygdala should be cor-
related with all loci in the hippocampal/parahippocampal region.
Instead, it makes the more specific prediction that particular loci
within these regions whose activation is significantly related to
memory performance should show correlated activity. There-
fore, the critical loci to test for intercorrelation are loci in the
amygdala and hippocampal/parahippocampal regions of inter-
est at which memory-correlated activity was maximal, specifi-
cally the loci listed in Table 2.
The results of this analysis were generally consistent with the
memory-modulation theory. For both pleasant and aversive pic-
ture conditions, activity (rCBF) at critical amygdala loci was sig-
nificantly correlated with activity at the corresponding
hippocampal or parahippocampal loci, both ipsilaterally and con-
tralaterally (r > 0.68, p < 0.05) with two exceptions: nonsignificant
positive correlations between the left amygdala and left hip-
pocampus for pleasant stimuli (r = 0.64), and between the right
amygdala and right hippocampus for aversive stimuli (r = 0.57).
The finding of significant contralateral correlations is important
because the close proximity of some of the amygdala and hip-
pocampal/parahippocampal loci within the same hemisphere rais-
es the possible concern of partial overlap of smoothed rCBF data
between loci, which would tend to inflate ipsilateral correlations;
the contralateral correlations are not subject to this concern.
It is probable that the amygdala is part of a larger network of
brain regions involved in encoding conscious memory for emo-
tional stimuli. For example, for pleasant stimuli, the regions of
correlated rCBF in the amygdala (Fig. 1a) were spatially con-
tiguous with a larger, superior region of correlated rCBF includ-
ing the right nucleus accumbens/subcallosal cortex (9, 9, –7
mm
11
, r = 0.93, p < 0.001) and right anterior cingulate cortex (7,
21, –7 mm
11
, r = 0.82, p < 0.01). The nucleus
accumbens has been linked to pleasure and
reward mechanisms
15,16
and receives prominent
input from the amygdala
17
. These interconnect-
ed regions may compose a functional network
preferentially involved in encoding pleasant
episodic memories. However, as these regions
were not included in the a-priori regions of inter-
est, their involvement and functional interpreta-
tion should be viewed as tentative, pending
replication.
The reliability of these correlational data is
supported by several lines of evidence. First, it is
unlikely that correlated activity in the regions of
a-priori interest is a chance artifact because activ-
ity correlated with memory enhancement for
pleasant and aversive pictures falls within discrete,
contiguous regions, and the memory-correlated
activity is largely confined to the a-priori regions
of interest (Fig. 1). For example, within a large
region of the brain extending from the horizontal
level corresponding to the inferior limit of the
most inferior region of correlated activity in an
a-priori region of interest (z = –22, Ta b l e 2 ) up to
and including the horizontal slice at z = 0, mem-
ory-correlated brain activity was largely confined
to the a-priori regions of interest. Exceptions
included the putative network for encoding pleas-
ant episodic memories noted above, two small
regions in visual cortex and one in right frontal
lobe showing correlated activity for pleasant pic-
tures, and one small region of visual cortex and
a small right medial-temporal-lobe region show-
ing correlated activity for aversive pictures.
articles
Table 2. Loci of maximal correlation.
Talairach coordinates Structure rp-value
xyz
Pleasant pictures
–21 –4 –10 L. amygdala 0.83 0.01
19 –9 –10 R. amygdala 0.80 0.01
–33 –22 –13 L. hippocampus 0.67 0.05
21 –19 –7 R. hippocampus 0.70 0.05
Aversive pictures
–13 –7 –18 L. amygdala/ periamyg. cortex 0.71 0.05
17 –7 –18 R. amygdala 0.81 0.01
–33 –27 –9 L. hippocampus 0.87 0.01
24 –22 –6 R. hippocampus 0.69 0.05
–15 –9 –22 L. parahippocampal gyrus 0.81 0.01
16 –7 –22 R. parahippocampal gyrus 0.89 0.01
Interesting pictures
34 –30 –3 R. hippocampus 0.84 0.01
These are representative loci within the two a priori regions of interest
(amygdala and hippocampus/parahippocampal gyrus) in which rCBF was cor-
related with long-term enhanced episodic memory.
Fig. 2. Relationship between pleasant-picture memory and brain activity for individual
subjects. Correlation scatterplots for the pleasant-picture memory correlations with
rCBF, n = 10. Memory enhancement is defined as recognition for pleasant pictures minus
recognition for neutral pictures, in d accuracy units
24
. rCBF is in units of ml per min per
100 g of brain tissue, normalized across subjects and scans by proportionate scaling of
global cerebral blood flow. (a) Correlation plot for left amygdala. (b) Correlation plot
for right amygdala. (c) Correlation plot for left hippocampal region. (d) Correlation plot
for right hippocampal region.
c
d
Recognition enhancement
Recognition enhancement
Recognition enhancement
Recognition enhancement
Left amygdala rCBF
Right amygdala rCBF
Left hippocampal rCBF Right hippocampal rCBF
a
b
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292 nature neuroscience • volume 2 no 3 • march 1999
Inspection of correlation plots relating rCBF to memory enhance-
ment also suggests that the observed correlations are not due to
extreme scores skewing the observed correlations (see Fig. 2 for
correlation plots for the pleasant-picture correlation data; removal
from the correlational analysis of the apparent outlying score on
the far right in scatterplots a, b and c reduced the observed cor-
relations slightly but not significantly).
D
ISCUSSION
Only one previous neuroimaging study has examined the rela-
tionship between amygdala activity at encoding and episodic
memory for emotional stimuli
9
. Using a different PET method-
ology with [
18
F]fluoro-2-deoxyglucose (FDG-PET), that study
examined recall for aversive and neutral films. It found a signif-
icant positive correlation between brain glucose metabolic rate
in the right amygdala during encoding and the number of emo-
tional but not neutral films recalled three weeks later, demon-
strating a relation between amygdala activity and episodic
memory for aversive stimuli. Although significant correlations
with neutral-film recall were observed in other brain regions out-
side the amygdala, the specificity of the relation of amygdala activ-
ity to aversive emotional memory could not be established as
conclusively as in the current study, because memory of neutral
films was poor, reducing likelihood of significant correlation. To
establish that amygdala activity is not related to memory for non-
emotional stimuli, it is necessary to rule out the possibility that
the amygdala has a nonspecific memory-enhancing role for all
stimuli. The use of interesting and memorable yet nonemotion-
al pictures as control stimuli in the current study allowed the
selectivity of the amygdalas memory enhancement for emotional
stimuli to be established more conclusively. The specificity of the
amygdalas mnemonic role for emotional stimuli is also supported
by a recent neuroimaging study that reported inactivity of the
amygdala during formation of nonemotional declarative memory
for verbal stimuli
18
. Although the FDG-PET study
9
used total
recall rather than an enhancement measure as the behavioral cor-
relate of amygdala activity, reanalysis of the FDG-PET study data
using enhancement scores (number of emotional films recalled –
number of neutral films recalled) does not significantly change
the conclusions of that correlational analysis (L. Cahill, person-
al communication, 1998).
Our results confirm and extend these previous FDG-PET
findings
9
by demonstrating that activity in the left as well as right
amygdala is related to enhanced episodic memory for aversive
stimuli, and that this relationship is specific to emotional stimuli.
In addition, the current study is the first demonstration that the
amygdala is involved in encoding memory for emotionally arous-
ing, pleasant stimuli in humans. The role of the amygdala in
memory for pleasant, rewarding stimuli in nonhuman animals
has received some attention
5,15,16,19
, but relatively little in com-
parison to the intense scrutiny afforded the amygdalas role in
aversive memory phenomena such as fear conditioning
20,21,22
and fear-potentiated startle
23
. The current findings suggest that
the amygdalas role in encoding memory for emotionally arous-
ing, pleasant stimuli in humans is significantly greater than has
been appreciated previously. In summary, the present findings
suggest that the amygdala in humans is important in modulat-
ing memory for events according to their emotional importance,
regardless of whether the nature of the emotion is pleasant or
aversive. The hippocampal data are consistent with the notion
that the amygdala may exert its influence on episodic memory
for emotionally arousing stimuli in part through modulation of
the hippocampal/medial-temporal-lobe memory system
3,5,6
.
M
ETHODS
Subjects.The ten subjects were right-handed male university students
with a mean age of 22.8 years (range 20–32) who had been screened for
neurological and psychiatric conditions. To ensure effectiveness of the
sexually arousing, pleasant pictures, only self-identified heterosexual sub-
jects were included in the study. The study was approved by the Emory
University School of Medicine Human Investigations Committee; writ-
ten informed consent was obtained from the subjects.
Behavioral tasks. During each PET scan, subjects viewed pictures on a
computer monitor that spanned their field of view, and were instructed,
“pay attention and experience whatever thoughts or feelings the pictures
may elicit in you.” No mention of the later memory tests was made. Fol-
lowing each scan, subjects rated the set of pictures they had just viewed
(13 pictures) on 3 dimensions using scales of 1–5: emotional arousal (1,
lowest arousal; 5, highest), emotional valence (1, most unpleasant; 3,
neutral; 5, most pleasant) and degree of interest (1, lowest interest; 5,
highest interest). Mean ratings for the pleasant, aversive, interesting and
neutral stimuli are shown in Table 1. Each picture was presented for 7.5
s, beginning 10 s before and during each scan. Different sets of stimuli
were used for each picture-presentation condition, and the order of con-
ditions was counterbalanced across subjects.
Skin conductance and heart rate were measured at 100 Hz beginning
1 min before each scan. Table 1 shows the mean skin-conductance
response to each stimulus type averaged across the 10 subjects, in
microsiemens (µS, units of electrical conductance). The mean skin-con-
ductance response (SCR) for each subject was calculated by first deter-
mining the SCR to each picture stimulus, defined as the maximal positive
deflection in skin-conductance level with onset occuring 0.5–4.0 s after
stimulus presentation, and then averaging the four largest SCRs for each
scan. (The SCRs corresponding to the first three stimuli of each scan
were excluded from this analysis because their SCR values were affected
by the SCR generated by the injection of the radioactive tracer.) Mean
SCRs for pleasant, aversive or interesting conditions differed significantly
from the mean SCRs in the neutral condition (all t (8) > 3.65, p < 0.01,
paired t-test), but did not differ significantly from each other (p > 0.10).
(SCRs were elevated in the interesting condition because skinconduc-
tance was affected by the orienting response to interesting stimuli as well
as by emotional arousal.) Heart-rate change was assessed by subtracting
the lowest heart rate observed during stimulus presentation (in beats per
minute; bpm) from the baseline heart rate measured 20 s before the injec-
tion of the radioactive tracer. Heart-rate deceleration to emotional and
attention-provoking stimuli is typically observed in situations where such
stimuli are presented for passive viewing. Heart rate decelerated signifi-
cantly more during viewing of the pleasant, aversive, or interesting pic-
tures than for the neutral pictures (all t (8) > 2.37, p < 0.05, paired t-test).
Memory measures. The immediate-recall test was given 10 min after the
end of the final scan. Subjects were instructed to try to recollect the pic-
tures they had seen during the scans in any order they chose and to write
down words or phrases that would describe the pictures so that they
could be identified from the set they had seen. Two independent judges
determined which picture (if any) each verbal response described. Four
weeks later, subjects were given another unannounced recall test using
the same procedure as the 10-min recall test, followed by a recognition
test in which all of the pictures that had been viewed during the PET ses-
sion (except for the first picture of each set, which was a buffer item not
included in the analysis) were presented in a pseudo-random order
together with an equal number of similar but previously unseen pictures.
Subjects were asked to indicate which pictures they had seen before and
which were new. Memory-enhancement scores for each subject were cal-
culated by converting individual-subject recognition scores from each
picture condition to d
recognition-accuracy statistics
24
(to control for
the effects of differing response criteria across subjects) and then sub-
tracting the d
scores for the neutral condition from each of the corre-
sponding d
scores from the other conditions. All pictures are from a
standard set of affective pictures
25
except for the interesting pictures,
which were collected from commercial sources and standardized on a
separate group of subjects.
articles
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© 1999 Nature America Inc. • http://neurosci.nature.com
nature neuroscience • volume 2 no 3 • march 1999 293
PET image acquisition. PET images of task-related rCBF were acquired
in two-dimensional mode with an ECAT 951 or 921 scanner (Siemens,
Knoxville, Tennessee) following the intravenous administration of the
blood-flow tracer
26
H
2
15
O. Acquisition of emission data was initiated 10
seconds after tracer injection and continued for 90 s, with 10 min between
each tracer injection. Head movement was minimized by use of the
TruScan restraint system. Images were reconstructed using a calculated
attenuation correction. PET images for each subject were aligned and
resliced
27
. The PET scans were coregistered to a population-average PET
target
28
centered in Talairach coordinates
11
, derived from 20 subjects who
also had structural MRI. The average MRI from this population was used
as the anatomical reference. PET images were smoothed to a final isotrop-
ic resolution of 9 mm and normalized to each other by proportionate scal-
ing of global activity. The PET data for one subject was not available for
part of the right amygdala and right anterior regions corresponding to
inferior horizontal slices at z = – 18 and below
11
. Therefore, all correla-
tional analyses in this study were done with the other nine subjects with
complete PET data. The correlational analyses did not change significantly
when recalculated with all 10 subjects for loci at which PET data was avail-
able for all subjects. For reliability checks on the correlations and the cor-
relation scattergrams shown in Fig. 2 that assessed the effects of extreme
scores, all available data from all 10 subjects were used because the 10th
subject had the potential to reveal instability in the correlations if his data
were highly discrepant from those of the other subjects.
Region of interest selection. We defined a priori our two regions of inter-
est, the amygdala and the hippocampal/parahippocampal region, by trac-
ing the neuroanatomical boundaries of these brain regions on 1.5
mm-thick axial slices of the averaged-subject magnetic-resonance refer-
ence image that was used for PET coregistration. We also traced the
boundaries of these brain regions onto a second reference, the horizon-
tal slices from the standard atlas of Talairach and Tournoux
11
. The cor-
relational analysis examined rCBF, estimated from radioactivity relative
to the global mean, computed for every 1.5 mm ×1.5 mm × 1.5 mm pixel
in the entire brain that fell within the field of view of the PET scanner.
For the region-of-interest analysis, a strict criterion was used for neu-
roanatomical localization. Specifically, a correlated pixel was accepted as
being localized within the amygdala or hippocampal/parahippocampal
region only if it fell both within the traced ROI on the averaged subject
structural magnetic resonance image and within the Talairach-based ROI
as determined by the plotted Talairach coordinates of the correlated pixel.
This same procedure was also used to determine the neuroanatomical
localization of correlated regions that were not defined a priori (for
instance, nucleus accumbens).
A
CKNOWLEDGEMENTS
We thank E. Tulving for comments on the manuscript, L. Stefanacci for
neuroanatomical localization advice and J. Hoffman for advice and assistance
with PET image acquisition. The research was funded by a grant (#97–24) from
the James S. McDonnell Foundation to S. H., by the Emory Center for PET and
by the Emory University Research Committee.
RECEIVED 23 OCTOBER 1998; ACCEPTED 26 JANUARY 1999
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articles
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294 nature neuroscience • volume 2 no 3 • march 1999
articles
© 1999 Nature America Inc. • http://neurosci.nature.com
© 1999 Nature America Inc. • http://neurosci.nature.com
... As frequently noted, memory performance is generally enhanced for emotional, compared to neutral, information (Bradley et al., 1992;Hamann et al., 1999;Dolcos et al., 2005Dolcos et al., , 2017Kensinger and Schacter, 2008), and amygdala activation at encoding and/or retrieval is often proposed as a critical mechanism. Much of the supporting data, however, arise from studies assessing memory for visual scenes or faces, whereas amygdala activation is not a general finding across emotional challenges. ...
... Given that the amygdala has been strongly implicated in long-term (i.e., ranging from 1 to 4 weeks) emotional memory in previous individual differences studies using scene pictures as visual stimuli (Hamann et al. 1999;Mackiewicz et al. 2006;Ritchey et al. 2008), as well as that the fusiform gyrus plays a pivotal role in face recognition (Kanwisher et al. 1997;McCarthy et al. 1997), we examined effects in the amygdala and fusiform gyrus with increased sensitivity using a priori region-of-interest (ROI) analysis. Bilateral amygdala masks were created from the Brainnetome atlas (http:// atlas. ...
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Studies demonstrated that faces with threatening emotional expressions are better remembered than non-threatening faces. However, whether this memory advantage persists over years and which neural systems underlie such an effect remains unknown. Here, we employed an individual difference approach to examine whether the neural activity during incidental encoding was associated with differential recognition of faces with emotional expressions (angry, fearful, happy, sad and neutral) after a retention interval of > 1.5 years (N = 89). Behaviorally, we found a better recognition for threatening (angry, fearful) versus non-threatening (happy and neutral) faces after a delay of > 1.5 years, which was driven by forgetting of non-threatening faces compared with immediate recognition after encoding. Multivariate principal component analysis (PCA) on the behavioral responses further confirmed the discriminative recognition performance between threatening and non-threatening faces. A voxel-wise whole-brain analysis on the concomitantly acquired functional magnetic resonance imaging (fMRI) data during incidental encoding revealed that neural activity in bilateral inferior occipital gyrus (IOG) and ventromedial prefrontal/orbitofrontal cortex (vmPFC/OFC) was associated with the individual differences in the discriminative emotional face recognition performance measured by an innovative behavioral pattern similarity analysis (BPSA). The left fusiform face area (FFA) was additionally determined using a regionally focused analysis. Overall, the present study provides evidence that threatening facial expressions lead to persistent face recognition over periods of > 1.5 years, and that differential encoding-related activity in the medial prefrontal cortex and occipito-temporal cortex may underlie this effect.
... Likewise, functional MR studies in normal human subjects show amygdala activation during valence judgments (Canli et al., 2000;Garavan et al., 2001;Hariri et al., 2002;Phelps and LeDoux, 2005;Sergerie et al., 2008;Ball et al., 2009;Salzman and Fusi, 2010;Murray et al., 2014). Lastly, studies describing human subjects with acquired destructive amygdala lesions demonstrate deficits in perception of negatively valenced images-such as faces-with subjects reporting them as less fearful or less threatening (Adolphs et al., 1994;Hamann et al., 1999;Canli et al., 2000;Anderson and Phelps, 2001;Kilpatrick and Cahill, 2003;Kensinger and Corkin, 2004;Phelps, 2004;Richardson et al., 2004;LaBar and Cabeza, 2006;Sergerie et al., 2006). ...
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Background Multiple lines of evidence show that the human amygdala is part of a neural network important for perception of emotion from environmental stimuli, including for processing of intrinsic attractiveness/“goodness” or averseness/“badness,” i.e., affective valence. Objective/Hypothesis With this in mind, we investigated the effect of electrical brain stimulation of the human amygdala on perception of affective valence of images taken from the International Affective Picture Set (IAPS). Methods Using intracranial electrodes in patients with epilepsy, we first obtained event-related potentials (ERPs) in eight patients as they viewed IAPS images of varying affective valence. Next, in a further cohort of 10 patients (five female and five male), we measured the effect of 50 Hz electrical stimulation of the left amygdala on perception of affective valence from IAPS images. Results We recorded distinct ERPs from the left amygdala and found significant differences in the responses between positively and negatively valenced stimuli ( p = 0.002), and between neutral and negatively valenced stimuli ( p = 0.017) 300–500 ms after stimulus onset. Next, we found that amygdala stimulation did not significantly affect how patients perceived valence for neutral images ( p = 0.58), whereas stimulation induced patients to report both positively ( p = 0.05) and negatively (< 0.01) valenced images as more neutral. Conclusion These results render further evidence that the left amygdala participates in a neural network for perception of emotion from environmental stimuli. These findings support the idea that electrical stimulation disrupts this network and leads to partial disruption of perception of emotion. Harnessing this effect may have clinical implications in treatment of certain neuropsychiatric disorders using deep brain stimulation (DBS) and neuromodulation.
... Episodic memory is a subtype of declarative memory, defined as the ability to remember where and when past events occurred (Tulving, 1972) and involves subjective consciousness (Wheeler et al., 1997). Furthermore, there is consensus that emotional episodic memories, whether they are pleasant or aversive events, are better remembered than neutral events (Hamann et al., 1999;Payne et al., 2006;Cahill & McGaugh, 1998;Reisberg & Heuer, 2004) proposing that emotional activation mediates episodic memory processes, and it serves as contextual cues for these memories (Damasio & Damasio, 1994;Damasio, 1999;Bechara et al., 2003;Allen et al., 2008). Moreover, emotion improves encoding as well as consolidation processes (LaBar & Cabeza, 2006;Dolcos et al., 2012). ...
Article
The threatening context of the COVID-19 pandemic provided a unique setting to study the effects of negative psychological symptoms on memory processes. Episodic memory is an essential function of the human being related to the ability to store and remember experiences and anticipate possible events in the future. Studying this function in this context is crucial to understand what effects the pandemic will have on the formation of episodic memories. To study this, the formation of episodic memories was evaluated by free recall, recognition, and episode order tasks for an aversive and neutral content. The results indicated that aversive episodic memory is impaired both in the free recall task and in the recognition task. Even the beneficial effect that emotional memory usually has for the episodic order was undermined as there were no differences between the neutral and aversive condition. The present work adds to the evidence that indicates that the level of activation does not modify memory processes in a linear way, which also depends on the type of recall and the characteristics of the content to be encoded.
... Norepinephrine fosters sustained representation of an experience in working memory (Arnsten & Li, 2005) while also promoting synaptic plasticity in general (Harley, 2007). The amygdala and hippocampus play a major role in learning (Hamann et al., 1999;Murty et al., 2010), and both of them have receptors for norepinephrine and cortisol. Increased activity at these receptor sites related to physically-or emotionally-based arousal heightens the formation of explicit and implicit memory (Cahill & McGaugh, 1996). ...
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People draw on psychological resources such as gratitude to cope with adversity and maintain well-being. These resources must largely be acquired, and studies have identified environmental and behavioral factors of this learning. Yet little research has investigated how people can be active agents in this process by how they engage their experiences of psychological resources. Consequently, the HEAL framework was developed to organize numerous ‘mental engagement factors,’ and the Taking in the Good Course (TGC) was created to explore their use. In a multiple arm, pre-post intervention study, TGC participants reported significant increases in composite measures of Cognitive Resources, Positive Emotions, and Total Happiness, and decreases in a composite measure of Negative Emotions; these results persisted two months after the course ended. These findings suggest that people can learn how to heighten the internalization of beneficial experiences, with implications for improving responses to treatment and the development of psychological resources.
... Moreover, compared with men, women show enhanced memory for emotional stimuli 9 . Emotional hypermnesia is partially mediated through activation of the amygdala 10,11 and imaging studies revealed a sex-related hemispheric lateralization of the amygdala in response to emotional stimuli: right amygdala activation while viewing emotional stimuli is more significantly related to subsequent memory for the images in men than women, whereas the reverse sex difference is evident for the left amygdala 9,12-14 . ...
Preprint
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Few studies have examined how multisensory emotional experiences are processed and encoded into memory. Here, we aimed to determine whether, at encoding, activity within functionally-defined visual- and auditory-processing brain regions discriminated the emotional category (i.e., positive, negative, or neutral) of the multisensory (audio-visual) events. Participants incidentally encoded positive, negative, and neutral multisensory stimuli during event-related functional magnetic resonance imaging (fMRI). Following a 3-hour post-encoding delay, their memory for studied stimuli was tested, allowing us to identify emotion-category-specific subsequent-memory effects focusing on medial temporal lobe regions (i.e., amygdala, hippocampus) and visual- and auditory-processing regions. We used a combination of univariate and multivoxel pattern fMRI analyses (MVPA) to examine emotion-category-specificity in mean activity levels and neural patterning, respectively. Univariate analyses revealed many more visual regions that showed negative-category-specificity relative to positive-category-specificity, and auditory regions only showed negative-category-specificity. These results suggest that negative emotion is more closely tied to information contained within sensory regions, a conclusion that was supported by the MVPA analyses. Functional connectivity analyses further revealed that the visual amplification of category-selective processing is driven, in part, by mean signal from the amygdala. Interestingly, while stronger representations in visuo-auditory regions were related to subsequent-memory for neutral multisensory stimuli, they were related to subsequent-forgetting of positive and negative stimuli. Neural patterning in the hippocampus and amygdala were related to memory for negative multisensory stimuli. These results provide new evidence that negative emotional stimuli are processed with increased engagement of visuosensory regions, but that this sensory engagement—that generalizes across the entire emotion category—is not the type of sensory encoding that is most beneficial for later retrieval.
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Preprint
Full-text available
Studies demonstrated that faces with threatening emotional expressions are better remembered than non-threatening faces. However, whether this memory advantage persists over years and which neural systems underlie such an effect remains unknown. Here, we employed an individual difference approach to examine whether the neural activity during incidental encoding was associated with differential recognition of faces with emotional expressions (angry, fearful, happy, sad and neutral) after a retention interval of > 1.5 years ( N = 89). Behaviorally, we found a better recognition for threatening (angry, fearful) versus non-threatening (happy and neutral) faces after a > 1.5 years delay, which was driven by forgetting of non-threatening faces compared with immediate recognition after encoding. Multivariate principal component analysis (PCA) on the behavioral responses further confirmed the discriminative recognition performance between threatening and non-threatening faces. A voxel-wise whole-brain analysis on the concomitantly acquired functional magnetic imaging (fMRI) data during incidental encoding revealed that neural activity in bilateral inferior occipital gyrus (IOG) and ventromedial prefrontal/orbitofrontal cortex (vmPFC/OFC) was associated with the individual differences in the discriminative emotional face recognition performance measured by an innovative behavioral pattern similarity analysis (BPSA) based on inter-subject correlation (ISC). The left fusiform face area (FFA) was additionally determined using a regionally focused analysis. Overall, the present study provides evidence that threatening facial expressions lead to persistent face recognition over periods of > 1.5 years and differential encoding-related activity in the medial prefrontal cortex and occipito-temporal cortex may underlie this effect.
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Both pictures and words are frequently employed as experimental stimuli to investigate the neurocognitive mechanisms of emotional processing. However, it remains unclear whether emotional picture processing and emotional word processing share neural underpinnings. To address this issue, we focus on neuroimaging studies examining the implicit processing of affective words and pictures, which require participants to meet cognitive task demands under the implicit influence of emotional pictorial or verbal stimuli. A coordinate-based activation likelihood estimation meta-analysis was conducted on these studies, which revealed no common activation maximum between the picture and word conditions. Specifically, implicit negative picture processing (35 experiments, 393 foci, and 932 subjects) engages the bilateral amygdala, left hippocampus, fusiform gyri, and right insula, which are mainly located in the subcortical network and visual network associated with bottom-up emotional responses. In contrast, implicit negative word processing (34 experiments, 316 foci, and 799 subjects) engages the default mode network and fronto-parietal network including the ventrolateral prefrontal cortex, dorsolateral prefrontal cortex, and dorsomedial prefrontal cortex, indicating the involvement of top-down semantic processing and emotion regulation. Our findings indicate that affective pictures (that intrinsically have an affective valence) and affective words (that inherit the affective valence from their object) modulate implicit emotional processing in different ways, and therefore recruit distinct brain systems.
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Modern neurosurgical concepts call for not only "seeing" but also for "localizing" structures in three-dimensional space in relationship to each other. Hence there is a need for a reference system. This book aims to put this notion into practice by means of anatomical and MRI sections with the same stereotaxic orientation. The purpose is to display the fundamental distribution of structures in three-dimensional space and their spatial evolution within the brain as a whole, while facilitating their identification; to make comparative studies of cortico-subcortical lesions possible on a basis of an equivalent reference system; to exploit the anatomo-functional data such as those furnished by SEEG in epilepsy and to enable the localization of special regions such as the SMA in three-dimensional space; and to apply the anatomical correlations of this reference system to neurophysiological investigations lacking sufficient anatomical back-up (including PET scan).
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Abstract Theoretical arguments and empirical data are presented in favor of the hypothesis that the hippocampal system supports a declarative memory capacity in animals as well as humans. This view is advanced by identifying two prominent characteristics of human declarative memory and by operationalizing and evaluating them using both experimental lesion and single unit recording studies on animals. First, hippocampal processing is not selective to any particular category of learning materials; instead, it supports comparisons among all kinds of information in memory, resulting in a representation of critical relations between items. Conversely, individual representations are supported outside the hippocampal system. Second, hippocampal-dependent, relational memory representations involve a flexible organization that permits inferences from memory in novel situations. Conversely, hippocampal-independent individual representations can support only repetition of procedures acquired during original learning. Correspondences between the neuropsychological and neurophysiological findings presented serve to indicate how these properties of hippocampal representation support declarative memory across behavioral paradigms and across species.
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Discusses the role of the amygdaloid complex in conditioning of autonomic processes during emotional learning situations. Results from studies on animals and normal humans have implicated at the simplest, the activation of β-adrenergic receptors, and the amygdaloid complex in such learning. Recent experimental results with patients with brain-damage and Urbach-Weithe disease show selective impairment of memory for emotional material (e.g., L. Cahil, et al, 1995), have confirmed this hypothesis for conscious, long-term memory. However, these autonomic processes are not required for normal retention in non-emotionally arousing situations. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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The analysis of the behavioural and neural mechanisms of reinforcement and motivation has benefited from the recent application of learning theory and better anatomical knowledge of the connectivity of certain key neural structures, such as the nucleus accumbens. This progress has enabled the dissection of motivational processes into components that can begin to be related to the functioning of specific limbic cortical structures that project to different compartments of the ventral striatum.
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Incidental memory performance for pictures that varied along the affective dimensions of pleasantness and arousal was assessed. For both an immediate and delayed (1 year later) free-recall task, only the arousal dimension had a stable effect on memory performance: Pictures rated as highly arousing were remembered better than low-arousal stimuli. This effect was corroborated in a speeded recognition test, in which high-arousal materials encoded earlier in the experiment produced faster reaction times than their low-arousal counterparts. Pleasantness affected reaction time decisions only for pictures not encoded earlier. These results suggest that whereas both the dimensions of pleasantness and arousal are processed at initial encoding, long-term memory performance is mainly affected by arousal.