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The Journal of Neuroscience, 2000, 20:RC99:1-5
RAPID COMMUNICATION
Event-Related Activation in the Human Amygdala Associates with
Later Memory for Individual Emotional Experience
Turhan
Canli1,
Zuo
Zhao1,
James
Brewer1,
John D. E.
Gabrieli1, 2, and
Larry
Cahill3, 4
Departments of 1 Psychology and
2 Radiology, Stanford University, Stanford, California
94305, and 3 Center for the Neurobiology of Learning and
Memory and 4 Department of Neurobiology and Behavior,
University of California, Irvine, California 92697
 |
ABSTRACT |
The role of the amygdala in enhancing declarative memory for
emotional experiences has been investigated in a number of animal, patient, and brain imaging studies. Brain imaging studies, in particular, have found a correlation between amygdala activation during
encoding and subsequent memory. Because of the design of these studies,
it is unknown whether this correlation is based on individual
differences between participants or within-subject variations in
moment-to-moment amygdala activation related to individual
stimuli. In this study, participants saw neutral and negative scenes
and indicated how emotionally intense they found each scene. Separate
functional magnetic resonance imaging responses in the amygdala
for each scene were related to the participants' report of their
experience at study and to performance in an unexpected memory
test 3 weeks after scanning. The amygdala had the greatest response to
scenes rated as most emotionally intense. The degree of activity in the
left amygdala during encoding was predictive of subsequent memory only
for scenes rated as most emotionally intense. These findings support
the view that amygdala activation reflects moment-to-moment subjective
emotional experience and that this activation enhances memory in
relation to the emotional intensity of an experience.
Key words:
amygdala; affect; emotion; arousal; individual
experience; memory
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INTRODUCTION |
Emotional
experiences are often better recalled than nonemotional ones
(Christianson, 1992 ). For example, people show superior declarative
memory for emotionally vivid segments of a story, relative to
emotionally neutral segments (Cahill et al., 1995; Adolphs et al.,
1997). The amygdala appears to play a critical role in such an
enhancement of emotional memory, because patients with bilateral
amygdala damage do not remember emotional better than neutral story
segments (Cahill et al., 1995; Adolphs et al., 1997).
Imaging studies have shown that amygdala activation correlates with
emotional memory in the intact brain. Two positron emission tomography
(PET) studies (Cahill et al., 1996; Hamann et al., 1999) and one
functional magnetic resonance imaging (fMRI) study (Canli et
al., 1999) reported significant correlations between amygdala
activation related to emotional stimuli and subsequent memory.
In all three studies, individuals who showed strong amygdala activation
in response to a set of emotional stimuli (relative to other study
participants) also showed superior memory for those stimuli (relative
to other study participants). Importantly, such correlations between
amygdala activation and subsequent memory were not observed for
emotionally neutral stimuli.
These first imaging studies have identified a correlation between
amygdala activation and declarative memory for emotional stimuli across
different individuals. This between-subjects study design allows for at
least three alternative interpretations of the data. The first is that
some individuals are more responsive to emotional experiences than
others. The observed amygdala activation therefore would reflect a
tonic personality characteristic. The second is that some individuals,
during a particular scanning session, may have been in some sort of
state that enhanced responsiveness to emotional experience. The third
interpretation is that the amygdala is responsive in a dynamic or
phasic way to moment-to-moment individual emotional experience, so that
amygdala activation would reflect a flexible, rapidly changing
emotional response that ought to be observable within an individual.
This explanation is consistent with animal studies (Cahill and McGaugh,
1990; McGaugh et al., 1996).
The phasic interpretation makes the specific prediction that the
amygdala is sensitive to the emotional intensity of a stimulus, where
intensity may refer to the valence or arousal characteristics of that
stimulus, or a combination of both. The phasic interpretation makes the
additional prediction that those emotionally intense stimuli that
produce greater amygdala activation should be better remembered than
stimuli that produce less amygdala activation.
The present study used event-related fMRI in a within-subject,
subsequent-memory design (Brewer et al., 1998) to test the predictions
made by the phasic interpretation. Participants saw neutral and
negative scenes and indicated how they experienced the emotional
intensity of each scene. A separate fMRI response was recorded in the
amygdala for each such emotional experience. Three weeks later,
participants' memories for the scenes were assessed. Thus, each
amygdala response could be related to the participants' report of
their experience of emotional intensity at study, and to
long-term memory for that experience. The central questions addressed
by this study were (1) whether the amygdala is sensitive to varying
degrees of individually experienced emotional intensity and (2) whether
the degree of emotional intensity affects the role of the amygdala in
enhancing memory for emotional stimuli.
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MATERIALS AND METHODS |
Subjects. Ten right-handed healthy female volunteers
were scanned in a 1.5T magnet. Women were chosen in this study
because they are more likely to report intense emotional experiences
(Shields, 1991) and show more physiological reactivity in concordance
with valence judgments than men (Lang et al., 1993).
Behavioral procedures. During scanning, subjects viewed 96 scenes through a mirror directed at a back-projection screen, each with
a normative rating for valence and arousal, from the International Affective Picture System stimuli set (Lang and Greenwald, 1993). For the scenes used in this study, normative ratings for valence ranged
from 1.17 (highly negative) to 5.44 (neutral). Normative ratings for
arousal ranged from 1.97 (tranquil) to 7.63 (highly arousing). Arousal
and valence (degree of negativity) were highly correlated
(r = 0.89). The order of scenes was randomized across subjects, with each picture presented for a period of 2.88 sec. During
the interstimulus interval of 12.96 sec, subjects viewed a fixation
cross. Subjects were instructed to view each picture for the entire
time that it was displayed, and after its replacement with a fixation
cross they were to indicate their emotional arousal by pressing a
button with their right hand. Subjects chose from four buttons to
indicate emotional arousal on a scale from 0 ("not emotionally
intense at all") to 3 ("extremely emotionally intense"). Three
weeks after the scan, subjects were tested in an unexpected recognition
test in the laboratory, during which they viewed all of the previously
seen and 48 new scenes (foils). The foils were selected to match the
previously presented scenes in their valence and arousal
characteristics: foils had normative valence ratings that ranged from
1.31 (highly negative) to 5.78 (neutral) and normative arousal ratings
that ranged from 2.74 (tranquil) to 7.22 (highly arousing); there was
no significant difference between foils and previously presented scenes
with respect to their normative valence
(t(142) = 0.16, p = 0.88) and arousal (t(142) = 0.98, p = 0.33) ratings. During the recognition test,
subjects were asked whether they had seen each picture before. For
scenes judged as previously seen, subjects reported whether they
remembered with certainty ("remember") or had a less certain
feeling of familiarity ("know"). Forgotten, familiar, and
remembered trials were encoded in a numerical format (as 1, 2, and 3, respectively) to construct correlation maps.
MRI. Data were acquired in a 1.5 T General
Electric Signa MR imager, which was used to measure
blood-oxygen level-dependent (BOLD) contrast (Ogawa et al., 1990). For
structural images, eight slices perpendicular to the axial plane of the
hippocampus were obtained with a 2.4 mm2
in-plane and 7.0 mm through-plane resolution. The anterior slice was
positioned 7 mm anterior to the amygdala. Functional images were
obtained using a two-dimensional spin echo sequence with two
interleaves [repetition time (TR)/slice = 90 msec, echo time (TE) = 40 msec, flip angle = 80°, field of view (FOV) = 20 cm, acquisition time = 1.44 sec per frame, number of
frames = 264]. A whole-head coil was used for all subjects. Head
movement was minimized by using a bite-bar formed with each subject's
dental impression, and motion artifact was examined and corrected
automatically for all scans using Air 3.0 (Woods et al., 1992). During
functional scanning, 11 frames were captured per trial. Individual
frames in each trial were assigned to the baseline fixation period
(frames 1, 2, 10, 11) or to the activation period (frames 5-8) based
on a lag in peak hemodynamic response of ~4 sec after the
presentation of the stimulus (Malonek and Grinwald, 1996).
A correlation map was created to correlate brain activation with
subjects' arousal ratings and memory scores as follows: for each
trial, the average area under the curve was integrated to measure each
voxel's event-related response during both baseline scans and
activation scans. Integrated values from baseline scans were then
subtracted from activation scans. A Kendal rank-order correlation was
calculated for each voxel between event-related responses and reported
experienced emotional intensity on a scale from 0 to 3. Correlation
coefficients were transformed into z scores.
For the composite map shown here, the structural MRI scans were
normalized into the same space to allow for the superimposition of
statistical maps averaged across subjects onto an averaged structural
image. The averaged correlation maps were intensity-thresholded at
p < 0.025, one-tailed, and each slice was subjected to
a cluster analysis procedure (Xiong et al., 1995) to correct for
multiple statistical comparisons using a spatial extent threshold that yielded a p < 0.025, one-tailed, significance level
over the entire image. Significant voxels located within the region of
interest of the amygdala were colored according to their level of
significance and overlaid on the averaged structural image.
| |
RESULTS |
Individuals' experience of emotional intensity in the present
study correlated well with normative ratings on emotional valence and
arousal. The average correlation coefficient between subjects' intensity ratings, on the one hand, and normative valence and arousal,
on the other hand, was  0.66 and 0.68, respectively. Thus, subjects'
ratings of emotional intensity reflected equally well the valence and
arousal characteristics of the stimuli.
Amygdala activation was significantly, bilaterally correlated with
higher ratings of individually experienced emotional intensity (Fig.
1). This represents first evidence that
amygdala activation is related to the subjective sense of emotional
intensity.
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Figure 1.
Degree of experienced emotional intensity
correlates with amygdala activation. A, Cluster of
significant correlation between amygdala activation (a priori region of
interest) and subjects' emotional intensity ratings. Left
side of the image is left side of the brain. Figure shows
cluster with Talairach coordinates 24, 10, 15, based on Talairach
and Tournoux (1988), where x = distance in
millimeters to the right (+) or left () of midline;
y = distance anterior (+) or posterior () to the
anterior commissure; and z = distance superior (+)
or inferior () to a horizontal plane through the anterior and
posterior commissures. Additional amygdala clusters (data not shown)
were located at +21, 3, 12, and 28, 3, 15. B,
A time course plot showing average signal intensity in response to
scenes that were rated in emotional intensity from 0 (least intense) to
3 (most intense) for the cluster shown in A. Averages
were made by drawing, for each subject, a region of interest around the
left amygdala. Voxels that exhibited significant (>1.96)
z-scores within this region (representing significant
correlations) were averaged for each subject, and then across subjects,
for each trial type.
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Subjects' ratings of emotional intensity, from 0 to 3, were similarly
distributed across the four intensity categories, with 29, 22, 24, and
25% of all scenes being rated as 0, 1, 2, or 3, respectively.
Therefore, any difference in how well scenes are remembered in a
given intensity category (relative to the other categories) cannot be
attributed to differences in statistical power. Indeed, scenes in these
four categories were not equally well remembered. A repeated-measures
ANOVA testing for the effects of reported emotional intensity (ratings
from 0 to 3) and memory performance (forgotten, familiar, remember)
revealed a significant interaction between intensity and memory
performance (F(6, 54) = 3.01, p < 0.05), indicating that memory performance was
significantly better for scenes that were rated as highly
emotionally intense (i.e., rated 3) than for scenes rated less
emotionally intense. Scenes that were rated mild-to-moderate (ratings 0 to 2) had similar distributions of items that were forgotten, familiar,
or remembered, whereas scenes that were rated as emotionally highly
salient (rated 3) were more memorable, because fewer items were
forgotten and more were familiar and remembered (Fig.
2A). The mean
false-positive rate for foils was 10%, well below the hit rate for
studies scenes, which ranged from 22 to 44% across these intensity
categories.
View larger version (24K):
[in this window]
[in a new window]
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Figure 2.
Enhanced emotional memory correlates with amygdala
activation to highly emotionally intense stimuli. A,
Behavioral data on memory performance as a function of subjects'
ratings of emotional intensity. B, Cluster of
significant correlation between amygdala activation and subjects'
memory for scenes rated as emotionally highly intense (rated 3). The
correlation map was constructed as in Figure 1, except that only trials
rated as 3 were included in the analysis, and activation intensity was
correlated with three trial outcomes: whether an individual item was
forgotten, familiar, or remembered. Left side of the
image is left side of the brain. Coordinates of the amygdala are 20,
10, 14 (Talairach and Tournoux, 1988). C,
Correlation between left amygdala activation and memory for emotional
items increases with greater emotional intensity. Black solid
line shows higher z-score averages across the
amygdala with higher emotional intensity ratings.
Z-scores represent the strength of correlation between
amygdala activation and subsequent memory for emotional stimuli. The
red dotted line shows that there were no pixels within
the amygdala that reached statistically significant
z-score level (<1.96) for scenes that were rated 0 to
2, but there were 14 significant pixels for scenes that were rated
3.
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For scenes that were rated highly emotional (rated 3), the degree of
left (but not right) amygdala activation predicted whether individual stimuli would be forgotten, appear familiar, or be remembered in a later memory test (Fig. 2B). Thus,
little amygdala activation in response to a picture rated as highly
emotionally intense was associated with the subject's forgetting the
stimulus, whereas intermediate and high amygdala activation was
associated with a subject's later report of familiarity or confident
recognition, respectively.
An additional analysis of the left amygdala revealed a significant
correlation between emotional intensity and the modulatory influence of
the amygdala on emotional memory. The correlation between amygdala
activation and subsequent memory grew stronger as subjects experienced
greater emotional intensity (Fig. 2C, black
line), but only reached significant levels for individual pixels
for the most emotionally intense stimuli (Fig. 2C, red line). This analysis suggests that a stimulus may need to exceed a
certain threshold of emotional intensity before amygdala activation is
likely to modulate memory to produce enhanced memory for that stimulus.
This is consistent with the behavioral evidence reported in Figure
2A that shows that only the most emotionally intense scenes were associated with superior memory.
Other locations in frontal and temporal regions were noticed that
correlated with subjects' individual experiences of emotional intensity and subsequent memory. Because these locations did not constitute a priori regions of interest, they will be considered as
tentative constituents of a larger network of structures, until replicated in future studies. The coordinates of these structures are
published on our website
(http://sucia.stanford.edu/~gablab/ index.shtml).
| |
DISCUSSION |
Event-related fMRI revealed an association between individual
experiences of emotional intensity for discrete stimuli with amygdala
activation and subsequent memory for these stimuli. This study found
that (1) the amygdala is sensitive to individually experienced
emotional intensity of discrete visual stimuli; (2) activity in the
left amygdala during encoding is predictive of subsequent memory; and
(3) the degree to which amygdala activation at encoding can predict
subsequent memory is a function of emotional intensity. These findings
provide strong new support for the view that amygdala activation
reflects moment-to-moment subjective emotional arousal and that this
activation enhances memory in relation to the emotional intensity of an
experience. These findings are consistent with the hypothesis that the
human amygdala enhances declarative memory in a phasic fashion.
The role of the amygdala complex in memory has received considerable
attention in recent years. Substantial evidence from studies of both
infra-human and human subjects suggests that the amygdala influences
the storage of explicit memory for emotionally arousing events (Cahill
and McGaugh, 1998). Previous human brain imaging studies showed a
correlation between amygdala activation and enhanced declarative memory
between subjects, but could not dissociate alternative ("tonic" vs
"phasic") interpretations that assigned the amygdala different
causal significance.
The hypothesis that the degree of arousal produced by an emotional
stimulus determines the degree of amygdala participation in memory
storage for the stimulus (Cahill and McGaugh, 1990) predicts that the
relationship between amygdala activity at encoding and subsequent
memory should become stronger as increasingly arousing stimuli are
tested. This important theoretical prediction was not examined in
previous imaging studies. In the present study, the correlation between
amygdala activity and long-term memory increased significantly as the
degree of experienced emotional intensity increased. Whether this
correlation was driven by the arousal or valence characteristics of the
stimuli cannot be determined, because subjects were only asked to give
one rating ("emotional intensity") that correlated equally well
with normative valence and arousal ratings. However, the finding of
Hamann et al. (1999) that the correlation between amygdala activation
and subsequent memory is similar for negative and positive stimuli
argues that valence may not be as relevant a determinant as arousal.
Future work needs to include emotional stimuli of positive valence with differing arousal ratings and address whether arousal plays a similar
role for those stimuli. It is expected that amygdala activation to high
arousal positive (or negative) stimuli would be more predictive of
subsequent memory than activation to less arousing positive (or
negative) stimuli.
In the present study, activity in the left amygdala correlated with
subsequent recognition of emotional material. In two PET studies,
amygdala activity related to negatively valenced emotional stimuli in
the right (Cahill et al., 1996) or right-lateralized (Hamann et al.,
1999) side correlated with recall. An fMRI study (Canli et al., 1999)
reported bilateral amygdala correlations (with larger correlation
clusters on the left). One potential explanation of this difference is
gender. Both previous PET studies used only male subjects, whereas the
previous and current fMRI studies used only females. Laterality could
also conceivably relate to differences between the PET and fMRI
technologies. Clearly, the determinants of amygdala laterality in
influencing memory for emotional events are an important area for
future studies. Some of these determinants may be subtle and relate to
individual differences in the experience of arousal (Canli et al.,
1998), cognitive representations (Phelps et al., 1998), or differences between conscious and unconscious processes (Morris et al., 1998).
Bilateral activity of the amygdala also correlated significantly with
the subjects' emotional ratings of the stimuli. One interpretation is
that a subject's experience of emotional arousal is the result of
amygdala activation, i.e., that the amygdala participates in the
production of emotional responses. This interpretation, however, is
inconsistent with other data suggesting that the human amygdala is not
necessary for the production of emotional responses. Most critically,
subjects with amygdala damage often exhibit normal cognitive (Cahill et
al., 1995; Adolphs et al., 1997; Hamann et al., 1997) and physiological
(Bechara et al., 1995) reactions to emotional stimuli, despite having
impaired long-term memory for the stimuli. One subject with
bilateral, nearly selective amygdala damage even spontaneously
expressed her strong negative emotional reaction to a highly aversive
stimulus, but failed to demonstrate enhanced recall of the same
stimulus (Adolphs et al., 1997). Finally, the results of a recent study
using excitotoxin lesions of the amygdala in monkeys suggest that the
emotional changes produced by selective amygdala damage are far smaller than is generally believed (Meunier et al., 1999). Therefore, although
the present study shows that subjective experience of emotional
intensity is correlated with amygdala activation, other findings imply
that the amygdala may not be necessary to experience emotional
intensity. Our data suggest that the role of the amygdala is to
translate information about the moment-to-moment state of subjective
emotional intensity into the modulation of long-term memory, but only
for the most emotionally intensive experiences.
| |
FOOTNOTES |
Received March 10, 2000; revised July 19, 2000; accepted July 21, 2000.
Correspondence should be addressed to Turhan Canli, Department of
Psychology, Jordan Hall, Stanford, CA 94305. E-mail:
canli{at}psych.stanford.edu.
This article is published in
The Journal of Neuroscience, Rapid Communications Section,
which publishes brief, peer-reviewed papers online, not in print. Rapid
Communications are posted online approximately one month earlier than
they would appear if printed. They are listed in the Table of Contents
of the next open issue of JNeurosci. Cite this article as:
JNeurosci, 2000, 20:RC99 (1-5). The
publication date is the date of posting online at
www.jneurosci.org.
| |
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[Abstract]
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P.-O. Harvey, P. Fossati, and M. Lepage
Modulation of memory formation by stimulus content: specific role of the medial prefrontal cortex in the successful encoding of social pictures.
J. Cogn. Neurosci.,
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K. L. Mackiewicz, I. Sarinopoulos, K. L. Cleven, and J. B. Nitschke
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L. H. Somerville, G. S. Wig, P. J. Whalen, and W. M. Kelley
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B. A. Strange and R. J. Dolan
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E. A. Kensinger and S. Corkin
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B. A. Strange, R. Hurlemann, and R. J. Dolan
From The Cover: An emotion-induced retrograde amnesia in humans is amygdala- and {beta}-adrenergic-dependent
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TOP
ABSTRACT
INTRODUCTION
