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The Journal of Neuroscience, September 1995, 75(g): 5879-5891
Fear and the Human Amygdala
Ralph Adolphs,’ Daniel Tranel,’ Hanna Damasio1s2 and Antonio R. Damasio1’2
‘Department of Neurology, Division of Cognitive Neuroscience, University of Iowa College of Medicine, Iowa City,
Iowa and ‘The Salk Institute for Biological Studies, La Jolla, California
We have previously reported that bilateral amygdala dam-
age in humans compromises the recognition of fear in fa-
cial expressions while leaving intact recognition of face
identity (Adolphs et al., 1994). The present study aims at
examining questions motivated by this finding. We ad-
dressed the possibility that unilateral amygdala damage
might be sufficient to impair recognition of emotional ex-
pressions. We also obtained further data on our subject
with bilateral amygdala damage, in order to elucidate pos-
sible mechanisms that could account for the impaired rec-
ognition of expressions of fear.
The results show that bilateral, but not unilateral, dam-
age to the human amygdala impairs the processing of fear-
ful facial expressions. This impairment appears to result
from an insensitivity to the intensity of fear expressed by
faces. We also confirmed a double dissociation between
the recognition of facial expressions of fear, and the rec-
ognition of identity of a face: these two processes can be
impaired independently, lending support to the idea that
they are subserved in part by anatomically separate neural
systems. Based on our data, and on what is known about
the amygdala’s connectivity, we propose that the amygdala
is required to link visual representations of facial expres-
sions, on the one hand, with representations that consti-
tute the concept of fear, on the other. Preliminary data sug-
gest the amygdala’s role extends to both recognition and
recall of fearful facial expressions.
[Key words: amygdala, emotion, affect, fear, facial ex-
pression, social cognition]
As borne out by two recent reports on human amygdala dam-
age (Adolphs et al., 1994; Young et al., 199.5) the amygdala
is ideally suited to participate in processing visual stimuli that
communicate emotional significance in social situations, such
as facial expressions (Darwin, 1872/1965; Stein et al., 1990;
Kling and Brothers, 1992). We previously reported that bilat-
eral damage to the human amygdala impairs the recognition of
fear in facial expressions (Adolphs et al., 1994). This finding
left open the possibility that unilateral amygdala damage could
produce the same deficit, a question we address here. An ad-
ditional purpose of the present study is to provide a more com-
plete characterization of the processing defect that results from
Received Feb. X, 1995; revised Apr. 25, 1995; accepted Apr. 28, 1995.
We thank all subjects for their participation. This study was supported by
NINDS Grant NS 19632. R.A. is a Burroughs-Wellcome Fund Fellow of the
Life Sciences Research Foundation.
Correspondence should be addressed to Ralph Adolphs, Department of Neu-
rology, 200 Hawkins Drive, Iowa City, IA 52242.
Copyright 0 1995 Society for Neuroscience 0270.6474/95/155879-13$05.00/O
bilateral amygdala damage, in order to suggest mechanisms by
which the amygdala helps to process stimuli related to fear.
Since our study involves vision and emotion, we briefly re-
view the amygdala’s role in these two domains. Highly pro-
cessed visual information reaches the amygdala via temporal
cortices, including areas TE, TEO, and the temporal pole (Her-
zog and Van Hoesen, 1976; Iwai and Yukie, 1987; Amaral et
al., 1992). The inferotemporal cortex in the monkey contains
neurons that respond selectively to the sight of faces and bodies
of conspecifics. These responses can be selective for a particular
face, or a particular view of faces or bodies, for a particular
direction of gaze in the face, or for facial expressions (Perrett
et al., 1982; Hasselmo et al., 1989; Wachsmuth et al., 1994). In
humans, bilateral lesions of the temporal cortex are usually re-
quired to impair recognition of the identity of faces (Damasio
et al., 1990), but unilateral lesions of the right temporal cortex
can be sufficient to impair recognition of emotional expressions
(Bowers and Heilman, 1984; Rapcsak et al., 1989; Rapcsak et
al., 1993). While both the human (Heit et al., 1988; Allison et
al., 1994) and monkey (Leonard et al., 198.5; Rolls, 1992) amyg-
dala also contain neurons that respond selectively to faces, little
is known about the functional significance of this finding. Given
our previous finding that bilateral amygdala damage causes spe-
cific deficits in recognizing facial expressions, we wanted (1) to
investigate the unilateral contributions of the left and right
amygdala independently, and (2) to show how specific to facial
expressions of fear the deficits are.
Evidence suggesting that the amygdala participates in emo-
tion is found in the close links between the amygdala and the
autonomic nervous system (Chapman et al., 1954; LeDoux et
al., 1988; Lee et al., 1988a; Amaral et al., 1992), as well as in
the high densities of binding sites within the amygdala to sub-
stances that modulate fear and aggression, such as the benzo-
diazepines (Niehoff and Kuhar, 1983) and serotonin (Hensman
et al., 1991; Saudou et al., 1994). Some neurons in the monkey
amygdala respond to the affective significance (the rewarding
or punishing contingencies) of sensory stimuli (Nishijo et al.,
1988). Monkeys with lesions of the amygdala are insensitive
to stimuli that normally arouse intense fear (Weiskrantz, 1956;
Blanchard and Blanchard, 1972) and cannot be conditioned to
associate stimuli with fear (Kapp et al., 1982; Hitchcock and
Davis, 1986; LeDoux et al., 1990; Davis, 1992a,b). While
many of these findings may extrapolate to humans, we won-
dered if the amygdala would be equally involved in processing
components of the concept of fear that depend mostly on lan-
guage, as well as those that depend mostly on nonverbal im-
ages. We show here that while bilateral amygdala damage im-
pairs recognition of fearful facial expressions, and impairs their
5880 Adolphs et al. * Fear and the Human Amygdala
recall in imagery, it leaves relatively unaffected verbal knowl-
edge related to fear.
Materials and Methods
Subjects
We compared target subjects, who all had damage to the amygdala, to
a group of brain-damaged controls, who had no damage to the amyg-
dala. The target subjects were chosen on the basis of neuroanatomical
site of lesions, and consisted of one patient with bilateral damage to the
amygdala, three patients with unilateral damage to the left, and three
with unilateral damage to the right amygdala. Control subjects were 12
patients with brain damage, but intact amygdalae, and 7 normal indi-
viduals with no history of neurological or psychiatric disease. Both
target and control brain-damaged subjects were selected from the Pa-
tient Registry of the Division of Behavioral Neurology and Cognitive
Neuroscience at the University of Iowa, and had been fully character-
ized neuroanatomically and neuropsychologically according to the stan-
dard protocols of the Benton Neuropsychology Laboratory (Tranel,
1995) and the Laboratory of Neuroimaging and Human Neuroanatomy
(Damasio and Damasio, 1989; Damasio and Frank, 1992). For each
subject, MR and/or CT scan data were available, and additional neu-
roanatomical analyses were carried out as necessary. Three-dimensional
reconstructions of MR images were obtained for all target subjects in
order to allow a detailed analysis of their lesions (Damasio and Frank,
1992). We excluded subjects who were significantly depressed, as as-
sessed with the Beck Depression Inventory and the Minnesota Multi-
phasic Personality Inventory. All subjects used in our study had given
informed consent to participate in research.
Bilateral amygdalu lesions. Patient SM-046 had nearly complete bi-
lateral amygdala lesions. This subject suffers from a rare, autosomal
recessive, genetic disease, Urbach-Wiethe disease (Hofer, 1973), which
has resulted in bilateral calcification and atrophy of her amygdala (Tra-
nel and Hyman, 1990; Nahm et al., 1993; Adolphs et al., 1994).
Unilaterul umygdala lesions. The six subjects in this group had uni-
lateral damage to the amygdala and to other cortical and subcortical
regions in the anterior temporal lobe, caused by either temporal lobec-
tomy for the treatment of epilepsy, or by herpes simplex encephalitis.
Bruin-damaged controls. Twelve subjects with lesions that did not
include the amygdala were selected to address a number of possibly
confounding variables.
To conclude that a target subject might be impaired in processing
facial expressions of emotion, we needed to exclude the possibility that
defective task performance could be attributed solely to confounding
variables that could also affect performance on our tasks. These vari-
ables included IQ and visuoperceptual function. Our 12 brain-damaged
controls, consequently, included subjects with IQ similar to, or lower
than, that of subjects with amygdala damage. We addressed the possi-
bility of an effect due to the visuoperceptual demands of the task by
including brain-damaged controls who had poor visual acuity or visual
field defects, and who performed at or below the level of target subjects
on standard tests of visuoperceptual function. To control for the bila-
terality of brain damage of SM.046 we included four control subjects
with bilateral brain damage. All 12 subjects had participated as controls
in a previous study of the recognition of emotion in facial expressions
(Adolphs et al., 1994), and included patients with histories of stroke,
tumor, or anoxia.
Normal controls. Seven normal controls, with no history of neuro-
logical and psychiatric disease, were also included in our study, in order
to provide an independent, normal group to which results from subjects
in other groups could be compared.
Experimental tasks
Recognition of facial expressions of emotion. Subjects were shown
black and white slides of facial expressions, and were asked to judge
the expressions with respect to several verbal labels (which were the
adjectives that corresponded to the emotions we showed), as reported
previously (Adolphs et al., 1994). We chose 39 facial expressions from
Ekman and Friesen (Ekman, 1976) that had all been shown to be iden-
tified reliably by normal subjects at greater than 80% success rate. Each
of the 39 expressions was presented six times in two blocks separated
by several hours. Six faces (both male and female) each of anger, fear,
happiness, surprise, sadness, disgust, and three neutral faces, were pro-
jected on a screen, one at a time, in randomized order. Subjects had in
front of them cards with verbal labels describing emotions typed in large
print, of which they were periodically reminded by the experimenter.
Prior to rating faces on any label, subjects were involved in a brief
discussion that clarified the meaning of that word through examples.
Subjects were asked to judge each face on a scale of O-5 (0 = not at
all; 5 = very much) on the following six labels: happy, sad, disgusted,
angry, afraid, surprised (one adjective per block of slides), in random
order. There was no time limit. Care was taken to ensure that all subjects
knew which label they were rating and used the scale correctly. All
subjects understood the labels, as assessed by their ability to describe
appropriately scenarios pertaining to that emotional label.
SM-046 repeated the experiment a total of four times, in two sessions
6 months apart. In both sessions, she was tested by different experi-
menters who were blind to the nature of the experiment, and by R.A.
We also replicated the experiments with six of the brain-damaged con-
trols (data not shown), all of whom gave very consistent intrasubject
ratings.
Data from the task above were analyzed to yield three measures: (1)
subjects’ ratings of a facial expression on the verbal label that corre-
sponded to the emotion expressed. This measure is an index of the
intensity with which subjects judge a prototypical emotion to be ex-
pressed. (2) Correlations between a subject’s ratings of an expression
and normal ratings. This is a measure of recognition of facial expres-
sions of emotion (Adolphs et al., 1994). A subject’s ratings of a facial
expression on the six adjectives were correlated with mean ratings of
that expression given by the seven normal controls. The correlations
were Z-transformed to normalize their distribution, averaged over faces
that expressed the same emotion, and inverse Z-transformed to give the
mean Pearson correlation to normal ratings for that emotion category.
(3) Profile of ratings on all six emotional labels for each of the 39
individual facial expressions. An analysis of the raw ratings given by
subjects allowed us to investigate further those aspects of task perfor-
mance that may have resulted in defective recognition. Details are pro-
vided in the legend to Figure 5.
Recognition of identity of a face. We also assessed subjects’ ability
to recognize and name familiar faces, to provide further evidence that
recognition of the identity and of the emotion expressed by a face are
dissociable (Damasio et al., 1990). Subiects were shown black and
white slides of faces that were cropped to mclude only the head. Stimuli
consisted of faces of famous public figures, or of acquaintances of the
patient. The scores from these tests are presented as “impaired,” “bor-
derline,” or “normal,”
as previously described (Tranel et al., in press).
Drawing facial expressions. The tasks described above do not ex-
haust in any way the characterization of the defect in recognizing fear
in facial expressions. To begin further inquiry on this issue, we carried
out additional, qualitative studies with patient SM-046.
To assess SM-046’s ability to retrieve nonverbal information pertinent
to fear, we asked her, as well as four of our subjects with unilateral
amygdala lesions and four control subjects, to draw pictures of facial
expressions from memory, given both the oral and written command.
She was given unlimited time and was repeatedly prompted by the
experimenter. SM.046 had taken a correspondence art class in drawing,
and enjoyed drawing.
The verbal concept of fear. Interviews were conducted to address
whether SM-046’s defect extends to defective conceptual knowledge of
fear. Her recognition of the meaning of words that denote emotional
states was assessed by asking her to sort printed labels of the words
into piles on the basis of the similarity of the emotion they denote.
Results
Neuroanatomical projiles
MR scans of the subjects with amygdala damage are shown in
Figures 1 and 2. Subject SM-046 had damage that was restricted
to the amygdala, and which may have included some of the very
anterior entorhinal cortex, sparing hippocampus and all neocor-
tical regions (Fig. 1). All of neocortex and the hippocampi are
spared, thus providing a particularly specific case study with
selective amygdala lesions. PET scans confirmed that the tissue
of the amygdala was hypometabolic, consistent with atrophy of
this structure (data not shown).
Our subjects with unilateral amygdala damage included tem-
poral lobectomy cases and two subjects with limitkd damage
from herpes simplex encephalitis (LDV-692 and FR-1465). The
subjects all had unilateral damage to the amygdala and to some
of the surrounding structures in the temporal lobe (Fig. 2).
Neuropsychological profdes
SM-046 is fully dextrous, has an IQ in the low average range,
and a high school education. She has intact visual fields and
normal acuity, can read and write fluently, and has normal color
perception. She has no impairments of memory, language, or
perception, with the possible exception of somewhat impaired
immediate nonverbal memory (Tranel and Hyman, 1990) and
borderline olfactory recognition.
The ability of SM-046 to match simple stimuli across different
sensory modalities, as evidenced by visual-tactile associations
of simple geometric shapes, is normal (Nahm et al., 1993). SM-
046 has an inadequate ability to make decisions in regard to
personal and social matters, and has somewhat inappropriate so-
cial behavior (Tranel and Hyman, 1990; Nahm et al., 1993).
Our subjects with unilateral amygdala damage are all fully
dextrous, and include patients with a large range of IQ. All target
subjects had normal, or corrected to normal, visual acuity, and
none had visual field defects. Table 1 summarizes these data.
Judgments of intensity of emotional facial expressions
We first examined the intensity of emotion that subjects judged
to be signalled by a face. For each face within an emotion
category, subjects rated that face on its prototypical verbal la-
bel (e.g., for happy faces,
“how happy does this person
look?“), on a 6-point scale. Brain-damaged and normal con-
trols, as well as subjects with unilateral amygdala lesions all
endorsed high ratings on this task across every emotion cate-
gory (Fig. 3a), indicating that the expressions were, indeed,
strong, typical expressions of their respective emotions. There
were no significant differences between the ratings given by
brain-damaged controls, normal controls, or subjects with uni-
lateral amygdala damage. While all subjects with left amygdala
lesions rated faces showing disgust or sadness as slightly less
intense than did subjects with right amygdala lesions (p = 0.05
for both emotions; Mann-Whitney U test), we do not think this
finding is significant for our study, since all six subjects’ rat-
ings fell within the range of ratings given by brain-damaged
controls. Future studies, with planned comparisons between
larger numbers of unilaterally lesioned subjects, might follow
up this finding in relation to possible hemispheric asymmetries
in processing emotion, as has been suggested for other brain
regions (e.g., Davidson, 1992).
Our subject with bilateral amygdala damage, SM-046, judged
faces showing fear to be less intense expressions of that emotion
than did any of the brain-damaged controls, or than did any of
the subjects with unilateral amygdala damage (Fig. 3b). SM-046
also differed from brain-damaged controls in her judgments of
faces expressing emotions normally judged to be similar to fear:
she judged surprised and angry faces to signal less surprise or
anger than did controls. Her average ratings of surprise and fear
were 5 SD below the mean of thecbrain-damaged controls’ rat-
ings; her ratings of anger were 3 SD below the control mean,
and her ratings of all other emotions were within 1 SD of the
control mean. These results suggest that bilateral, but not uni-
lateral, damage to the amygdala impairs judgments of the inten-
sity of expressions of fear, and of expressions normally judged
to be very similar to fear, such as surprise.
The Journal of Neuroscience, September 1995, k?(9)
5881
Figure
1. MR scans of the brain of SM-046. From
top to bottom:
coronal section at the level of the hippocampus; coronal section at the
level of the amygdala; horizontal section at the level of the amygdala.
SM-046 has extensive and bilateral damage to the amygdala
(arrows),
but not to other structures,
such
as the hippocampus
(top).
Recognition of emotional facial expressions
To assess recognition of facial expressions, we asked subjects to
rate the face not just on the verbal label that described it best,
but also on labels denoting other emotions. The rationale for this
5882 Adolphs et al.
l
Fear and the Human Amygdala
A.
Figure 2.
Sites of lesions of
subjects
with unilateral amygdala damage. A,
Subjects with left amygdala lesions. B,
Subjects with right amygdala lesions.
For each subject, coronal and horizon-
tal sections at the level of the amygdala
are shown at leji and right, respective-
ly. The intact amygdala on one side is
indicated with an asterisk. Note that the
left side of the image corresponds to
the right side of the brain, and vice ver-
sa.
method came from previous studies with normal subjects, which
typical facial expression of surprise, and yet also be judged to
showed that facial expressions signal more than one emotion,
exhibit some happiness, or some fear. Asking subjects to apply
and that emotion categories have fuzzy and overlapping bound-
a single label to a facial expression will thus not be a complete
aries (Russell and Bullock, 1986; Russell and Fehr, 1987; Rus-
index of all the information recognized, and is not a sensitive
sell, 1991). For example, a surprised person can have a proto-
test of recognition of emotion.
B.
The Journal of Net Jroscience, September 1995, 15(9)
5883
Figure 2.
Continued.
Brain-damaged controls and subjects with unilateral amygdala
domed ratings for afraid faces that correlated very poorly, or not
damage gave ratings of the faces that correlated well with nor- at all, with normal ratings, and which correlated more poorly
mal ratings (Fig. 4). Our subject with bilateral amygdala dam-
with normal ratings than did the ratings given by any brain-
age, by contrast, had a severe impairment in the ability to rec- damaged control (Fig. 4).
ognize some expressions, as assessed by this task. SM-046 en-
These data show that bilateral, but not unilateral, damage to
5884 Adolphs et al.
l
Fear and the Human Amygdala
Table 1. Background neuropsycbology of subjects
Visuoperceptual
function (%ile)
Subject Age/sex
VIQ PIQ
Lines Faces
4.5
Bilateral amygdala damage
SM-046 30/F 86
Left amygdala damage
LV-580 31/F
81
JS-1077 22&l
129
UB-1251 35/M 93
Right amygdala damage
LDV-692 3 l/F 87
FR-1465 64lM
100
AK- 1603 25/F 106
Brain-damaged controls
CE- 1023 68/M 117
m-1257 73/M
117
RM- 1362 68/M
96
RJ- 1374” 52/M 96
JR-1584 51/M 90
RJ- 1605 49/M
1146
DE- 1607 77/F
98
RS-165@ 49/M 101
BL- 1 722d 52/F 85
RM- 1740 63/M
94
MR- l79@ 62/F 97
90 11th 90th
112 40th 49th
126 74th 8th
99 22nd 49th
77 11th
4th
130 72nd 77th
133 56th 32nd
'r;
3
a
a 2.5
5
z 2
1.5
96
93
110
96
111
112b
90
82
85
101
80
115
40th
86th
86th
NT
99th
NT
22nd
4th
0th
NT
6th
97th
15th
7lst
49th
15th
49th
71st
49th
NT
77th
71st
happy surprise
sgusted sad
0
Brain-damaged controls
-- Normal controls
4 Left Amygdala damage
b Right Amygdala damage
0 SM-046
56th CF- 1899 64/M 120
VIQ. PIQ: verbal and performance IQs from the Wechsler Adult Intelligence
Test-Revised (WAIS-R) (Wechsler, 1981). Lines: ability to discriminate be-
tween orientation of lines (Benton et al., 1983). Faces: ability to discriminate
between similar faces (Benton et al., 1983). Underlined subjects have bilateral
lesions. NT: Not tested.
(’ Blind in one visual field.
h Estimated from the National Adult Test-Revised.
’ Perimetric mapping indicated complete blindness in the left visual field, and
macular sparing not extending past 10” eccentricity in the right visual field.
” Nearly blind in left eye; achromatopsic.
5_
4.5-r,
cm
41
un
3.5-3;
Cl
El
Cl
cl
El
Cl
0.5:
0
happy
mprise afraid
Cl
Cl
cl
Cl
0
cl
m
cl
all
0
isguste sad
the amygdala impairs the processing of some facial expressions
of emotion. The recognition of fear appears to be most severely
impaired.
Recognition
of
multiple emotion categories
The impaired recognition of expressions of fear seen in SM-046
could have several causes at the level of task performance. She
might not know what fearful faces signal at all, or she might
misrecognize fear as another emotion. To address this issue, we
analyzed each facial expression’s membership in different emo-
tion categories. Figure 5 shows the ratings given by subjects for
all the faces, on all the different adjectives that describe emotions.
Controls show peaks in their rating profiles that coincide with the
facial expression most typical of that adjective: happy faces re-
ceived the highest ratings on “happf,” sad faces on “sad,” and
so on. Several important points emerge from the data of the con-
trols
(both
brain-damaged and normal controls): (1) there are pro-
totypical expressions that best exemplify an emotion, (2) most
faces belong largely to one emotion category, (3) most faces also
have some membership in other categories of emotions that are
judged to be similar, (4) most faces therefore signal multiple emo-
Figure
3. Ratings of the intensity of an emotion in facial expressions.
Rating scores (from O-5) on the emotional word for which the face was
a typical example are shown as the mean of all faces within an emotion
category.
A,
Data from 12 brain-damaged controls
(0).
3 subjects with
left (d), and 3 with right (b) amygdala damage. B, Mean data from
four experiments with SM-046 (0).
The Journal of Neuroscience, September 1995, 15(9) 5885
0 Controls
0 ’
happy surprisec afraid
b Right
Amygdala
q Left
Amygdala
8
?
El
4
0
angry
isgustel
!
t
8
4
sad
0.5-
0
happy
El
0
;urprisc
a SM-046
El
q
afraic
Ei
awry
u
isgusl
0
El
sad
Emotion Category of Faces
Figure 4. Correlations of subjects’ ratings with normal ratings. Mean Pearson correlations are shown of mean normal control ratings (n = 7)
correlated with the ratings given by brain-damaged controls (0;)
II = 12, by subjects with left amygdala lesions (4; IZ = 3), and subjects with
right amygdala lesions (b; n = 3) (left), and correlated with the ratings given by SM-046 (0; four experiments) (right). All normal controls’ ratings
c&elatedwell with one another (Y 5 0.7 for every emotion category).
tions. These observations have been made in previous studies of
normal subjects (e.g., Russell and Bullock, 1986).
Normal controls, brain-damaged controls, and patients with
unilateral amygdala damage yielded similar data in this analysis.
However, SM-046 differed from all other subjects in the ratings
she assigned to some faces (Fig. 5). SM-046 failed to assign
high ratings of fear to faces that controls judge to depict fear.
She also failed to assign normal ratings of fear or of surprise to
faces that are judged similar to fear, such as surprised faces.
However, the highest ratings that SM-046 gave on the adjective
“afraid” do correspond to faces expressing fear or surprise. In
one session (January) she generally gave such faces higher
scores on adjectives denoting emotions other than fear, leading
to classification of the expression into an incorrect emotion cat-
egory. Consequently, SM-046 often described faces depicting
fear as surprised or angry. In another session (July), she did not
give fearful faces high ratings on any emotion label (Fig. 5).
We followed up this experiment by asking SM-046 explicitly
to comment in more detail about those fearful facial expressions
that she had been unable to recognize, and that she had rated as
not being afraid. Although she could recognize that an emotion
was being expressed (she did not think they were neutral), she
was unsure of what the emotion might be, supplying answers
that included surprise, anger, disgust, sadness, and, on some oc-
cassions, fear.
Given these data, and the further finding that SM-046 never
attributed a clearly absent emotion to faces expressing fear (she
never called them happy, for instance), we think that the primary
defect in SM-046 consists in a specific insensitivity to the emo-
tion of fear in facial expressions, with intact recognition of all
other emotions.
Double dissociation between recognition
of
identity
and
expression
SM-046 had no difficulty recognizing people by their faces. She
correctly identified 19 of 19 acquaintances (Adolphs et al.,
1994), and learned the identity of new faces with ease (Table
2). She also performed normally in discriminating similar faces
from one another (Tranel and Hyman, 1990; see Table 1).
Several of the patients with unilateral amygdala lesions had
difficulty in naming familiar faces, which we have previously
attributed to damage to anterior temporal cortices (Damasio et
al., 1990). The two patients with the most extensive lesions of
the temporal lobe (LDV-692 and FR-1465) were also signifi-
cantly impaired in recognizing the identity of faces (Table 2).
These data provide additional evidence for a double dissoci-
ation (cf. McCarthy and Warrington, 1990, pp 17-19) between
recognition of emotion and of identity in faces: while SM-046
is impaired at recognizing some emotional facial expressions,
but not facial identity, two of our other subjects, LDV-692 and
FR-1465, were impaired at recognizing facial identity (cf. Tranel
et al., 1988, patient #2), but not emotion in facial expressions.
These results are consistent with previous findings that recog-
nition of facial identity can be impaired while sparing recogni-
tion of the emotion signalled by a face (Tranel et al., 1988;
Damasio et al., 1990; Humphreys et al., 1993).
5888 Adobhs et al. * Fear and the Human Amvodala
DISGUSTED
S&l-046: January 9-l
Table 2. Recognition and naming of familiar faces
Subject
Recognition Naming
Bilateral amygdala damage
SM-046 normal normal
Left amygdala damage
LV-580 normal impaired
JS-1077 normal normal
UB-1251 normal impaired
Right amygdala damage
LDV-692 impaired impaired
FR-1465 impaired impaired
AK- 1603 normal normal
Brain-damaged controls
CE-1023 normal normal
WW-1257 normal normal
RM-1362 normal borderline
RJ-1374 normal normal
JR-1584 normal normal
RJ- 1605 normal normal
DE- 1607 normal normal
RS-1658 normal normal
BL-1722 normal normal
RM-1740 NT NT
MR-1790 normal normal
CF-1899 normal normal
Drawing ,facial expressions
We now describe the results of more qualitative experiments,
which are intended to supplement the above data. Might SM-
046’s impairment be limited to recognition, or might she have a
more general impairment in memory for stimuli with emotional
meaning? This question is especially important, as recent evi-
dence suggests that there are double dissociations between im-
pairments of visual perception and impairments of visual im-
agery (Behrmann et al., 1992; Guariglia et al., 1993).
To assess the ability of SM-046 to construct an image of an
afraid face, we asked her and eight other subjects to draw pic-
tures of facial expressions from memory. This task was admin-
istered immediately after subjects had been exposed to all the
pictures of facial expressions used in our other experiments.
They thus had significant exposure to facial expressions just pri-
or to the drawing session.
Subjects vary widely in their ability to draw facial expressions.
However, all subjects that were able to draw disgusted or angry
faces, or able to draw faces in the detail that SM-046 did, were
able to draw clear facial expressions of fear. All patients with
unilateral amygdala damage that we tested on this task (n = 4)
were able to draw facial expressions of fear, although many sub-
t
The Journal of Neuroscience, September 1995, 15(9) 5887
jects found fear, anger, and disgust more difficult expressions to
draw.
SM-046’s drawings are reproduced in Figure 6. SM-046 was
able to produce without difficulty skillful renditions of all facial
expressions except fear. She often provided additional context,
and enjoyed drawing. However, she was entirely unable to draw
expressions of fear. She explained that she did not know what
an afraid face would look like, and that she was unable to draw
any depiction of it. The experimenter had to prompt repeatedly
to elicit any kind of drawing of fear at all; she produced her
drawing only after several failed attempts. She knew, however,
that people who are afraid will tend to cower, and are typically
portrayed with their hair standing on end, two features that did
find their way into her drawing (Fig. 6). But she could not bring
to mind any image of a facial expression to go with fear, and,
accordingly, this was the only one of her six drawings that did
not include a frontal view of the face.
The
concept of fear
The above results might suggest that SM-046 simply lacks the
concept of fear, and thus cannot evoke this concept when she
encounters a facial expression that denotes it. However, our in-
terviews with her revealed that she does know (a) what sorts of
situations would evoke fear in people (being threatened, being
alone in a dark alley at night, and so on), and (b) how frightened
people tend to behave (their heart pounds, they may scream, and
they try to run away). During the course of extensive interviews,
SM-046 used the words, “fear,” “afraid,” “frightened,” appro-
priately.
We further tested SM-046’s ability to recognize the meaning
of words denoting emotions by her ability to sort a set of 28
adjective labels into various numbers of piles on the basis of the
similarity of the emotion denoted by an adjective. She performed
normally on this task, and grouped together the words, “afraid,”
“scared,” “worried,” “terrified,” and “alarmed,” indicating
that she found them to be closely related.
We have no way of testing for all components of the concept
of fear in SM-046. It does appear that she can access many im-
portant components of the concept, provided that they admit of
verbal description. We think it likely, however, that SM-046 does
not experience fear in a normal way, as we have found no con-
vincing evidence that she feels frightened given the appropriate
stimulus, and have preliminary evidence that she fails to exhibit
the full range of psychophysiological responses to fear (A. Be-
chara, R. Adolphs, D. Tranel, personal observation). This issue
requires additional studies, some of which are now underway.
Discussion
Based on a series of quantitative tasks, we have shown that
bilateral amygdala damage (1) impairs judgments of the intensity
of faces depicting fear, (2) impairs judgments of faces depicting
fear with respect to several emotional labels, (3) impairs the
ability to detect fear in faces predominantly depicting other ex-
category
is denoted on each plot by the colored bar at the very top of the graph. The y-axis represents the mean rating (from O-5) given to a facial
expression. Each of the differently colored lines corresponds to the ratings endorsed on a particular emotional label. For ease of visualization, all
plots were smoothed as follows. We triplicated the summed raw data for each plot, producing three plots strung together, in order to embed the
center plot in continuous data, and applied a Lowess smoothing filter with a 5% window. The center plot of the three plots was used, and numbers
were divided by the number of datasets to produce the final plot shown on the figure. Careful comparisons with the raw data confirmed that the
smoothing procedure conservatively captured the relevant trends in the data without producing artifacts. Top: data from brain-damaged (n = 12)
and normal controls (n = 7). Middle:
data
from subjects with left (n = 3) and right (n = 3) unilateral amygdala damage. Bottom: data from subject
with bilateral amygdala damage. Each of the two plots for SM-046 correspond to the mean of two experiments.
5888 Adolphs et al. * Fear and the Human Amygdala
HAPPY
SUiiPRISED
ANG-i3Y
SAD
tJ/ /.’
DISGUSTED
AFRAID
Figure 6. SM-046’s drawings of facial expressions from memory. SM.046 tended to provide context to her drawings, in all cases appropriate.
She insisted that she did not know how to draw an afraid face, because she did not know what such an expression would look like. Her drawing
was produced only after repeated prompting, and she was not satisfied with it.
pressions (such as surprise), and (4) leaves intact the ability to
recognize the identity of faces. In addition, based on supple-
mentary, qualitative tasks, we suggest that bilateral amygdala
damage compromises the ability to reconstruct visual images of
faces that depict fear, while leaving intact many aspects of the
concept of fear that can be verbally described. None of the sub-
jects with
unilateral
amygdala damage were impaired at rec-
ognizing any facial expressions.
Taken as a whole, these results suggest that bilateral amygdala
damage impairs the processing of facial expressions of fear both
in recognition and in recall. However, the full scope of the im-
pairments that follow bilateral damage to the human amygdala
will be broader than what we have reported here. For example,
it is likely that behaviors that depend on recognition of facial
expressions, such as components of social behavior, are also
compromised in some way.
One important issue is the age of subjects at the onset of their
amygdala damage: all patients with unilateral amygdala damage
sustained damage to this structure in late adolescence or in adult-
hood. They would thus have had many years with bilaterally
The Journal of Neuroscience, September 1995, 15(9) 5889
intact amygdalae prior to sustaining their lesion. It is somewhat
less clear at what point in time SM-046 acquired her amygdala
lesions. We cannot reconstruct the time course of SM-046’s le-
sions with any certainty. However, the literature on Urbach-Wie-
the disease (Hofer, 1973) together with reports of SM-046’s
childhood, suggest that the neurological symptoms that can re-
sult from this disease are progressively acquired throughout late
childhood and adolescence, as calcified material continues to be
deposited in the tissue and blood vessels of mesial temporal
structures. We thus consider it likely that all our patients with
amygdala lesions acquired such lesions several years into their
life, and had occasion to develop an initially normal concept of
fear prior to the onset of their lesion.
Studies of the amygdala in humans
Studies of the amygdala in humans have come largely from two
sources: surgical lesions and electrical stimulation. Although
surgical lesions of the human amygdala suffer from the draw-
back that they may be incomplete, and that the subjects may not
be normal prior to the surgery (Narabayashi, 1972; Jacobson,
1986; Lee et al., 1988a,b), a review of these cases (Aggleton,
1992) strongly supports the role of the amygdala in processing
fear and aggression and in social behavior. Electrical stimulation
studies of the amygdala in epileptic patients also suffer from
comparable drawbacks, but are again suggestive of functions
related to fear, aggression, and social behavior (Chapman et al.,
19.54; Heath et al., 1955; Halgren et al., 1978; Gloor et al.,
1982).
Our subject SM-046 provides a rare opportunity to examine
selective and bilateral lesions of the amygdala in humans. A
recent report of two other patients with Urbach-Wiethe disease
suggested that they were impaired in processing information that
had emotional significance (Markowitsch et al., 1994). Func-
tional imaging studies with PET in these patients (Markowitsch
et al., 1994), as well as in SM-046, confirmed that the amygdala
is severely hypometabolic, as would be expected of atrophic
tissue.
The amygdala is an essential link in the response to stimuli
with emotional value
In primates, the amygdala projects back to all visual cortices,
including the striate cortex (Amaral and Price, 1984; Iwai and
Yukie, 1987; Amaral et al., 1992). It is thus possible that high-
level feedback from the amygdala directly participates in the
activity of those regions, during both perception (Rolls, 1992)
and visual imagery (Damasio et al., 1993; Kosslyn et al., 1993).
We envision the function of the human amygdala as a high-order
“convergence” zone for the social, homeostatic, and survival-
related meaning of a class of complex stimuli, such as facial
expressions of some emotions (Damasio, 1989; Damasio and
Damasio, 1993; Damasio, 1994). In this view, to recognize
someone as afraid, the amygdala must make the sight of the
fearful face activate myriad cortical and subcortical regions,
whose ensemble, temporally coordinated activity constitutes the
concept of fear. Important components of such a distributed,
macroscopic neural representation would result from the amyg-
dala’s engagement of limbic and somatic activity during danger
or threat, and from the engagement of sensory cortices that rep-
resent entities and scenarios related to fear. The amygdala may
thus orchestrate patterns of neural activation in disparate sectors
of the brain that would encode both the intrinsic, physical fea-
tures of stimuli (e.g., shape, position in space, and so on), and
the value that certain stimuli have to the organism (e.g., their
emotional significance).
We propose that SM-046 can perceive the visual features of
a face normally; i.e., she constructs normal percepts of the phys-
ical features of a face. She can also connect such percepts with
the class of knowledge necessary to identify a familiar person:
the sight of a familiar face activates internal responses that sub-
sume knowledge pertinent and specific to that unique face. How-
ever, she lacks the ability to link the perception of certain con-
stellations of facial features to the class of knowledge related to
emotions, specifically to the knowledge of fear: the perception
of an expression of fear fails to activate responses that subsume
the concept of fear (these responses would include autonomic
changes, changes in posture, and facial expression of SM-046,
mental images describing scenarios related to fear, verbal reports
pertaining to the fearful face, etc.). The broken link in SM-046
affects a bidirectional process: she cannot retrieve knowledge
about fearful faces when confronted with the face, and she also
cannot generate constellations of the facial features of fear in
imagery when given the verbal label.
When SM-046 fails to recognize fear in facial expressions,
what does she think those expressions are? SM-046 sometimes
described faces denoting fear as looking surprised or angry, be-
havior exhibited also by normal subjects to some degree. Rarely,
she would even describe a face as looking afraid, but always
insisted that it was not very afraid. In several experiments, she
appeared to have no idea what emotion was being signalled by
an afraid face, and gave the face the lowest possible ratings on
all emotion labels. Our interpretation is that SM-046 did not
think afraid faces looked as afraid as the controls thought they
did. However, since she was able to recognize other emotional
expressions, she also did not think that afraid faces exhibited an
emotion that was not at all present (for instance, she never
thought afraid faces looked happy).
Interestingly, SM-046 did give the highest mean ratings on
the adjective “afraid” to faces that depicted fear, just as controls
did (Fig. 5), but she was quite abnormal in the low magnitude
of fear she ascribed to those faces. These results are consistent
with our proposal: SM-046 can decide to some extent whether
a person may be expressing fear or not, possibly by reasoning
from prototypical features she knows to accompany fear (e.g.,
wide eyes), and possibly reasoning from exclusion of other emo-
tions that she can recognize normally. However, she lacks the
ability to link the perception of the expression with knowledge
that would allow her to judge the intensity of the emotion. Our
proposal, then, is that the amygdala is essential to retrieve com-
prehensive knowledge related to the concept of fear.
Her impaired ability to produce drawings of expressions of
fear lend further support to this interpretation. Although SM-046
was able to portray some of the stereotypical features normally
associated with the expression of fear (cowering posture, hair
standing on end), she was unable to construct an image of a
facial expression. This task requires the generation of an image
on the basis of its link to a verbal label denoting a concept. We
propose that the ability to link representations of facial expres-
sions of fear to other components of the concept of fear is bi-
directionally defective in SM-046.
The amygdala and social behavior
The behavioral impairments of amygdalectomized monkeys are
most severe in the wild, resulting in the death of the animal if
left unattended in its troop (Kling and Brothers, 1992). Neurons
5890 Adolphs et al. * Fear and the Human Amygdala
within the amygdala are active during social interactions (Kling
et al., 1979) and social communication (Jurgens, 1982). The pro-
found social dysfunction of amygdalectomized animals (Rosvold
et al., 1954) can be understood in the context of the findings
described above. The integration of complex sensory informa-
tion, such as recognition of faces, with the motivational valence
of the stimulus, is especially important in order to recognize
social intentions, social status, and to guide behavior on the basis
of social cues (threats, warnings, submissive gestures; Kling and
Brothers, 1992).
It is noteworthy that the behavior of SM-046, even in real
life, is not nearly as impaired as that of monkeys with experi-
mental amygdala lesions. She has a history of inadequate social
decision making, somewhat inappropriate behavior, failure to
maintain employment or marital relations, and she depends on
welfare. Nonetheless, SM-046 is not a social outcast. One reason
for the discrepancy between social behavior in amygdalectomi-
zed monkeys and in SM-046 might be that the monkeys have
more complete lesions, or lesions in structures other than the
amygdala. Another reason for the difference may be that the
amygdala is less important to social behavior in the case of
humans than in the case of monkeys. Humans can engage de-
clarative knowledge and reasoning in a purely verbal mode,
which largely parallels the nonverbal processes directly guided
by circuits that include the amygdala. Nonetheless, we believe
complex social and aesthetic judgments in humans do require
all the neural machinery used to process emotions, and certainly
do include the amygdala (Damasio, 1994). It is only that the
deficits produced by dysfunction in these basic systems may be
partially masked by the intact propositional competence of hu-
mans, thus making the behavioral sequalae of bilateral human
amygdala damage somewhat more subtle.
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