Neuropsychologia 37 (1999) 1135±1141

www.elsevier.com/locate/neuropsychologia

Normal recognition of emotional similarity between facial

expressions following bilateral amygdala damage
Stephan B. Hamann a,*, Ralph Adolphs b
a
Department of Psychology, Emory University, 532 North Kilgo Circle, Atlanta, GA 30322, USA
b
Department of Neurology, University of Iowa, College of Medicine, Iowa City, IA 52242, USA
Received 24 August 1998; accepted 4 February 1999

Abstract

Bilateral damage to the amygdala in humans has been previously linked to two de®cits in recognizing emotion in facial
expressions: recognition of individual basic emotions, especially fear, and recognition of similarity among emotional expressions.
Although several studies have examined recognition of individual emotions following amygdala damage, only one subject has
been examined on recognition of similarity. To assess the extent to which de®cits in recognizing similarity among facial
expressions might be a general consequence of amygdala damage, we examined this ability in two subjects with complete
bilateral amygdala damage. Both subjects had previously demonstrated entirely normal recognition of individual facial emotions.
Here we report that these two patients also are intact in their ability to recognize similarity between emotional expressions.
These results indicate that, like the recognition of individual basic emotions in facial expressions, the recognition of similarity
among emotional expressions does not have an absolute dependence on the amygdala. # 1999 Elsevier Science Ltd. All rights
reserved.

Keywords: Amygdala; Facial emotion; Expression; Similarity; Recognition

1. Introduction recognize similarity between di€erent facial expressions

Several recent neuropsychological studies have inves-
tigated the role of the amygdala in the recognition of
emotion in human facial expressions. The ®rst of these
studies described patient S.M., a 30-year old female
with nearly complete bilateral destruction of the amyg-
dala through calci®cation resulting from congenital
Urbach-Wiethe disease [2]. In that initial report, two
facial emotion processing de®cits were identi®ed in
S.M. The ®rst was an impairment in recognizing
speci®c emotions in facial expressions, particularly
fear. This de®cit was revealed by her inability to recog-
nize the emotion fear in a task that involved judging
the intensity of individual basic emotions in facial ex-
pressions. The second de®cit involved the ability to
* Corresponding author. Tel.: +1-404-727-4261; fax: +1-404-727-
0372.
E-mail address: shamann@emory.edu (S.B. Hamann)
of emotion that normal subjects rate as similar. When
shown two facial expressions and asked to rate their
emotional similarity, S.M. gave abnormally low simi-
larity ratings to pairs of expressions that normal sub-
jects judge as similar, such as anger and disgust or fear
and surprise. Further analysis indicated that S.M. gave
abnormal similarity ratings because she could only
recognize the most dominant or prototypical emotion
in each facial expression, in contrast to normal sub-
jects who can recognize that a given facial expression
can contain a blend of di€erent intensities of di€erent
emotions [17]. From these data, Adolphs et al. [2] con-
cluded that the amygdala may be indispensable to
recognizing individual basic emotions in facial ex-
pressions (especially fear) and in recognizing similarity
between di€erent facial expressions.
Following upon this initial report, several neuropsy-
chological studies have investigated de®cits in recogniz-
ing individual basic emotions in facial expressions in

0028-3932/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 2 8 - 3 9 3 2 ( 9 9 ) 0 0 0 2 7 - 5
1136 S.B. Hamann, R. Adolphs / Neuropsychologia 37 (1999) 1135±1141
patients with bilateral amygdala damage [4,6,22,23].
These studies have generally supported the link
between bilateral amygdala damage and facial emotion
de®cits involving fear and other negative emotions,
although such de®cits are not invariably present [3,9].
Neuroimaging studies have also provided evidence that
the amygdala has an important role in the perception
of fearful, angry, and happy facial expressions
[4,12,13,21].
In contrast to the extensive scrutiny that the relation
between amygdala damage and de®cits in recognizing
individual basic emotions in facial expressions has
received, however, no studies have investigated S.M.'s
other de®cit, the inability to recognize similarity
between di€erent facial expressions of emotion. It is
important to examine the nature of this de®cit further
in other patients with bilateral amygdala damage for
two reasons. First, it is not known to what extent this
facial emotion de®cit is general to other cases of bilat-
eral amygdala damage besides S.M. Secondly, it is
unclear whether the two facial emotion recognition
de®cits that S.M. exhibited are separate or whether
they simply re¯ect di€erent aspects of the same under-
lying de®cit.
The current study investigated these issues in two
postencephalitic patients, E.P. and G.T. [9], each of
whom have complete bilateral amygdala lesions. We
assessed the ability of E.P. and G.T. to recognize simi-
larity between emotional expressions using the same
task that Adolphs et al. [2] used previously with
patient S.M. In addition to collecting these new data,
we conducted a reanalysis of the raw facial emotion
recognition data from a previous study with these
patients [9], using multidimensional scaling (MDS)
techniques to address the same issue in a di€erent way.
In an MDS plot, facial expressions of emotion that a
subject perceives as similar are represented as close
together, whereas expressions that are perceived as dis-
similar are represented as far apart. Patient S.M.
exhibited an abnormal MDS plot that indicated that
she failed to perceive normally the similarity between
di€erent facial expressions of emotion [2]. We com-
pared the MDS plots generated for E.P. and G.T. to
those obtained previously for S.M. and normal control
subjects to examine whether E.P. and G.T. would be
normal or abnormal on this additional measure.
E.P. and G.T. are notable in that they have been
shown previously to exhibit normal recognition of
speci®c facial emotions, including fear, despite com-
plete bilateral lesions to the amygdala [9]. Thus, if E.P.
and G.T. are impaired on recognizing similarity
between di€erent facial expressions, this would imply
both that the similarity-recognition de®cit is not
unique to S.M. and also that this ability is dissociable
from the ability to recognize speci®c emotions in facial
expressions, suggesting that the two facial emotion def-
icits that S.M. previously exhibited are in fact separate.
Conversely, if both E.P. and G.T. can recognize simi-
larity between emotional expressions normally, this
would indicate that the de®cit that S.M. exhibited in
this ability does not generalize to all cases of bilateral
amygdala damage and would demonstrate that this
ability does not have an absolute dependence on the
amygdala, paralleling the ®ndings of the previous
report that examined the ability of these two patients
to recognize speci®c emotions in facial expressions [9].
2. Method
2.1. Subjects
Two males who survived herpes simplex encephalitis
(E.P. and G.T., aged 73 and 59 respectively) partici-
pated in the study. Both patients have complete bilat-
eral lesions of the amygdala con®rmed by MRI, as
described in previous case reports [2,18]. E.P.'s bilat-
eral amygdala damage extends rostrally to the tem-
poral pole and caudally to include the hippocampal
formation. There is also severe atrophy of the entorh-
inal, perirhinal, and parahippocampal cortices. G.T.'s
damage extends through the anterior 7.0 cm of the left
temporal lobe and through the anterior 5.0 cm of the
right temporal lobe. The lesion includes bilaterally the
amygdaloid complex, hippocampus, entorhinal, peri-
rhinal, and parahippocampal cortices as well as the in-
ferior, middle, and superior temporal gyri. There is
also bilateral damage in insular cortex, medial and
orbital frontal cortex, and cingulate gyrus.
Both patients are profoundly amnesic due to their
medial temporal lobe damage but have IQ scores in
the normal range (Wechsler Adult Intelligence Scale-
Revised [19]; Verbal IQ=98 and 88, Performance
IQ=111 and 99, Full Scale IQ=103 and 92, respect-
ively). The severity of the amnesia is documented by
their zero scores on several tests of anterograde amne-
sia [10,14,18]. Their mean scores were 106, 57, 66, 55,
and 53 on the ®ve indices of the Wechsler Memory
Scale-Revised [20] (Attention-Concentration, Verbal
Memory, Nonverbal Memory, General Memory, and
Delayed Memory). These 5 indices yield means of 100
in the normal population (S.D.=15) and minimum
scores of 50. E.P. and G.T. are also anomic (Boston
Naming Test [11] score=42 and 18 out of 60, respect-
ively; normal score>50), and E.P. has some behavioral
evidence of frontal-lobe dysfunction.
2.2. Materials and procedure
2.2.1. Facial expression similarity task
The ability of E.P. and G.T. to recognize similarity
between facial expressions of emotion was assessed
 S.B. Hamann, R. Adolphs / Neuropsychologia 37 (1999) 1135±1141
with the same task that Adolphs et al. [2] had used to
assess this ability with patient S.M. Twenty-one facial
expressions, depicting happy, surprised, afraid, angry,
disgusted, sad and neutral emotion (three of each
emotion) were each converted from the Ekman [7]
slide set into glossy 5  7 in black-and-white photo-
graphs and presented as pairs for subjects to rate for
similarity (see Appendix for a list of the speci®c stimuli
used).
For each pair, subjects directly judged the similarity
between the emotions expressed in each face using a 5-
point Likert-type rating scale. Presentation rate was
subject-paced, although subjects were encouraged to
make their rating as soon as they were sure of their re-
sponse. The rating scale was printed on a card that
was placed below the pair of photographs. At the top
of the card was printed the question, `How similar do
you think these two people are feeling?' Below this
question were the numbers 0±5 ordered from left to
right. Short explanations were presented below each
number: `0: feeling completely the opposite emotion; 1:
not feeling the same emotion; 2: feeling maybe a little
similar emotion; 3: feeling a similar emotion but not
the same one; 4: feeling the same emotion but not
equally strongly; 5: feeling identical (same degree of
the same emotion)'. The rating scale was thoroughly
explained to subjects, and subjects were frequently
reminded of the meaning and use of the scale during
the procedure. Despite E.P. and G.T.'s profound
amnesia, both patients could understand and use the
rating scale, albeit with frequent reference to the rating
card and frequent reminding from the experimenter.
These patients have also demonstrated normal compre-
hension and use of other, similar Likert-type rating
scales [8,9].
The following procedure was used to present the
facial emotion photographs. On the ®rst trial, one
photograph was selected randomly and placed either
to the left or right (randomly determined) of midline
on the table in front of the subject. Each of the
remaining photographs was then placed next to this
photograph one at a time (on the other side of the
midline), and then was removed after the subject made
a response. After all of the remaining photographs
were presented, the ®rst selected photograph was
removed from the set and was not presented again.
The order of the remaining photographs was then ran-
domized and the procedure was repeated with a new
randomly selected card. This procedure was repeated
until all photographs were exhausted. In this way, all
possible pairwise combinations of these 21 facial ex-
pression photographs (210 total pairs, irrespective of
left-right position) were presented as horizontally adja-
cent pairs, one pair at a time.
1137
Fig. 1. Similarity ratings in the facial expression similarity task for
patients E.P. and G.T. (indicated by their initials) for facial ex-
pression pairs in which the expressions depicted di€erent emotions.
Each category shows average similarity ratings of all 54 possible
pairings of expressions (three expressions of the given emotion six
other emotions three expressions of each of these six emotions). All
other data points are from Adolphs et al. [2]. Circles indicate the
performance of each of eight brain-damaged control subjects whose
lesions spared the amygdala. The ®lled triangles indicate the per-
formance of patient S.M., who was tested twice.
2.2.2. Multidimensional scaling analysis
To further explore whether E.P. and G.T. were nor-
mal in their ability to recognize similarity between
facial expressions of emotion, we performed a multidi-
mensional scaling (MDS) analysis of the facial emotion
intensity rating task data for these patients using the
raw data corresponding to the summary statistics pre-
viously reported in Hamann et al. [9]. This task
involves presentation of 39 facial expressions of
emotion (six each of happy, surprised, afraid, angry,
disgusted, or sad emotion plus three neutral faces) nine
times. Each time the set of 39 facial expressions were
presented they were in a di€erent random order and
were paired with a di€erent adjective (the emotional
adjectives happy, surprised, afraid, angry, disgusted,
and sad in addition to the three non-emotional adjec-
tives awake, sleepy, and interested). Subjects rated
each face on a scale of 0±5 (0=not at all; 5=very
much) with respect to each adjective (the same adjec-
tive for each block of 39 faces).
For each subject, rating pro®les for each of the 39
expressions were correlated with one another. This cor-
relation matrix was used to compute non-metric MDS
of dissimilarities in Euclidean 2-space with two algor-
ithms that yielded identical results. Similarity varied
with Euclidean distance as a smooth, nearly linear,
monotonically decreasing function.
1138 S.B. Hamann, R. Adolphs / Neuropsychologia 37 (1999) 1135±1141
Fig. 2. Similarity ratings in the facial expression similarity task for
patients E.P. and G.T. (indicated by their initials) for facial ex-
pression pairs in which the expressions depicted the same emotion.
Each category shows average similarity ratings of all three possible
pairings of the three facial expressions depicting the same emotion.
All other data points are from Adolphs et al. [2]. Circles indicate the
performance of each of eight brain-damaged control subjects whose
lesions spared the amygdala. The ®lled triangles indicate the per-
formance of patient S.M., who was tested twice.
3. Results
3.1. Facial expression similarity task
Fig. 1 shows the results for the facial expression
similarity task for patients E.P. and G.T. for facial ex-
pression pairs in which the two faces depicted di€erent
emotions. Each category shows average similarity rat-
ings of all 54 possible pairings of expressions (three ex-
pressions of the given emotion six other emotions
three expressions of each of these six emotions). The
data for E.P. and G.T. are plotted against the data
from Adolphs et al. [2] obtained using the same task
(data are from two experiments with S.M. and one ex-
periment with eight brain-damaged control subjects).
Unlike control subjects, who perceived a moderate
degree of similarity between faces expressing di€erent
emotions, S.M.'s ratings re¯ected a tendency not to
endorse any emotions other than the protypical or
dominant ones depicted in a facial expression. In con-
trast, patient E.P. clearly exhibited normal perform-
ance on this task, giving similarity ratings in the upper
range of control performance for every emotion cat-
egory. G.T.'s performance was also within the per-
formance range of the control subjects for all facial
expression categories except two, happiness and fear.
G.T.'s similarity ratings for these fell just outside the
range of control performance, and G.T.'s scores were
also well above both of S.M.'s scores in the category
of fear. The one category in which G.T.'s performance
matched S.M.'s (happiness) was the one in which con-
trol subjects tended to give very low similarity ratings.
In summary, G.T.'s overall performance was lower
than that of E.P. and lower than any individual con-
trol subject, but at the same time his performance was
much closer to being completely normal than was
S.M.'s.
Fig. 2 shows the results for the facial expression
similarity task for patients E.P. and G.T. for facial ex-
pression pairs in which the two faces depicted the
same emotion. Each category shows average similarity
ratings of all three possible pairings of the three facial
expressions depicting the same emotion. The data for
E.P. and G.T. are plotted against the data from
Adolphs et al. [2] in the same manner as in Fig. 1.
S.M. was not impaired in the ability to recognize simi-
larity between two faces depicting the same emotion, a
task which requires only the ability to detect the most
prototypical emotion in a facial expression. E.P. and
G.T. showed normal performance on this task.
3.2. Multidimensional scaling analysis
Fig. 3 shows the MDS plots for the average of seven
normal controls (CON), G.T. (GT) and S.M. (SM).
For technical reasons related to the MDS procedure, a
valid MDS plot could not be computed for the data
from E.P. The nearly continuous circular ordering of
emotional faces in the MDS plot for G.T. shows that
he perceived similarity between the emotional faces
normally. For example, in both the CON and GT
plots, surprised and afraid faces were adjacent, indicat-
ing that they were perceived as being relatively similar.
The overall arrangement of emotions in the MDS
plots for CON and GT was also similar to what has
been found in previous studies of judgments of
emotional facial expressions [16] and emotional words
[15]. In contrast, S.M.'s abnormal MDS plot showed
clustering of the emotional faces into three discrete
groups. The gaps in S.M.'s MDS plots corresponded
to the endorsement of very low ratings when judging
expressions of di€erent emotions on each other's adjec-
tives (e.g., how much fear is there in surprised ex-
pressions, and vice versa?), as illustrated quantitatively
in Fig. 1.
4. Discussion
The results from both the facial emotion similarity
task and the multidimensional scaling analysis of the
data from Hamann et al. [9] indicate that both E.P.
and G.T. can recognize similarity between facial ex-
pressions of emotion, despite complete bilateral loss of
the amygdala. For di€erent-emotion face pairs, E.P.
gave similarity ratings that were clearly normal. G.T.'s
similarity ratings were near the lower range of control
performance but were clearly well above those of S.M.
 S.B. Hamann, R. Adolphs / Neuropsychologia 37 (1999) 1135±1141 1139

Fig. 3. Multidimensional scaling (MDS) of perceived similarity judgments of emotions expressed by faces. Each colored point represents one of
the 39 facial expressions which subjects rated. Euclidean distance between points corresponds to perceived dissimilarity between simuli.
CON=normal control subjects (N = 7); GT=patient G.T.; SM=patient S.M.. Data for CON and SM are from Adolphs et al. [2].

In contrast to G.T.'s borderline performance in the
facial comparison task, his MDS plot clearly indicated
normal recognition of similarity between di€erent
facial expressions. Thus, G.T. also appears to be able
to recognize similarity between di€erent facial ex-
pressions normally. Patient S.M.'s facial emotion rec-
ognition de®cits on the same tasks examined here were
attributed to her selective bilateral amygdala lesions
[2]. Because E.P. and G.T. also have complete bilateral
amygdala lesions, the present results indicate that nor-
mal recognition of similarity between di€erent facial
emotions can occur independently of the amygdala.
Combined with the results of a previous study that
found E.P. and G.T. to be normal in recognizing indi-
vidual basic emotions in facial expression [9] the pre-
sent ®ndings indicate that these two patients are intact
on both of the facial recognition abilities that were
found to be impaired in patient S.M. [2].
The question of why only some patients with bilat-
eral amygdala damage exhibit particular facial emotion
recognition de®cits cannot be de®nitively answered
from the current data. However, the hypotheses which
1140 S.B. Hamann, R. Adolphs / Neuropsychologia 37 (1999) 1135±1141
were advanced to answer this question in the context
of facial recognition of speci®c emotions [9] also
appear to be the most plausible explanations for the
current results involving recognition of similarity
between facial expressions of emotion.
The ®rst possibility is that amygdala lesions lead to
facial emotion recognition de®cits when such damage
is sustained during development but not when it is sus-
tained in adulthood. These two patients E.P. and G.T.
di€er from patient S.M. in several respects, but per-
haps the most important of these di€erences is the fact
that E.P. and G.T. both acquired their lesions in adult-
hood, after the age of 50, whereas the disease that
caused S.M.'s lesions was congenital. Abnormal devel-
opment of facial recognition abilities may result in the
agenesis of the ability to recognize similarity between
facial expressions showing di€erent emotions and the
related ability to recognize the presence of multiple
emotions in a single face. Alternately, some subjects
may adopt strategies that allow brain regions other
than the amygdala to mediate these facial recognition
abilities. Adolphs et al. [1] identi®ed speci®c cortical
areas in the right hemisphere which participate in
facial emotion recognition. Conceivably, after damage
to the amygdala some subjects may continue to be
able to recognize facial emotion using these intact cor-
tical areas. Finally, other between-subject di€erences in
IQ and other neuropsychological characteristics cannot
be de®nitively excluded as possible contributing fac-
tors. For example, both E.P. and G.T. had higher IQ
scores (102 and 92, respectively) than S.M. (86) which
may have facilitated their use of alternative facial
emotion recognition strategies (Wechsler Adult
Intelligence Scale-Revised Full Scale IQ) [19].
Recently, other cases of bilateral amygdala damage
have been reported which do not appear to support
either the developmental hypothesis or the hypothesis
involving between-subject di€erences in neuropsycho-
logical characteristics [5,6]. These cases involve patients
who sustained bilateral amygdala damage in adulthood
who have de®cits in recognizing fear and other nega-
tive emotions in facial expressions. Because their
lesions were acquired after a normal course of cogni-
tive development and their neuropsychological pro®les
(including IQ and other factors) overlap substantially
with those of E.P. and G.T., neither of the hypotheses
involving these factors appear to be able to accommo-
date these data.
Importantly, however, these new cases with bilateral
amygdala damage [5,6] were not assessed on the ability
to recognize similarity between di€erent emotions.
Therefore, these cases are not directly relevant to the
issue of explaining between-subject di€erences in the
ability to recognize emotional similarity. However,
these cases do suggest that the developmental and neu-
ropsychological factors hypotheses are unlikely to be
satisfactory as general explanations for the di€erences
among amygdala-lesioned patients in both recognizing
individual basic emotions and recognizing emotional
similarity. A potentially important factor in explaining
these between-subject di€erences is the frequent pre-
sence in these cases of varying degrees of brain damage
to areas outside of the amygdala [5,6,9]. Depending on
the speci®c areas a€ected, the e€ects of these ad-
ditional lesions may either interact with the e€ects of
amygdala damage or may independently cause facial
emotion recognition de®cits. Data from additional
selective cases of bilateral amygdala lesions will be
needed to help resolve the issue of why only some
patients with bilateral amygdala damage exhibit par-
ticular facial emotion recognition de®cits.
Because no dissociation was observed between the
ability to recognize individual basic emotions and the
ability to recognize similarity between di€erent
emotions in the current study, the question of whether
the de®cits observed in both of these abilities in S.M.
[2] are separate is still unresolved. Regardless of
whether the de®cits are independent, however, it is im-
portant to note that these two de®cits may interact.
For example, inability to recognize emotions in an ex-
pression other than the most intense or dominant one
might exacerbate a speci®c fear recognition de®cit.
This could occur if the fear recognition de®cit were to
reduce the perceived intensity of fear in fearful facial
expressions such that that fear became less intense
than other emotions that were also present (e.g., sur-
prise). In such a case, recognition of fear might be
entirely prevented because of masking by more domi-
nant emotions.
Although G.T. was normal on the recognition of
facial similarity as assessed by the MDS analysis, he
performed near the lower range of control perform-
ance on the facial similarity recognition task. This dis-
crepancy may be related to di€erences in diculty
between the two tasks. The facial similarity recognition
task would appear to be a more dicult task that
could potentially reveal a more subtle de®cit in facial
emotion recognition than the speci®c basic emotion
recognition task that provided the data for the MDS
analysis. In the facial similarity task, two di€erent ex-
pressions must be compared to judge their relative
similarity with respect to multiple possible emotions.
In contrast, the speci®c facial emotion recognition task
requires subjects to rate the intensity of one emotion
in a single facial expression. It remains possible, there-
fore, that on even more sensitive tests than those used
in the current study patient G.T. might have exhibited
signi®cant impairments in facial emotion recognition.
However, there is no suggestion that this would have
been the case for patient E.P., who was clearly normal
on the putatively more sensitive task.
To our knowledge, with the exception of the current
 S.B. Hamann, R. Adolphs / Neuropsychologia 37 (1999) 1135±1141
study and the previous single case study by Adolphs et
al. [2], no other studies have investigated de®cits in
recognizing similarity between di€erent facial ex-
pressions of emotion. Like the recognition of individ-
ual, basic emotions in a face, the ability to recognize
emotional similarity between facial expressions and the
related ability to recognize multiple emotions of di€er-
ing intensities are important for social interaction.
These de®cits warrant further investigation in other
patients with unilateral and bilateral amygdala lesions,
particularly with regard to the issue of whether such
de®cits can be dissociated from de®cits in the recog-
nition of individual basic emotions in facial ex-
pressions.
In summary, the results of the current study indicate
that normal recognition of similarity between facial ex-
pressions displaying di€erent emotions can take place
independently of the amygdala. These results extend
those of a previous study [9] with these same patients
that demonstrated that the recognition of fear and
other basic emotions in facial expressions of emotion
does not have an absolute dependence on the amyg-
dala. Additional data assessing the recognition of simi-
larity between facial expressions of emotion in other
patients with amygdala damage will help to clarify the
relation between de®cits in this ability and other facial
emotion recognition de®cits and may help explain the
variability in the consequences of amygdala damage
with respect to facial emotion recognition.
Acknowledgements
This research was supported by the James S.
McDonnell Foundation (Grant No. 97-24) and the
Emory University Research Committee (to S.H.) and
an NIMH FIRST award and a Sloan Research
Fellowship (to R.A.).
Appendix
Facial emotion stimuli used in facial expression simi-
larity task. Codes refer to identi®ers in the Ekman [7]
set. Happy: JB1-9, MF1-6, A1-6; Surprised: A1-24,
GS1-16, SW1-16; Afraid: JJ5-13, PE3-21, PF2-30;
Angry: NR2-7, MO2-11, MF2-7; Disgusted: MO2-18,
JB1-16, EM4-17; Sad: NR2-15, JM3-11, EM4-24;
Neutral: EM2-4, PE2-4, JB1-3.
References
[1] Adolphs R, Damasio H, Tranel D, Damasio AR. Cortical sys-
tems for the recognition of emotion in facial expressions.
Journal of Neuroscience 1996;16:7678±87.
1141
[2] Adolphs R, Tranel D, Damasio H, Damasio A. Impaired recog-
nition of emotion in facial expressions following bilateral
damage to the human amygdala. Nature 1994;372:669±72.
[3] Adolphs R, Tranel D, Hamann S, Young A, Calder A, Phelps
E, Anderson A, Lee GP, Damasio AR. Recognition of facial
emotion in nine individuals with bilateral amygdala damage.
Neuro-psychologia 1999;37:1111±7.
[4] Breiter HC, Etco€ NL, Whalen PJ, Kennedy WA, Rauch SL,
Buckner RL, Strauss MM, Hyman SE, Rosen BR. Response
and habituation of the human amygdala during visual proces-
sing of facial expression. Neuron 1996;17:875±87.
[5] Broks P, Young AW, Maratos EJ, Co€ey PJ, Calder AJ, Isaac
CL, Mayes AR, Hodges JR, Montaldi D, Cezayirli E. Face pro-
cessing impairments after encephalitis: amygdala damage and
recognition of fear. Neuropsychologia 1998;36:59±70.
[6] Calder Andrew J, Young Andrew W, Rowland Duncan, Perrett
David I, Hodges JR, Etco€ NL. Facial emotion recognition
after bilateral amygdala damage: Di€erentially severe impair-
ment of fear. Cognitive Neuropsychology 1996;13:699±745.
[7] Ekman P. Pictures of facial a€ect. (Photographic slides). Palo
Alto, CA: Consulting Psychologists 1976.
[8] Hamann SB, Cahill L, Squire LR. Emotional perception and
memory in amnesia. Neuropsychology 1997;11:104±13.
[9] Hamann SB, Stefanacci L, Squire LR, Adolphs R, Tranel D,
Damasio H, Damasio A. Recognizing facial emotion. Nature
1996;379:497.
[10] Hamann SB, Squire LR. Perceptual memory in the absence of
conscious memory. Behavioral Neuroscience 1997;111:850±4.
[11] Kaplan E, Goodglass H, Weintraub S. Boston Naming Test
(manual). Philadelphia: Lea & Febiger, 1983.
[12] Morris JS, Friston KJ, Buchel C, Frith CD, Young AW, Calder
AJ, Dolan RJ. A neuromodulatory role for the human amyg-
dala in processing emotional facial expressions. Brain
1998;121:47±57.
[13] Morris JS, Frith CD, Perrett DI, Rowland D, Young AW,
Calder AJ, Dolan RJ. A di€erential neural response in the
human amygdala to fearful and happy facial expressions.
Nature 1996;383:812±5.
[14] Reed MJ, Hamann SB, Stefanacci L, Squire LR. When amnesic
patients perform well on recognition memory tests. Behavioral
Neuroscience 1997;111:1163±70.
[15] Russell JA. A circumplex model of a€ect. Journal of
Personality & Social Psychology 1980;39:1161±78.
[16] Russell JA, Bullock M. Multidimensional scaling of emotional
facial expressions: Similarity from preschoolers to adults.
Journal of Personality & Social Psychology 1985;48:1290±8.
[17] Russell JA, Bullock M. Relativity in the perception of emotion
in facial expressions. Journal of Experimental Psychology
1986;116:223±37.
[18] Squire LR, Knowlton BJ. Learning about categories in the
absence of memory. Proceedings of the National Academy of
Sciences of the United States of America 1995;92:12,470±,474.
[19] Wechsler D. Wechsler Adult Intelligence ScaleÐRevised (man-
ual). New York: Psychological Corporation, 1981.
[20] Wechsler D. Wechsler Memory ScaleÐRevised (manual). New
York: Psychological Corporation, 1987.
[21] Whalen PJ, Rauch SL, Etco€ NL, McInerney SC, Lee MB,
Jenike MA. Masked presentations of emotional facial ex-
pressions modulate amygdala activity without explicit knowl-
edge. Journal of Neuroscience 1998;18:411±8.
[22] Young AW, Aggleton JP, Hellawell DJ, Johnson M, Broks P,
Hanley JR. Face processing impairments after amygdalotomy.
Brain 1985;118:15±24.
[23] Young AW, Hellawell DJ, Van de Wal C, Johnson M. Facial
expression processing after amygdalotomy. Neuropsychologia
1996;34:31±9.