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Recognition of emotion from facial expression following traumatic brain injury

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DOI: 10.1080/02699050500110033 · Source: PubMed

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Brain Injury, September 2005; 19(10): 787–799

ORIGINAL PAPER

Recognition of emotion from facial expression following

traumatic brain injury

V. CROKER & S. MCDONALD

University of New South Wales, Sydney, Australia

(Received 20 May 2004; accepted 15 February 2005)

Abstract
Primary Objective: To assess three domains of emotion recognition in people with traumatic brain injury (TBI).
Research design: A between group comparison.
Procedures: Twenty-four participants with severe TBI and 15 matched participants without brain damage were asked to label
and match facial expressions with and without context. The participants with TBI were also interviewed regarding changes in
subjective experience of emotion.
Main outcomes and results: Participants with TBI were found to be significantly impaired on expression labelling and match-
ing, but experienced some improvement when provided with context. Negative emotions were particularly affected. Affective
semantic knowledge and face perception appeared to be relatively intact in this group. The majority of participants with
TBI reported some change in the post-injury experience of everyday emotion, although the pattern of changes differed
greatly between individuals. Reduced subjective experience, especially of sadness and fear, was associated with poor emotion
matching but not emotion labelling.

Keywords: Traumatic brain injury, emotion recognition, perception, affect, facial expression

Introduction may contribute to difficulties in regulating, moni-

Severe traumatic brain injury (TBI) results in a range
of neuropsychological deficits that lead to diminished
psychosocial functioning. A great deal of research
has been undertaken to examine the cognitive and
behavioural sequelae of TBI, as well as the outcomes
for this population. What is relatively less well
understood, however, is how TBI impacts upon
emotional processing.
Changes in the social and emotional behaviour of
an individual following TBI have long been noted.
More recently, these changes have been hypothesized
to influence post-injury social skills that, in turn,
have emerged as one of the major barriers to success-
ful reintegration into family, community and work
environments post-injury [1–3]. Changes in social
behaviour following TBI include self-focused speech,
insensitivity, inappropriate intimacy and disclosure
and talking out of turn [4–6]. Executive dysfunction
toring and inhibiting behaviour. However, the possi-
bility that social skill difficulties commence at the
level of affective processing has also been raised
[7–9]. This is supported by a growing body of evi-
dence to suggest that individuals with TBI are poor
at recognizing emotion conveyed by both speech
and facial expression [7–14].
TBI is typically the outcome of motor vehicle acci-
dents, sporting accidents or falls [15]. These insults
usually result in diffuse brain damage, although the
ventrolateral frontal lobes, inferior orbital cortices
and temporal lobes are noted to be particularly
vulnerable to injury. Damage to these areas can
result from direct impact to the frontal areas or
from impact to other parts of the skull that, in turn,
causes the brain to rebound off the bony protu-
berances of the anterior and middle fossae. It is of
particular note that research with primates has
identified specialized neurons in the temporal visual

Correspondence: Skye McDonald, PhD, School of Psychology, University of New South Wales, Sydney, 2052, Australia. Tel.: (61) þ 2 9385 3029. E-mail:
s.mcdonald@unsw.edu.au
ISSN 0269–9052 print/ISSN 1362–301X online # 2005 Taylor & Francis Group Ltd
DOI: 10.1080/02699050500110033
788 V. Croker & S. McDonald
cortex for processing facial expression [16] and a
direct projection from this region to the orbitofrontal
cortex [17]. Furthermore, neuroimaging studies
with healthy controls have demonstrated that areas
such as the right inferior occipitotemporal regions
[18, 19], the right and left temporal cortex, the amyg-
dala [18–20], the left inferior frontal cortices [19, 21]
and the right anterior cingulated gyrus region are
critically involved in processing facial affect [19].
Similarly, studies of people with focal cerebral lesions
[22–26] have implicated regions within the bilateral
frontal cortices, temporal lobes, insular and amygda-
lae as associated with loss of facial affect recognition.
As these regions are often damaged in TBI, deficits in
processing facial affect may be anticipated.
Indeed, an increasing number of studies have
reported pervasive deficits in emotion recognition
following TBI affecting recognition of emotional
expressions in static stimuli [7, 9, 10, 13], taped
speech [7, 9, 12] and naturalistic videotaped
portrayals [8, 11, 27]. Performances on tests of
(affectively neutral) face and voice quality recogni-
tion have been found to be either normal [7], or, if
impaired, unrelated to emotion [9]. Thus, problems
processing affect cannot simply be attributed to
visual or auditory perceptual impairments. In addi-
tion, Hornak et al. [7] raised the possibility that
emotion recognition deficits may extend to the
subjective experience of emotion. Working with a
group of people with brain injuries from a range of
aetiologies, they obtained self-reports of participants’
ability to experience various emotions since sustain-
ing brain injury (sadness, enjoyment, anger, fear
and disgust) and found that several of the partici-
pants with TBI reported blunted affect, particularly
for negative emotions such as sadness. For example,
one participant with a TBI reported, ‘I have no
feelings . . . I can’t tell if I have emotions — I can’t
tell if I’m saddened . . . I don’t get really sad’ (Case
10, p. 261). Total alteration in subjective emotional
experience also correlated significantly with emotion
recognition performance. On the basis of these
results, it was speculated that the observed deficits
in emotion recognition performance might have
been part of a ‘wider emotional disturbance’ [7].
The ability to read the emotional state of others
is likely to depend on the integrity of at least three
processing systems [28]. The first is geared towards
perceiving and decoding non-verbal signs of emo-
tion. Indeed, there is clear evidence to suggest that
the ability to recognize emotion from faces and the
ability to recognize faces per se are dissociable [7,
10, 29–32]. The second system is a semantic
system that contains knowledge of the situational
determinants of emotions. This contextual informa-
tion can often be used by an observer to disambigu-
ate another’s emotional experience [33], e.g. if one
understands that loss can lead to sadness, one may
be better able to detect sadness in someone if aware
that they have experienced loss. The extent to which
people with TBI can use context to inform emotional
judgements requires investigation. In the only study
to date to examine this, Milders et al. [9] asked
people with TBI to match verbal labels to pictorial
situations implying a range of different emotions.
Their participants were poor relative to controls.
These findings suggest that emotion-processing
deficits do extend into the semantic system.
However, the use of pictorial material can tap into
broader visuoperceptual difficulties rather than
semantic judgements per se. Thus, the extent to
which people with TBI are able to utilize semantic
knowledge of emotions to ameliorate deficits in
emotion recognition remains unclear.
The third system of potential importance is one
that enables one to subjectively experience emotions.
Some researchers have suggested that capacity
for empathy may be closely linked to the ability to
recognize emotion in others [34–36]. For example,
McHugo and Smith [34] found that exposure to dis-
plays of facial affect produced spontaneous changes
in observers’ skin conductance and facial muscula-
ture, approximating the expression of the subject.
These findings suggest a direct link between the
recognition and experience of emotion that is adap-
tive, enabling one to rapidly identify the emotional
state of the target without the need for conscious
processing [35]. Furthermore, lesions to the amygda-
lae and frontal cortices have been specifically asso-
ciated with a reduction in autonomic responding
to negative facial expressions and other affective
stimuli [26, 37]. A similar finding has been reported
in a sample of 15 people with TBI [38], although
a relationship between reduced responsivity and
impaired identification of facial emotion was not
found, possibly due to the relatively small sample
size in this study.
With some valuable exceptions [9, 38], studies
investigating emotional processing in TBI, to date,
have primarily focused on emotion recognition. No
one study has examined deficits in perception,
semantic knowledge and subjective experience in
a single TBI sample. It, therefore, remains to be
seen whether the observed deficits are specific to the
perceptual recognition of emotion or whether they
extend into semantic understanding of the situational
determinants of emotional responses and to the
subjective experience of emotion. The possibility
that TBI leads to differential difficulties with some
emotions relative to others also requires examination.
There is some evidence to suggest that, despite het-
erogeneous neuropathology in the TBI population,
impairments in emotion recognition are greater
for negative emotions such as sadness, fear and

disgust, than for positive emotions such as happiness
[10, 27, 38].
The purpose of the present investigation was to
assess performance across three domains of emotion
recognition: recognition of facial affect, semantic
knowledge for emotional states and situations and
subjective emotional experience. The authors chose
to restrict attention to recognition of emotion in
the visual modality, as facial expression is thought
to be the most powerful non-verbal conveyor of
emotion [39–41].
On the basis of existing literature on TBI and
other brain-damaged populations, several predic-
tions for the outcome of this research were proposed.
First, it was expected that individuals with TBI
would be significantly impaired when asked to iden-
tify the emotional expression of a target, replicating
the findings of previous studies [7, 9, 10, 13, 14,
27]. On the basis of previous findings [10, 13, 27]
the possibility that the participants with TBI might
evidence a greater impairment for recognition of
negative emotions, specifically fear, sadness and
disgust, compared to others was also considered.
Secondly, this study examined the capacity for
individuals with TBI to use contextual information
in making inferences about the emotional state of
another person. In an extension of previous work in
this field [9], contextual information was provided
to participants with TBI in the verbal modality,
thus bypassing any problems processing ambiguities
in pictorial material. This study examined not only
whether individuals with TBI have access to seman-
tic knowledge of affective states, but also whether
they can use this contextual information to aid
emotion recognition accuracy.
The final prediction for this investigation was that
there would be an alteration in the post-injury experi-
ence of everyday emotions for participants with TBI.
There has been no research to date on the subjective
experience of emotion in a pure TBI sample, although
the data from Hornak et al.’s [7] mixed sample study
is certainly suggestive. Their results also indicated
that those with the greatest alteration in subjective
emotional experience tended to evidence poorer
emotion recognition accuracy. Given that emotion
recognition is associated with empathic reactions in
the normal literature, the more specific prediction
was made that subjective reports of a reduction in
emotional responsivity in people with TBI would be
associated with poor emotion recognition in others.
Method
Participants
Thirty-one participants who had sustained severe
TBI were recruited from three major metropolitan
Recognition of emotion following TBI 789
brain injury units in Sydney, Australia. These referral
sites were requested to recommend participants
with TBI to the study who had no known primary
sensory deficits, aphasia, agnosia, psychosis, immedi-
ate memory difficulties or difficulties with face
recognition that would otherwise preclude participa-
tion. Participants who were known to have some
existing difficulty with socioemotional functioning,
i.e. poor social skills (through self- or staff-reports)
were particularly sought. Six participants demon-
strating abnormally poor performance on a test of
face perception were excluded from the study
according to selection criteria and data from another
participant was excluded due to non-compliance
with the testing.
The 24 participants remaining included 17 men
and seven women of average age 37.9 years
(SD ¼ 12.6). The mean post-injury period was 8
years (SD ¼ 8) and average duration of post-
traumatic amnesia (PTA) was 83 days (SD ¼ 43).
All participants were documented to be in PTA for
longer than 24 hours (range ¼ 7–151 days), placing
them in the severe range for TBI. As is typical of
this population, there was significant heterogeneity
in the types of injury sustained. The majority of
injuries were sustained in motor vehicle accidents,
although some were caused by falls, assaults and
sporting or work-related injuries. Pathology on
examination was available for 21 of the 24 partici-
pants and revealed skull factures (4), contusions
(10), subdural, subarachnoid and intra-cerebral
haemmorhages (13) and penetrating injuries (2). In
nine cases, there was documented frontal pathology.
Six participants had initial damage localized to the
right hemisphere, while five had damage reported
in the left hemisphere and a further 10 had report-
edly bilateral damage. These initial reports of the
damage sustained are only a gross indication of the
site and extent of neuropathology with many micro-
scopic lesions and neuronal shearing undetectable
using the available clinical tools. None-the-less they
provide an indication of the variability of damage
typical in this group as well as the significant pres-
ence of frontal pathology. On average, the partici-
pants with TBI had achieved 12 years of education
(ranging from 8–18 years). All had been employed
prior to their injuries in occupations ranging from
unskilled (4) to skilled trade or clerical (15), profes-
sional or managerial (3) or student (2). After their
injuries, the group experienced a significant drop in
employment status with only two people in employ-
ment and the remaining 22 either unemployed or
working in a voluntary capacity. Estimates of pre-
morbid intelligence were available for 20 of the 24
participants with TBI and all were estimated to be
of at least average pre-morbid intelligence, with the
790 V. Croker & S. McDonald
exception of two who were known to be in the low
average range pre-morbidly.
Fifteen control participants (10 men and five
women) without neurological history and matched
for age, sex, education and occupation of the TBI
group also participated in this study. Participants
were drawn from the community and participated
on a voluntary basis. The control group had a
mean age of 43.7 (SD ¼ 11.2), had achieved 12.5
years of education (SD ¼ 2.0) and were all employed
in a range of unskilled, skilled and professional occu-
pations. Both groups were comparable for age, sex,
education and pre-morbid occupation. The TBI
group, however, had a significantly greater propor-
tion of participants who were currently unemployed
(2 ¼ 34.93, df ¼ 5, p < 0.0000) relative to the control
group.
Materials
All participants were presented with one task of
visual discrimination and face perception and four
tasks of emotion recognition. There were two tasks
assessing perceptual recognition of emotion, one task
examining semantic knowledge of emotions given
contextual information only and a final task assessing
perceptual recognition of facial expressions given
contextual information. Participants with TBI were
additionally interviewed regarding perceived post-
injury changes in the intensity or frequency of
emotions, based on the brief interview previously
reported by Hornak et al. [7].
Test of face recognition and visual discrimination
The short form of the Benton Facial Recognition
Test BFRT [42] was used to assess participants for
accuracy in face recognition and fine discrimination
of black and white photographs. In this task, parti-
cipants were required to identify a target individual
from a set of six photographs. Early items of the
BFRT involved matching identical front-view photo-
graphs and later items involved matching front-view
with either three-quarter view photographs or front-
view photographs under different lighting conditions.
Emotion recognition tasks
All photographs of facial expression featured in the
emotion recognition tasks were taken from the
Ekman and Freisen [43] Pictures of Facial Affect
series. Photographs were printed in black and white
and were selected on the basis of reliability data [43].
The six emotions represented in the series were
happiness, sadness, anger, fear, surprise and disgust.
A neutral category was included in the context-free
labelling task according to convention, but was
excluded from subsequent tasks where the goal was
to assess participants’ ability to discriminate between
distinct emotions. In accordance with prior research
in the field of affect recognition, sadness, anger, fear
and disgust were considered to be ‘negative’ expres-
sions and happiness and surprise wee regarded as
‘positive’ expressions.
Expression labelling (context-free). In this task,
participants were required to match each photo-
graph of facial expression to a printed verbal label.
Photographs were shown one at a time, with four
exemplars of each expression presented in random
order across a total of 28 trials. Half of the photo-
graphs featured male subjects and half featured
female subjects. After examining each photograph,
participants were asked to choose a verbal descriptor
for the expression, from a list of seven corresponding
to the emotions represented in the series (the options
were read aloud by the experimenter where parti-
cipants had reading difficulties). List order was
randomized for each participant.
Matching expressions (context-free). Participants were
also presented with a matching task which bypassed
the need to produce verbal labels. Photographs used
in the matching task were different to those used
in the earlier labelling task, to minimize carry-over
effects. In order to prevent confusion, participants
were asked to choose the correct emotion from
an array limited to four alternative photographs.
The four alternatives comprised the correct emotion
plus three foils reflecting one similarly valenced
emotion (positive or negative) and two of the
opposite valence. All four photographs were shown
below the target. Four exemplars of each of the six
expressions were presented in random order, i.e. 24
trials with half of the presentations featuring
male subjects and the others female subjects. All
photographs in a given presentation featured subjects
matched for sex but of different identity in order to
prevent participants matching on the basis of physical
attributes.
Semantic knowledge of emotions. Participants were
presented with 18 verbal scenarios (three exemplars
in random order for each of the six emotions) and
were asked to report how a person would typically
feel if that event occurred, e.g. ‘How might a person
feel if they were being chased by a large vicious dog?’
Participants were then asked to choose the most
appropriate emotion from a list of four verbal labels.
As with the matching tasks these comprised the
target emotion, a foil of the same valence and two
foils of the opposite valence.

Matching facial expressions to context and context-
provided expression labelling. In this task participants
were presented with 24 scenarios, one at a time and
were asked to select a facial expression appropriate
for the subject of the story. For example, ‘Susan is
celebrating with a friend after winning a holiday in a
competition. . . Choose the facial expression that best
matches the way Susan would be feeling’. As with the
previous two tasks, four choices were presented: the
target emotion, a foil of the same valence and two
foils of the opposite valence. The photographs in this
task had been presented earlier for the context-free
labelling task, to aid direct comparison between the
two task formats.
Participants were then asked to look at the face
they selected and to choose an appropriate label for
the expression from a written list of seven choices,
as for the earlier context-free labelling task. Thus,
scores on the context-provided labelling task could
be compared directly with scores on the context-
free labelling task to examine the effect of context
on accuracy of expression identification.
Interview: self-reported changes in the
experience of emotion
Participants with TBI were interviewed regarding
their ability to experience and perceive each of the six
emotions in daily life. For each emotion, they were
asked to indicate the extent to which their experience
or perception of that emotion had changed
following TBI. As in Hornak et al. [7], participants
were required to indicate subjective change on a
seven-point scale (
1.5 ¼ dramatic decrease,
1.0 ¼
marked decrease,
0.5 ¼ mild decrease, 0 ¼ no
change, 0.5 ¼ mild increase, 1.0 ¼ marked increase,
1.5 ¼ dramatic increase).
Procedure
Participants were presented with the context-free
expression-labelling task first, followed by the
expression-matching task. The BRFT test of face
perception was then administered, followed by the
semantic knowledge task and finally the matching
expression-to-context task. The interview for TBI
patients was typically conducted at the end of testing.
All tasks (with the exception of the interview) were
presented in a multiple (forced) choice format.
No time limit were imposed, although all partici-
pants were generally able to respond to each item
within 10–40 seconds. The examiner prompted par-
ticipants to choose the most appropriate response
when they appeared hesitant or ambivalent about
their answer. No feedback on performance accuracy
was given during testing.
Recognition of emotion following TBI 791
Results
Group differences in performance accuracy
All raw scores were converted into percentage
accuracy scores. Independent group t-tests (two-
tailed) were performed on total scores from the test
of face perception and each of the emotion recogni-
tion tasks. Alpha was set at 0.01 for each comparison
to adjust for inflation of the Type 1 error rate
associated with multiple comparisons (Bonferroni
procedure).
BFRT: Test of face recognition and visual
discrimination. While participants in the control
group generally achieved higher accuracy scores on
this test than participants in the TBI group (t ¼ 3.01,
df ¼ 37, p ¼ 0.005), both groups scored within the
average range for this measure [42]. Both groups
performed better for the easier BFT items where the
target and choice faces were matched for perspective
and lighting than for harder items where the target
and choice faces differed in terms of these charac-
teristics, F(1, 37) ¼ 91.30, p < 0.0001. There was no
significant interaction between item type (easy vs
hard) and group (F(1, 37) ¼ 3.65, p ¼ 0.066).
Performance on the BFRT did not correlate with
performance on any of the perceptual emotion recog-
nition tasks for either group, suggesting that emotion
recognition performance was dissociable from face
perception in this sample.
Emotion recognition tasks. Figure 1 shows perfor-
mance accuracy across each of the emotion recogni-
tion tasks by group.
Table I shows the distribution of participants
with TBI across percentile ranks, relative to the
performance of participants in the control group.
Clinically significant impairment is defined as a
level of performance at or below the 5th percentile
for the control group.
Labelling expressions and matching expressions in
a context-free task format
Compared to the control group, participants in the
TBI group were relatively less accurate in labelling
emotions shown in facial expression (t ¼ 8.66,
df ¼ 36.96, p < 0.001, equal variance not assumed)
and in matching like facial expressions (t ¼ 3.93,
df ¼ 31.1, p < 0.001, equal variance not assumed).
Performance on the labelling task did not correlate
significantly with performance on the matching task
for either the TBI group (r ¼ 0.16, n ¼ 24, p ¼ 0.453)
or the control group (r ¼ 0.37, n ¼ 15, p ¼ 0.180).
While this is not surprising for the control group
given the small amount of variance in their perfor-
mance on these tasks overall, it was of significance
792 V. Croker & S. McDonald
Figure 1. Performance accuracy for each emotion recognition task by group with TBI compared to group with no brain
damage (NBD).
Table I. Percentile ranks for participants with TBI relative to the group with no brain damage for each emotion recognition task: number of
participants in each percentile category.
Context-free expression Expression
%ile labelling task matching task
>50th 0 1
25–50th 1 0
10–25th 0 11
5–10th 1 3
<5th 22 9 4
that no correlation was found within the TBI group
despite the variability of their performances and
suggests that these two tasks measured largely
independent aspects of performance.
Semantic knowledge of emotions and matching
expressions to contextual information
On the test of semantic knowledge for emotions,
both groups performed with a high level of accuracy
with no significant difference between groups
(t ¼ 0.324, df ¼ 37, p ¼ 0.748). Thus, participants in
both groups demonstrated good understanding of
the affective labels presented in this study and the
situations to which they typically apply.
When required to match facial expressions with an
appropriate context, the TBI group again performed
less accurately relative to the control group (t ¼ 4.15,
df ¼ 32.27, p < 0.001, equal variances not assumed).
A post-hoc exploratory analysis indicated that
participants in the TBI group chose labels that
corresponded more closely with the contextual infor-
mation than the facial expressions they actually
Semantic Expression matching Context-provided expression
knowledge task to context task labelling task
15 4 5
5 3 10
0 9 0
0 0 5
8 4
selected, whereas the control group demonstrated
near perfect correspondence between the face
chosen and the label assigned (F(1, 37) ¼ 5.29,
p ¼ 0.027). This pattern of results suggests that
participants in the TBI group were relying more
heavily on contextual information to choose labels
for expressions than the information contained in
the facial expressions themselves.
The influence of contextual information on emotion
recognition performance. To compare the effect of
contextual information on labelling facial expres-
sions, performance on the earlier context-free expres-
sion labelling task was contrasted with performance
on the context-provided expression labelling task.
Both groups demonstrated a significant improvement
in labelling accuracy when contextual informa-
tion was provided compared to the context-free con-
dition (F(1, 37) ¼ 79.93, p < 0.001). The degree of
improvement when moving from a context-free con-
dition to a context-provided condition was greater for
the TBI group (F(1, 37) ¼ 21.1, p < 0.001), although
the control group performed better overall.
 Recognition of emotion following TBI 793

Table II. Group means (and standard deviations) for emotion recognition tasks by emotion.

Happy Surprised Angry Sad Fear Disgust

Labelling TBI X (SD) 3.96 (0.20) 3.29 (1.04) 3.0 (1.02) 2.21 (1.02) 1.63 (1.24) 2.33 (1.05)
NBD X (SD) 4.00 (0.00) 3.80 (0.40) 3.47 (0.52) 3.53 (0.52) 3.0 (0.76) 3.67 (0.62)
Matching TBI X (SD) 3.88 (0.45) 3.75 (0.53) 3.00 (1.18) 2.83 (0.92) 2.79 (0.78) 3.21 (0.93)
NBD X (SD) 4.00 (0) 4.00 (0) 3.87 (0.35) 3.73 (0.59) 3.47 (0.64) 3.87 (0.35)
Semantic TBI X (SD) 3.00 (0) 3.00 (0) 2.93 (0.27) 2.64 (0.5) 3.0 (0) 2.8 (0.43)
NBD X (SD) 3.00 (0) 3.00 (0) 3.00 (0) 2.8 (0.41) 2.87 (0.35) 2.93 (0.26)
Context matching TBI X (SD) 3.96 (0.2) 3.04 (1.3) 3.29 (0.86) 3.63 (0.65) 3.00 (0.98) 3.33 (0.76)
NBD X (SD) 4.0 (0) 3.87 (0.35) 3.73 (0.46) 4.00 (0) 3.87 (0.35) 3.47 (0.64)
Context labelling TBI X (SD) 3.92 (0.41) 3.71 (0.62) 3.83 (0.38) 3.63 (0.58) 3.33 (1.09) 3.67 (0.48)
NBD X (SD) 3.93 (0.26) 4.00 (0) 3.93 (0.26) 4.00 (0) 3.8 (0.56) 3.6 (0.63)

TBI ¼ Participants with traumatic brain injury; NBD ¼ Participants with no brain damage.

Performance accuracy for different emotions.
Inspection of the data for tests of perceptual emotion
recognition suggested poorer accuracy in perfor-
mance for some emotions compared to others. Mean
accuracy scores and standard deviations for task by
emotion and group are presented in Table II.
In general, it appeared that positive emotions
(i.e. happiness and surprise) were better recognized
than negative emotions (anger, sadness, fear and
disgust). To test this observation, a 2 (group: TBI
vs control) by 2 (valence: positive vs negative)
mixed ANOVA was conducted for each of the
perceptual emotion recognition tasks.
Context-free expression labelling. The results indi-
cated that both groups were more accurate in
identifying positive emotional expressions than
negative emotional expressions in the context-free
condition (F(1, 37) ¼ 53.95, p < 0.0001) although
there was a greater discrepancy between accuracy
for negative expressions and positive expressions
for the TBI group than for the control group
(F(1, 37) ¼ 11.81, p ¼ 0.001). In order to identify
the specific emotions contributing to these effects,
t-tests were conducted on the means for individual
emotions within each valence category, controlling
the -level for family-wise error rate in line with
the Bonferroni procedure. The TBI group was no
different to the control group when labelling either
surprise or happiness. Within the negative expres-
sions the participants with TBI were no worse than
controls at judging anger but were poorer on each of
the remaining three negative emotions (sad: t ¼ 4.65,
df ¼ 37, p < 0.001; fear: t ¼ 4.292, df ¼ 37, p < 0.001;
disgust: t ¼ 4.45, df ¼ 36.92; p < 0.001).
Expression matching. Again, participants in both
groups were found to be more accurate in matching
facial expressions for positive emotions than for
negative emotions (F(1, 28) ¼ 64.3, p < 0.001); how-
ever, participants in the TBI group evidenced a
greater drop in accuracy rate for negative emotions
relative to positive emotions than the control group
(F(1, 37) ¼ 17.67, p < 0.001). Once again, within
positive emotions there was no difference between
groups when matching either happiness or surprise.
Within the negative emotions participants with
TBI were poorer than controls on all expressions
(sad: t ¼ 3.38, df ¼ 37, p ¼ 0.002; angry: t ¼ 3.37,
df ¼ 29.05, p ¼ 0.002; fear: t ¼ 2.81, df ¼ 37,
p ¼ 0.008; disgust: t ¼ 31.96, p ¼ 0.004).
Matching expressions to context. Participants in both
the control and TBI group evidenced greater
accuracy for judgements of positive expressions
than for negative expressions (F(1, 37) ¼ 4.46,
p ¼ 0.042); however, there was no significant
interaction with group membership. The participants
with TBI were poorer on surprised (t ¼ 2.94,
df ¼ 28.06, p ¼ 0.007), sad (t ¼ 2.84, df ¼ 23,
p ¼ 0.009) and fearful faces (t ¼ 3.95, df ¼ 31.31,
p < 0.001). They were the same as controls on the
remainder.
Labelling expressions in context. All participants
found the positive expressions easier to label in
context than the negative (F(1, 37) ¼ 8.14, p ¼ 0.007)
and there was no interaction. Participants with TBI
were similar to controls on all but the sad expressions
(t ¼ 3.19, df ¼ 23.0, p ¼ 0.004).
TBI performance across different emotion
recognition tasks
Post-hoc Sheffe contrasts were specified using the
Psy2000 program for Windows V2.0 (School of
Psychology, UNSW, 2000). The results indicated
that participants in the TBI group performed
significantly worse on the context-free expression
labelling task than for any other emotion recognition
task (F(1, 23) ¼ 83.44, p < 0.001), but that both
emotion labelling and emoting matching out of
794 V. Croker & S. McDonald

context were the two most poorly performed tasks
(F(1, 23) ¼ 81.4, p ¼ 0.000). As noted earlier, the
accuracy of emotion labelling improved significantly
when the task format included contextual informa-
tion (F(1, 23) ¼ 81.4, p ¼ 0.000). The task performed
with the greatest accuracy was the semantic knowl-
edge task, representing a particular strength for this
group relative to performance on the other emotion
recognition tasks (F(1, 23) ¼ 95.10, p ¼ 0.000).
This pattern of results for the TBI group suggests
a particular impairment in the spontaneous recogni-
tion and discrimination of emotion in facial expres-
sions, the impact of which was reduced by the
provision of contextual information.
Despite these group trends, some participants
evidenced contrary patterns of performance. For
example, two participants performed better on the
context-free expression labelling task relative to the
expression matching task and failed to demonstrate
improved accuracy in expression labelling in the
context-provided condition. Conversely, five parti-
cipants who performed relatively poorly on the
context-free labelling task benefited dramatically
from the provision of contextual information in
later tasks, performing at the level of the control
group.
Self-reported emotional change and performance accuracy
within the TBI group. The absolute mean change
score for the TBI group corresponded to mild-to-
moderate change in perceived post-injury experience
of emotions (M ¼ 0.68, SD ¼ 0.40: maximum possi-
ble change score ¼ 1.5. Following the hypothesis
that a reduction in subjective emotional experience
may be associated with reduced emotion recognition,
the actual mean change score was correlated to
emotion labelling (context free) and emotion match-
ing (context free) accuracy, i.e. a negative score
reflected a reduction in emotional experience. Scores
on the two emotion identification tasks were
expressed as Z-scores based on the control group’s
mean and standard deviation (see Table III for
individual values). There was no association between
emotion labelling and subjective experience. In
contrast, the association between emotion matching
and mean change scores was significant, i.e. those
who reported an overall decrease in subjective
emotion were also those who were poorest at

Table III. Self-reported emotional change scores for the group with TBI.

Happy Surprise Z-scoresa Z-scores

Case enjoy shock Sad Fear Ange r Disgust Mean change naming matching

1 0b 0 0 0 0 0 0
4.64
5.97
2 0
1.0 1.0 0 1.5 0 0.25
1.99
0.80
3 1.5 0
1.5
1.5
1.5
1.5
0.75
5.96
9.42
4 0.5 0 0 0 0 0 0.08
3.31
2.53
5 0 0 0 0 0 0 0.0
3.97
0.80
6 0 0
1.5
0.5 1.5 0 0.42
5.96
0.80
7 0 0 1.0 1.5 0.5 0 0.5
5.30
0.80
8
0.5 0 1.5 0.5 0 0 0.17
4.64
1.66
9 1.0 0 1.0 0 1.0
1.0 0.33
4.64 0.80
10 0.5 0 1.5 1.0 1.5 0 0.75
5.30 0.92
11 0 0 0 0
1.0 0
0.17
4.64
8.56
12
0.5 0 1.0
0.5 0.5 0 0.08
3.31
4.25
13 0 0 0.5 0
1.5 1.5 0.08
2.65
2.53
14
1.0
1.5 0.5 0
0.5
1.5
0.83
5.96
1.66
15 1.5 0.5
0.5
1.5 1.5
1.5 0
1.99
3.39
16 0.5 0.5
1.0
1.5 1.5
1.5
0.25
3.97
9.42
17
1.0
1.5 1.5 1.0 1.0 1.0 0.33
5.30
4.25
18 1.0
1.5 1.0 1.0 1.0 0.5 0.5
2.65
1.66
19
1.0
1.5 1.5 1.0 1.0 1.5 0.42
1.32 3.39
20
0.5
1.0 1.5 0.5 1.0 1.0 0.5
2.65
4.25
21 1.0 0.5 1.0 1.0 1.5 0 0.83
2.65
2.53
22 0 0 0 0 0 0 0
3.31
0.80
23
1.5 N/A 1.5
1.5 1.5
1.5
0.3
0.66
1.66
24 0.5 N/A
1.0 0.5 0
1.5
0.2
1.99
0.80
% reporting
Any change 67 38 79 63 75 50
Decrease 29 25 17 25 17 29
Increase 34 13 63 38 58 21
a
Z-scores based on the means and standard deviations of the group without brain damage.
b

1.5 ¼ dramatic decrease;
1.0 ¼ marked decrease;
0.5 ¼ mild decrease; 0 ¼ no change; 0.5 ¼ mild increase; 1.0 ¼ marked increase;
1.5 ¼ dramatic increase.

emotion matching relative to controls (r ¼ 0.438,
p ¼ 0.032).
Change scores by valence. Change scores were noted
to be more extreme for some emotions than for
others. A summary of self-reported changes in post-
injury subjective emotional experience are summar-
ized in Table III.
While there was a great deal of within-group varia-
bility for change scores across the different emotions,
changes in some categories were more commonly
reported than others. Changes in the experience of
sadness and anger were the most common (79%
and 75%, respectively), followed by happiness
(67%), fear and disgust (63% and 50%, respectively)
and, lastly, surprise (38%). Increases in emotionality
were commonly reported especially for sadness
(63%) and far (58%) and were generally twice as fre-
quent as decreases. Nevertheless, approximately one
third of the TBI group reported a reduction in the
experience of happiness and disgust while between
17–25% of the group reported decreased emotions
in the other categories. Of the different emotions,
a reduction in the experience of fear and sadness
was associated with poor performance on the
Emotion matching task relative to controls (Fear:
r ¼ 0.457, p ¼ 0.025, Sadness: r ¼ 0.484, p ¼ 0.017).
There was no association with a reduction in the
experience of other emotions.
Discussion
Emotion recognition performance
Consistent with the results of previous investigations,
the participants with TBI in this study were less
accurate than matched controls in their judgements
of facial affect. This effect was demonstrated for each
facial emotion recognition task in the study.
Participants in this study were selected, where
possible, on the basis that they had experienced
some difficulty with post-injury social skills. Thus,
the results of the study may not be generalizable to
TBI populations without this difficulty. The inci-
dence of impaired social functioning following TBI
is, however, high [3, 44], so the findings of this
study may bear relevance for a sizeable proportion
of the TBI population. Furthermore, while people
with social difficulties were sought, the group
reported here are at untypical of the TBI population
more generally. For example, the mean length
of PTA was not significantly difference (one sample
t-test) to the mean PTA duration of 81.2 days
reported in a consecutive series of 100 people with
TBI discharged from a comparable brain injury
unit in an independent study [45]. This indicates
that this group was representative of the severity of
Recognition of emotion following TBI 795
injury typically seen in this population. In addition,
the reduction in employment status post-injury of
the sample, while dramatic, is typical of this group
[45–48].
The TBI group appeared to have specific difficulty
with facial affect recognition that was not attributable
to group differences in the ability to perceive faces.
Although there was a statistically significant differ-
ence in BFRT scores between groups, both groups
performed within the average range on this test
according to normative data [42]. The between-
group difference in performance reflected compa-
ratively poorer performance of the TBI group for
those test items requiring perceptual extrapolation
from the target image (e.g. recognizing what the
target person’s face might look like in a three-quarter
view or when lit from underneath), which arguably
taxed participants’ visuoperceptual abilities to a
greater extent than any of the stimuli employed in
the emotion recognition tasks. Indeed, participants
in both groups made a greater proportion of errors
for items involving perspective or lighting change,
but there was no significant interaction effect with
group. Most importantly, however, there was no
correlation between scores on the BFTR and total
accuracy scores on any of the expression recognition
tasks for either group. Thus, despite the less accurate
visuoperceptual performance of the TBI group
relative to the control group (notably where mental
perspective transformations were required), emotion
recognition performance was, nevertheless, indepen-
dent of face perception performance in this sample.
These results concur with those reported elsewhere
[7, 9, 10].
Within-group analyses also suggested a specific
problem with expression recognition for the TBI
group. First, participants with TBI were significantly
poorer at matching and labelling facial expressions
than they were for matching front-view photographs
on the basis of identity. Indeed, none of the partici-
pants with TBI ranked lower than the 8–11th per-
centile for BFRT performance, whereas over half
ranked lower than this on the expression matching
task and almost all ranked lower than this (below
the fifth percentile) for the expression labelling
task. Secondly, facial expressions of particular
emotions (namely happiness and surprise) were
accurately labeled and matched with consistency by
the majority of participants in the TBI group. If a
general visuoperceptual deficit for faces existed,
one would expect to see impaired performance for
basic BFRT items as well as impaired expression
recognition performance for all emotions depicted,
not just for a select few.
These results are consistent with a modular frame-
work of face recognition such as advocated by Bruce
and Young [49]. According to the model, expression
796 V. Croker & S. McDonald
and identity are analysed in divergent processing
pathways following a common stage of basic
structural encoding. It is, therefore, possible for
recognition performance to be impaired for one of
these functions and not the other [24, 26, 27].
Given that there is heterogeneity in the localization
and severity of damage between individuals with
TBI, it is possible that individuals may demonstrate
a range of disorders reflecting disruption at different
points of this system. The participants in this study
were relatively normal on face recognition per se
but abnormally poor when recognizing expression,
supporting the notion of divergence between the
processing of affect vs identity. In addition, the
results suggested that, while the people with TBI
were impaired in their ability to both name and
match emotions within categories, these two abilities
were not associated. This would imply that these two
tasks rely, to some extent, upon separate cognitive
processes and suggest that further fractionation of
the emotion recognition system is warranted.
The effect of valence: positive vs negative emotions
Participants in both groups were more accurate in
labelling and discriminating between expressions of
positive emotions than negative emotions, suggesting
that expressions of negative emotions were generally
more difficult to classify (see also [10, 38]). The
group with TBI, however, demonstrated an exag-
gerated recognition deficit for the negative emotions
(especially fear, sadness and disgust) relative to
positive (happiness and surprise) in context-free
task formats. These results parallel earlier findings
[10, 50].
One possible explanation for this valence effect
concerns the number of discrete expressions belong-
ing to each valence. Given that there are fewer
expressions of positive emotion than negative
emotion, the task of distinguishing among negative
expressions might be relatively more difficult.
A related issue is that the decoding of expressions
of negative emotions may require more elaborate
processing than expressions of positive emotions,
particularly as distinctive features of negative expres-
sions may overlap (e.g. furrowed brows in anger
and sadness, widened jaws in fear, anger and some-
times disgust). Any inefficiency or interference with
normal processing resulting from neurological
impairment might see recognition accuracy rate fall
below threshold more readily for negative emotions
than positive emotions (see also [51]). Indeed,
research with schizophrenic patients [52–54] and
stroke patients (typically with right-hemisphere
lesions) [29, 30, 53] has similarly revealed a specific
recognition deficit for negative emotions.
Alternatively, these results may be taken as
support for cognitive models of emotion process
that specify separate neuronal pathways for select
emotions. In particular, it has been proposed that
negative emotions, such as fear, are mediated by
discrete circuits involving the amygdala and orbito-
frontal cortex [23], structures that are particularly
vulnerable to TBI.
Semantic knowledge and the effect of contextual
information
The TBI group matched labels of emotions to
everyday contexts with a high degree of accuracy,
performing as well as the control group in this area.
It would appear that the manifest difficulties the TBI
group experienced on the expression recognition
tasks were not attributable to semantic access to
words pertaining to basic emotional states.
In contrast, when asked to match facial expres-
sions to a context, many participants with TBI
were poor. Furthermore, they tended to choose
labels that corresponded well to the context,
but not to the faces they had actually selected. This
accuracy for context rather than facial information
refines the earlier findings, suggesting that this
group had specific difficulty understanding facial
expressions rather than emotion more broadly
defined.
Evenso, both TBI and control groups evidenced
a similar degree of improvement in expression
identification when provided with contextual infor-
mation — in this case, information about the social
context — although the TBI group remained less
accurate than controls throughout. Thus, for
the majority of participants with TBI, access to
contextual information attenuated impairments in
expression recognition. It would seem that, for
these participants, knowledge of the meaning of
different facial expressions was partially available
but difficult to access in the absence of other affective
cues.
Importantly, this pattern did not hold for all
participants with TBI. For example, two of the 15
had very poor facial affect recognition and were not
helped by contextual information. Indeed, although
these participants were fully aware of the meaning
of affect labels and could also match these appropri-
ately to the context, they were unable to match them
to facial characteristics. Nor could these individuals
match faces on the basis of expression. For these
individuals, the problem was not access to the
meaning of facial expressions, but appeared to be
a more pervasive difficulty processing the percepts
themselves.
The finding that semantic knowledge of emotions
remains relatively intact for the majority of people

with TBI and can facilitate emotion perception,
at least for some, has interesting implications for
rehabilitation. It suggests that conceptual reasoning
regarding likely emotional states may be a useful
strategy to ameliorate perceptual deficits. It also
suggests that, in everyday situations where emotions
are perceived in context, deficits are likely to be less
apparent than reported here. However, given that
there are many situations where the emotional state
of another is not predictable, contextual knowledge
will not always be of assistance. At such times,
deficits in facial affect processing will put the indi-
vidual at a significant social disadvantage.
Subjective experience of emotion
There was a great deal of variability in the pattern
and degree of self-reported post-injury changes in
emotional functioning for the TBI group, although
most reported some change in intensity or frequency
for at least one emotion (see Table III). A small
proportion of the changes reported appeared to
be directly related to the impact of disability itself,
e.g. an increase in fearfulness expressed as
concern of being unable to effectively fend off or
flee an assailant. However, in the majority of cases,
comments such as increased happiness, spontaneous
tearfulness and poor control of anger were seemingly
unrelated to post-injury adjustment to disability.
Thus, the results suggest an overall pattern of
emotional lability, with individual variations in
expression. Increases in emotion intensity were
reported approximately as twice as often as
decreases, a finding also reported in a recently
study of patients with surgically excised focal, frontal
lesions [50]. Nevertheless, a significant proportion of
participants — ranging from 17–29% — reported
overall decreases in emotional intensity for each of
the six basic emotions. While Hornak et al. [50]
reported an association between absolute magnitude
of subjective emotional change and emotion recogni-
tion, this study found that it was specifically the
decrease in emotional intensity, especially in the area
of fear and sadness, that was significantly associated
with poor emotion discrimination as measured by the
matching task.
The relationship between subjective change in
emotional experience and emotion recognition is
an intriguing one that is, as yet, relatively unexplored
in the neuropsychological literature. Although the
normal and developmental literature suggests that
the experience of emotions and the development of
recognition of emotions in others are intertwined,
their functional association in people with brain
injury is not well established. While this study
accords with Hornak et al.’s [7] 1996 study in the
finding that emotional experience and emotion
Recognition of emotion following TBI 797
recognition are related, a more recent investigation
by Hornak et al. [50] has suggested that these two
aspects of emotional processing may be dissociable.
In that study, while bilateral lesions of the orbito-
frontal cortex were related to changes to subjective
emotional state, nor all patients with subjective
changes to emotional state were found to be
impaired on emotion recognition tasks or visa
versa. A specific examination of the relation between
reduced emotional responsivity and emotion
recognition was not, however, reported. Nor did
Hornak’s et al. studies examine aspects of facial
expression processing beyond face labelling Yet, it
may be that changes to emotional experience will
be differentially associated with different kinds of
emotion processing tasks.
In a review of both animal and human studies,
Phillips et al. [55] argued that the immediate and
automatic identification of the emotional significance
of a stimulus and the affective response to it may be
mediated by a neural system that encompasses the
amygdala, insula and ventral portions of the anterior
cingulate and pre-frontal lobes. In contrast, they
argued for a separate system encompassing the
dorsal aspects of the anterior cingulate and frontal
lobes and the hippocampus that mediates effortful
regulation of responses to emotional stimuli as well
as other cognitive processes that are called into play
depending on the task. A similar dissociation was
reported by Adolphs et al. [22] such that damage
to the insula was specifically implicated in emotion
categorization failure, whereas the frontal operculum
was involved when the task required naming.
According to our findings, the ability to match facial
expressions on the basis of perceptual characteristics
was related to the ability to experience normal levels
of emotion, whereas the ability to provide verbal
labels for emotional expressions was not. Nor were
the ability to match facial expressions and the ability
to label expressions related. This suggests that
(1) matching and labelling rely, to some extent, on
different abilities and (2) matching, unlike labelling,
is partially related to the experience of emotions.
These patterns are consistent with the dual route of
emotion processing advocated by Phillips et al. [55].
Conclusion
In summary, these results suggest that the partici-
pants with TBI in this study were specifically
impaired in facial affect recognition relative to
matched controls, replicating the findings of previous
studies. They were impaired in both the labelling and
matching of emotional expressions, although these
two attributes appeared unrelated. Semantic knowl-
edge for affective terms and emotional contexts
was unaffected, arguing against the suggestion that
798 V. Croker & S. McDonald
TBI equally affects all components of the emotion
processing system. By the same token, two patterns
of difficulty were apparent. First, some participants
had problems with perceptual categorization that
was assisted by contextual cueing. They were also
able to use (intact) semantic memory stores to assist
retrieval of these perceptual categories implicating
a retrieval problem rather than loss of categorical
information. In contrast, some participants were not
assisted by context, suggesting a more profound
deficit categorizing facial affect.
Most participants with TBI reported some subjec-
tive change in the post-injury experience of everyday
emotion. Furthermore, there was a correlation
between subjective report of a reduction in emotional
responsivity and poor ability to match emotions
across identities. This suggests that the two facets
of emotional processing may be linked. No corre-
lation between labelling emotions and subjective
experience was observed, suggesting that labelling
is reliant upon a different set of processes. While
these results are suggestive, further investigations
are required in order to establish the impact of TBI
on the subjective experience of emotion, including
empathic reactions to others and the relationship
between this and emotion recognition.
The growing evidence that disorders in emotional
processing are prevalent amongst people with TBI
is intriguing and contributes a greater degree of
specificity to characterizing psychosocial functioning
in this population. Indeed, poor emotion recognition
in people with TBI does appear to translate into poor
social skills [8]. Nevertheless, there is still much to
be learned about the antecedents and consequences
of poor emotional functioning in this group.
Acknowledgements
Collection of data for this study was facilitated by
Discovery Grant DP0218141 from the Australian
Research Council. The authors would like to
acknowledge Clare Saunders and Cristina Bornhoffen
for their assistance in the collection of this data.
We would also like to express our gratitude to the
staff of Liverpool, Ryde and Westmead Brain Injury
Units for facilitating access to patients within their
service. Finally, we are indebted to the people with
TBI and their families as well as our community
participants who gave willingly of their time to make
this research possible.
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