Journal of the International Neuropsychological Society (2010), 16 , 369 – 382 .
Copyright © INS. Published by Cambridge University Press, 2010.
Research documenting sequelae of traumatic brain injury
(TBI) consistently show that changes in socio-emotional
functioning are more common than neuropsychological def-
icits. Such defi cits increase with severity of the TBI, occur-
ring in up to 80% of the severely injured population (e.g.,
Brooks, Campsie, Symington, Beattie, & McKinlay, 1986 ;
Thomsen, 1984 ). Such changes refl ect, in part, an inability to
recognize and regulate responses to emotional cues during
social interactions (Croker & McDonald, 2005 ; Hornak,
Rolls, & Wade, 1996 ; Ietswaart, Milders, Crawford, Currie, &
Scott, 2008 ). Individuals with TBI have diffi culty identifying
emotions in face (Green, Turner, & Thompson, 2004 ; Jackson &
Moffatt, 1987 ; Milders, Fuchs, & Crawford, 2003 ; Spell &
Frank, 2000 ) and voice (Marquardt, Rios-Brown, Richburg,
Recognizing vocal expressions of emotion in patients with
social skills defi cits following traumatic brain injury
A. DIMOSKA , 1 S. MCDONALD , 1 M.C. PELL , 2 R.L. TATE , 3 and C.M. JAMES 1
1 School of Psychology , University of New South Wales , Kensington 2052 NSW , Australia
2 School of Communication Sciences & Disorders , McGill University , Montreal Quebec H3G 1A8 , Canada
3 Rehabilitation Studies Unit , Northern Central Clinical School , University of Sydney , Sydney 2006 NSW , Australia
(Received July 14 , 2009 ; Final Revision December 15 , 2009 ; Accepted December 17 , 2009 )
Perception of emotion in voice is impaired following traumatic brain injury (TBI). This study examined whether an
inability to concurrently process semantic information (the “ what ”) and emotional prosody (the “ how ”) of spoken
speech contributes to impaired recognition of emotional prosody and whether impairment is ameliorated when little or
no semantic information is provided. Eighteen individuals with moderate-to-severe TBI showing social skills defi cits
during inpatient rehabilitation were compared with 18 demographically matched controls. Participants completed two
discrimination tasks using spoken sentences that varied in the amount of semantic information: that is, (1) well-formed
English, (2) a nonsense language, and (3) low-pass fi ltered speech producing “muffl ed” voices. Reducing semantic
processing demands did not improve perception of emotional prosody. The TBI group were signifi cantly less accurate
than controls. Impairment was greater within the TBI group when accessing semantic memory to label the emotion of
sentences, compared with simply making “same/different” judgments. Findings suggest an impairment of processing
emotional prosody itself rather than semantic processing demands which leads to an over-reliance on the “what” rather
than the “how” in conversational remarks. Emotional recognition accuracy was signifi cantly related to the ability to
inhibit prepotent responses, consistent with neuroanatomical research suggesting similar ventrofrontal systems subserve
both functions. ( JINS , 2010, 16 , 369–382.)
Keywords : Emotion perception , Prosody , Semantic , Inhibitory control , Filtered , Nonsense
Correspondence and reprint requests to: Skye McDonald, School of
Psychology, University of NSW, Kensington NSW 2052, Australia. E-mail:
Seibert, & Cannito, 2001 ; McDonald & Pearce, 1996 ; Milders
et al., 2003 ). However, impairment is greater for vocal emo-
tion (Spell & Frank, 2000 ) even when paired with visual
emotional cues (McDonald & Saunders, 2005 ), and improves
less over time, compared with facial emotion perception
(Ietswaart et al., 2008 ). Yet relatively few studies have exam-
ined vocal affect defi cits in TBI (Zupan, Neumann, Babbage, &
Willer, 2009 ).
Most research examining emotional prosody has focused
on patients with focal brain lesions. There is some evidence
for right hemispheric specialization in processing emotional
prosody (Bowers, Coslett, Bauer, Speedie, & Heilman, 1987 ;
Heilman, Bowers, Speedie, & Coslett, 1984 ; Ross & Monnot,
2008 ), although others fi nd no distinction (Baum & Pell,
1999 ; Pell & Baum, 1997 ; Pell, 2006 ; Schlanger, Schlanger,
& Gerstmann, 1976 ). Processing of both emotional and
grammatical prosody involves the superior temporal gyrus
bilaterally, although evidence continues to favor right hemi-
sphere specialization for emotion (Adolphs, 2002 ; Mitchell,
Elliott, Barry, Cruttenden, & Woodruff, 2003 ). In addition,
overlapping frontal–subcortical circuits become selectively
A. Dimoska et al.
activated depending on task demands. The orbito and ventral
medial frontal regions, amygdale, and basal ganglia are en-
gaged, especially during encoding and maintenance of
meaningful representations of emotional prosody (Buchanan
et al., 2000 ; Johnstone, van Reekum, Oakes, & Davidson,
2006 ; Kotz, Meyer, Alter, Besson, von Cramon, & Friederici,
2003; Pell & Leonard, 2003 ). The dorsolateral prefrontal cor-
tex is also engaged during effortful access of semantic
memory for labeling an emotional cue (Hariri, Bookheiner,
& Mazziotta, 2000 ; Oschner & Barrett, 2001 ; Phillips,
Drevets, Rauch, & Lane, 2003 ). Ventral frontal and temporal
regions implicated in emotion processing are commonly
compromised following TBI (Fujiwara, Schwartz, Gao,
Black, & Levine, 2008 ; MacKenzie et al., 2002 ). Impairment
is not, however, contingent on the presence of particular focal
injuries (Ietswaart et al., 2008 ) but may also be due to diffuse
axonal injury causing a shearing of connections between crit-
ical areas mediating emotion perception (Adolphs, Damasio,
Tranel, Cooper, & Damasio, 2000 ; Green et al., 2004 ).
In part, judgments of vocal emotion are driven by the dis-
tinctiveness of prosodic elements including pitch, intonation,
loudness, and tempo. Patterns of errors suggest they are caused
by similarities in prosodic parameters between emotions
(Leinonen, Hiltunen, Linnankoski, & Laakso, 1997 ) with some
emotions easier to identify than others. Anger is characterized
by increased speech rate, wider range in pitch variations and
greater intensity, making it one of the most identifi able emo-
tions in voice (Scherer, 2003 ). Fear is also relatively easy to
identify, while happiness is more diffi cult to recognize in vocal
than facial expressions (Scherer, 2003 ; Zupan et al., 2009 ) and
surprise is the most diffi cult to distinguish (Pell, 2006 ).
Although some have reported that TBI causes impairment
across all emotions (Ietswaart et al., 2008 ; McDonald &
Saunders, 2005 ), Spell and Frank ( 2000 ) found adults with TBI
were more accurate identifying anger and happiness compared
with the fearful voice. This pattern is diffi cult to reconcile with
an emotion perception problem based on acoustic features alone
and suggests other factors underpin defi cits following TBI.
An important consideration is the interplay between
speech prosody (the how) and the content of what is being
said (the what ). Speech prosody delivers the emotion behind
the words in a spoken message (Mitchell & Ross, 2008 ).
While prosodic information is available and used early in
comprehension (Kaganovich, Francis, & Melara, 2006 ;
Steinhauer, Alter, & Friederici, 1999 ), there is a bias for pro-
cessing semantic content over prosody (Lew, Chmiel, Jerger,
Pomerantz & Jerger, 1997 ). Semantic information is less
open to interference than prosody (Jerger et al., 1993 ;
Morgan & Brandt, 1989 ). Furthermore, in a modifi ed Stroop
task, incongruent semantic information interferes more with
the identifi cation of prosody than vice versa (Grimshaw,
1998 ) and while directions to ignore prosody are easily com-
plied with, semantic information is diffi cult to completely
ignore when focusing on prosody (Besson, Magne, & Schön,
2002 ; Wambacq & Jerger, 2004 ).
It is possible that some of the diffi culties people with TBI
experience with vocal emotion stem from a failure to manage
dual processing demands. Many people with TBI show
an overly literal interpretation of indirect conversational
remarks such as sarcasm (McDonald & Flanagan, 2004 ).
Although various explanations have been considered (e.g.,
McDonald & Flanagan, 2004 ; Shamay-Tsoory et al., 2005 )
a consistent fi nding is that defi cits in information processing
speed, working memory, and reasoning are commonly asso-
ciated (McDonald et al., 2006 ; McDonald & Pearce, 1996 ,
Martin & McDonald, 2004 ). These cognitive defi cits appear
to lead to an over-reliance upon the salient semantic infor-
mation at the expense of contextual cues, some of which are
prosodic. If people with TBI have diffi culty processing both
prosody and semantic content, reducing semantic content
should lead to a shift in processing resources toward prosody
(Creusere, Alt, & Plante, 2004 ) improving accuracy. This is
unless TBI causes impaired processing of emotional prosody
itself (Zupan et al., 2009 ). Semantic information can be
reduced by using a “nonsense” language that conveys little
semantic meaning (Grandjean et al., 2005 ) or “fi ltering”
out high frequencies in speech making the semantic content
inaudible whilst preserving the prosodic elements (Kotz
et al., 2003 ).
Although studies of patients with focal unilateral lesions
have largely found a specifi c impairment in processing emo-
tional prosody (Bowers et al., 1987 ; Pell & Baum, 1997 ;
Pell, 2006 ), some have found that perception of prosody im-
proves with removal of semantic information in patients with
left-hemisphere lesions (Behrens, 1985 ; Heilman et al.,
1984 ; Lalande, Braun, Charlebois, & Whitaker, 1992 ; Ross
& Monnot, 2008 ; Ross, Thompson, & Yenkowsky, 1997 ).
TBI is characterized by diffuse, multifocal damage that is
often bilateral affecting frontal and temporal systems (Levin,
Williams, Eisenberg, High, & Guinto, 1992 ). Consequently,
it is unclear whether removing semantic information will
ameliorate defi cits in recognition of vocal emotion.
The following study aimed to replicate fi ndings of vocal
emotion perception problems in a sample of adults with TBI
presenting with postmorbid changes in social skills. We
hypothesized that if an inability to manage the dual processing
requirements of understanding the how and the what of
spoken speech contributes to impaired emotional prosody
recognition, then this impairment should be ameliorated
when little (nonsense sentences) or no semantic information
(fi ltered sentences) is provided. Alternatively, if TBI causes
impairment in the processing of emotional prosody itself,
then we anticipated performance would become more de-
graded with reduced semantic information.
Lesions in the orbito and ventral medial frontal cortices
cause perseveration of prepotent/automatic responses
(Bechara et al., 1996; Freedman et al., 1998 ) and disinhib-
ited, impulsive behavior (Starkstein, 1997 ) concurrently
with defi cits in emotion recognition (Damasio, 1994 ; Hornak
et al., 1996 ; Pettersen, 1991 ). These regions, with connec-
tions to subcortical and brain stem nuclei (Vogt, 1986 ) may
mediate a reciprocal function where effective recognition
of emotional cues assists with regulation of behavioral re-
sponses (Oschner & Barrett, 2001 ). Emotion recognition has
Recognizing vocal emotion after TBI
been linked to the display of socially appropriate behavior in
brain-injured patients (Hornak et al., 1996 ; Pettersen, 1991 )
and cognitive measures of inhibitory control (Dujardin et al.,
2004 ; Uekermann, Daum, Schlebusch, & Trenckmann, 2005 )
although not always (Langenecker, Bieliauskas, Rapport,
Zubieta, Wilde, & Berent, 2005; Milders et al., 2003 ). The
second aim of this study was to examine the relation between
emotion perception, inhibitory control, and behavioral im-
pulsivity. We hypothesized that there would be a positive
association among these three constructs.
Nineteen adults with moderate–severe TBI were recruited
from metropolitan Brain Injury Units in NSW, Australia. All
participants had suffered brain injuries of suffi cient severity
to warrant inpatient rehabilitation, and were recruited on the
basis of clinical judgment that they (1) were experiencing
social diffi culties as a result of the TBI and (2) had suffi cient
cognitive and motor capacity to understand and comply with
instructions. Exclusion criteria included premorbid neuro-
logical or psychiatric conditions; current aphasia or agnosia;
current psychosis. One participant was subsequently
excluded because of an insuffi cient number of attempted re-
sponses to allow meaningful statistical analysis. The
remaining 18 participants (13 males, 5 females) were aged
22 to 63 years (Mean 45.2; SD 11.7) ( Table 1 ).
Posttraumatic amnesia (PTA) was established from med-
ical records. Mean duration was 79.8 days (range, 1–270
days), no different (one sample t -test; p = .94) to that re-
ported in a consecutive series of TBI inpatients (e.g., Tate,
Broe & Lulham, 1989 : PTA mean = 81.2 days; range 4 to
>168 days). That is, this sample was representative of the
severity of injury typically seen in this population. Our
sample did include two participants with PTA of 1 day or
slightly less (Pts 15 and 21) which is identifi ed as a mild
TBI by some grading classifi cations (Mild Traumatic Brain
Injury Committee of the Head Injury Interdisciplinary Spe-
cial Interest Group of the American Congress of Rehabilita-
tion Medicine, 1993 ) and moderate by others (Jennett,
1976 ), although the presence of radiological abnormalities
suggests that these injuries were more complicated. Both
participants experienced social diffi culties as a consequence
of their brain injuries and had undergone inpatient rehabili-
tation. Mean time post injury for the group was 15.0 years
( SD 9.5 months). Before the injury, all participants had been
in full-time work (four professional, eight skilled, four un-
skilled) or studying (2). Following their injuries, two partic-
ipants were in full-time employment while six worked on a
part-time basis and 10 were unemployed. On average, TBI
participants had 12 years ( SD 2.2 years) of education. One
patient with TBI was deaf in his right ear due to peripheral
damage. While unilateral deafness affects speech localiza-
tion and reduces ability to screen background noise, speech
discrimination in the good ear remains intact. Thus, the par-
ticipant’s ability to perform the tasks was unaffected, and
this was confi rmed with the participant during practice
Eighteen control participants (12 males) aged 23–62 years
(Mean 44.4; SD 12.1), with 11.3 years education ( SD 1.6)
and without neurological impairment, were also tested.
These were volunteers recruited through community news-
paper advertisements and fl yers in local hospitals. They were
screened for neurological, psychiatric, and motor–sensory
impairments before acceptance into the study. The groups
did not differ with respect to age ( p = .837) or education ( p =
.317). All participants spoke fl uent English and had normal
or corrected-to-normal vision.
Three sets of prosody stimuli were presented over two emotion
recognition tasks. Two sets (Pell, Paulmann, Dara, Alasseri, &
Kotz, 2009 ) consisted of short, digitally recorded declarative
sentences (Mean Length: 1.7 s; Range: 0.9 to 2.5 s) produced
by two male (Mean Pitch: 192 Hz; Range: 114–388 Hz) and
two female (Mean Pitch: 237 Hz; Range: 112–388 Hz) actors.
Sentences were sampled at a rate of 48 kHz, at an intensity of
75dB, and were spoken in either (1) semantically well-
formed American English (e.g., That car just splashed me! )
or (2) a nonsense language with appropriate phonetic and
prosodic structure for English (e.g., Someone migged the
pazing ). Sentences were spoken as: happy, pleasantly sur-
prised, angry, and afraid (see Table 2 for acoustic character-
istics). The semantically well formed stimuli provided
emotionally biased semantic content that facilitated discrim-
ination for happy, angry, and afraid. (The pleasantly sur-
prised content was more ambiguous (e.g., You cleaned the
entire garage! ). In contrast, nonsense words provided little
linguistic information while leaving emotion prosody intact.
Each actor gave two exemplars of each emotion resulting in
a set of 32 stimuli for the semantic stimuli and a different set
of 32 stimuli for the nonsense stimuli.
A third set of 32 stimuli was created by low-pass fi ltering
the semantically-well formed stimuli using a Hann band fi l-
ter in Praat (v 5.0.2; www . praat . org ) with a cutoff at 360 Hz
for male actors and 400 Hz for female actors (Koff et al.,
1999 ), and a smoothing width of 100 Hz. Cutoff points were
selected following analysis of the fundamental frequency
(f 0 ) maximum across emotions and incrementally adjusting
the cutoff by 30 Hz around this point until linguistic infor-
mation was subjectively inaudible. The resultant fi ltered
stimuli retained pitch and contour variations over time whilst
offering no linguistic information, sounding like “muffl ed”
speech. Five postgraduate students listened to a subset of the
stimuli ( n = 10), and all reported that no linguistic informa-
tion was identifi able.
The design of the emotion discrimination and emotion
labeling tasks is depicted in Figure 1 .
A. Dimoska et al.
Table 1. Demographic and clinical characteristics of participants with TBI
Cause of injury
Site of injury/initial CT scan
Problems in social skills resulting from the injury
R frontal hematoma
1 Repeats self a lot. Does not understand meaning
behind what people are saying. Easily frustrated in social situations as diffi cult to get point across.
1 Slow to pick up on social cues. Hard to concentrate on
what people are saying. Gets frustrated and irritated.
R subdural hematoma, L intracranial hemorrhage, 5-mm midline shift
2 Wooden and awkward socially, doesn’t pick up
3 Giggles a lot, doesn’t know when to stop talking;
cannot take another’s perspective.
Large atrophic lesion in R temporal lobe
2 No humor, black and white in social situations,
Parieto-occipital fracture; focal atrophy of
R frontal and temporal lobes
2 Inappropriate verbal sexual comments. Misguided
humor. Frustration with self and others. Dogmatic and rigid in expressing opinions.
Extensive R temporal encephalomacia,
R frontal extradural collection, lateral and ventricular dilation
3 Lost sense of humor. Lost ability to pick up social
cues, e.g., appropriate conversation. Timid in social situations. Repeats himself. Only talks to people he likes otherwise can become rude. Decreased eye contact.
Cerebral edema, L fronto-temporal and occipital lobe contusions
2 Overfriendly, presents as very immature. Giggles a
lot and sulks. Excessive, unrelenting and loud conversation. Some inappropriate comments and touching.
R frontal contusion, L parietal and occipital contusions, depressed fracture of R frontal bone
2 Reserved and unresponsive in social situations
Mild frontal bruising
1 Cannot cope with multiple conversations. Inability
to focus. Short tempered with people.
Blow to Head
2 Problems regulating speech quality, overly loud and
Bilateral subdural hematoma
1 Feels like a social void. Frustrated with not
understanding social cues. Listens but does not speak as others cannot understand.
L frontal hematoma
1 Finds it hard to read signals and pick up on cues in
Ischemic impact on L parietal region and
small hematoma at level of 4 th ventricle
3 Loss of confi dence. Finds it diffi cult to pitch humor
appropriately. Improving slowly over the years but impact on sociability still clear.
Recognizing vocal emotion after TBI
Cause of injury
Site of injury/initial CT scan
Problems in social skills resulting from the injury
R temporal lobe fracture; extradural hematoma and contusion L temporal lobe
1 Finds socializing diffi cult. Lost sense of humor.
Does not appreciate jokes and takes things very seriously. More trusting of others and gullible. Colder and more defensive.
1 Not good with people any more. Isolated. Others
have diffi culty understanding him. Slow and cannot pick up on detail.
Subdural hematoma in R
2 Concrete and rigid; fails to understand irony and
sarcasm; inert in social settings.
R side injury; Possible brainstem
damage, air/fl uid in ethmoid and maxillary sinuses
1 Does not socialize at all as too diffi cult. Does not
understand social situations. Misses cues, e.g., when to leave, when to talk. No longer has a sense of humor
and cannot make jokes. Slow to comprehend people.
Note. Severity classifi cation as recommended by Jennett ( 1976 , 1996 ); Ext = extremely; GCS = Glasgow Coma Scale; MVA = motor vehicle accident; MVA Ped = motor vehicle accident as a pedestrian; R = right;
L = left;
2 Clinician report.
3 Maternal report.
Table 1. Continued
In the emotion discrimination task 32 pairs of nonsense
stimuli and 32 pairs of fi ltered stimuli were presented and
participants made same/different judgments regarding the
emotion in the voice pairs. Response options were presented
on computer screen and participants responded with either a
left (different) or right (same) button press on a keyboard.
Each trial began with a 500-ms warning stimulus followed
by the fi rst stimulus, a 500-ms inter-stimulus-interval, and
then the second stimulus. Participants had 10 seconds to re-
spond after the second speaker. The task consisted of eight
blocks of eight stimuli pairs, alternating between blocks of
nonsense and fi ltered stimuli. Pairings of “same” and “dif-
ferent” emotional prosody were equiprobable (50%) across
the task. All pairings involved sentences of different seman-
tic content spoken by different speakers of the same gender.
The fi rst block of each nonsense and fi ltered stimulus set
began with three practice trials.
In the emotion labeling task participants were required to
identify emotional tone in speech using either prosodic
features alone or with semantic information. Participants
listened to a single stimulus and identifi ed whether the emo-
tion in the voice was happy, surprised, angry, or afraid in a
forced-choice task. Use of only four options reduced working
memory demands (Pell, 2006 ) as did presentation of the re-
sponse options on both computer screen and keyboard but-
tons. The task consisted of eight blocks (eight trials/block)
of alternating semantic and nonsense stimuli (i.e., four
blocks for each stimulus type). 1 Each trial began with a
warning stimulus for 500 ms, followed by the speech stim-
ulus and then a request to match the speech stimulus to the
appropriate emotion (within 10 s). In the fi rst four blocks,
the response options on screen consisted of written words,
with participants required to press the corresponding labeled
keyboard button. In the second set of four blocks, the re-
sponse options were four black and white photographs (two
male, two female) (Ekman & Friesen, 1976 ) representing the
four emotions. Participants again were required to press the
corresponding labeled keyboard button (in the same order as
above). The fi rst block of each semantic and nonsense stim-
ulus set began with three practice trials.
Measures of Impulsivity and Inhibition
Participants completed Barratt’s Impulsiveness Scale
(BIS-11), a 30-item self-report survey measuring Motor
1 A pilot of the three stimulus sets on 13 undergraduate medical students
revealed fi ltered stimuli were labeled as one of four emotions with the
percentage of correct responses no better than chance (50%). Thus, we
excluded this stimulus set from the labeling task.
A. Dimoska et al.
Impulsiveness (i.e., acting without thinking), Attentional Im-
pulsiveness (i.e., easily bored when sustained attention re-
quired) and Nonplanning Impulsiveness (i.e., a lack of
concern for future consequences) (Patton, Stanford, & Barratt,
1995 ). Internal consistency reliability ranges from 0.79 to
0.83 for healthy adults, substance-abuse patients and prison
inmates (Patton et al., 1995 ) and is approximately 0.78
(Votruba et al., 2008 ) for adults with TBI, who show greater
total impulsiveness scores than controls (Dyer, Bell,
McCann, & Rauch, 2006 ; McHugh & Wood, 2008 ). Scores
for each sub-factor and an overall Impulsiveness score were
Inhibition of a prepotent, automatic response was evaluated
using the Haylings Sentence Completion Test (Burgess &
Shallice, 1997 ) whereby participants are asked to provide a
word to fi nish a sentence that either completes the sentence
(“initiation” task) or is completely unconnected (“inhibi-
tion” task). TBI patients (Draper & Ponsford, 2008 ) and
frontal-injured patients (Burgess & Shallice, 1996 ) show
poor performance on this test. A response time score and an
error score for the inhibition task as well as an overall re-
sponse score across tasks were calculated and scaled using a
scoring system in Burgess and Shallice ( 1997 ) and converted
to Sten scaled scores (differences between Sten scores = 0.5
of an SD ). Scores ranged from 1 (outside normal range)
through to 10 (99th percentile or very superior). A scaled
score of 2 (1%) or below is considered impaired (Burgess &
Shallice, 1997 ). Test–retest reliability of the inhibition error
score ranges from 0.41 for healthy controls to 0.72 for brain
injured (lesion) patients (Burgess & Shallice, 1997 ).
Table 2. Acoustic characteristics of emotional prosody stimuli
Pitch Mean (Hz) Pitch Range (Hz) Pulse rate Voice breaks (count) Duration (s)
Note. “Voice breaks” was estimated as the number of distances between consecutive pulses that are longer than 1.25 divided by the pitch
fl oor (Boersma & Weenink, 2007 ).
Fig. 1. In this experimental design, each participant completed an
emotion labeling and an emotion discrimination task, each consist-
ing of two stimulus sets (32 trials each), resulting in a total of 128
emotional prosody trials.
The discrimination and labeling tasks were presented on a
computer in counterbalanced order across participants. Par-
ticipants listened to prosody stimuli over volume-adjustable
computer headphones. In the labeling task, participants were
told that they would hear a person speaking in either English
or a “made-up” nonsense language and that they were to
identify the emotion in each voice from the four alternatives
offered. In the discrimination task, participants were in-
structed to listen to both speakers, who would either be
speaking in a nonsense language or a muffl ed tone, before
deciding whether the emotion in the two speakers was
“same” or “different”. Across all tasks, participants were in-
structed that it was more important that they should listen to
“how” the speaker was speaking rather than to “what” they
Following the experimental tasks, participants completed
the BIS-11 and neuropsychological tests including the
Wechsler Test of Adult Reading (WTAR), the Trail-Making
Test, WMSIII subtests: Logical Memory 1 and Faces 1,
WAISIII subtests: Similarities, Digit Span, Digit Symbol-
Coding (WAIS-III), and the Haylings Sentence Completion
Test. This study and its procedures were approved by the
University of NSW Human Research Ethics Committee.
Accuracy rates, converted to percentages of total attempted
responses (i.e., omission errors excluded), and RT were cal-
culated. A Repeated-measures 2 × 2 ANOVA was used in the
discrimination task, with the within-subject factor CONDI-
TION (nonsense vs . fi ltered) examining participants’ accu-
racy (%) and mean reaction time (MRT). A 2 × 2 × 2 design
was used in the labeling task, with the within subjects factors
CONDITION (original vs . nonsense) and TASK (match-to-
words vs . match-to-faces). A separate analysis was per-
formed in each task to examine differences between Emotion
Types, that is, happy versus pleasantly surprised, angry versus
afraid, and positive (happy + surprised) versus negative
(angry + afraid). Signifi cant main effects were followed
with separate analyses and alpha adjusted for the number of
For the Impulsiveness Scale, where data were missing for
items (2% of all cells), mean person was used to replace these
(Roth, Switzer, & Switzer, 1999 ), allowing a total score to be
Recognizing vocal emotion after TBI
calculated for each individual. ANOVAs were used to exam-
ine between-group differences on the Impulsiveness sub-
scales and on all neuropsychological measures except the
Haylings test for which the Mann-Whitney U test was used.
Pearson’s bivariate correlations were performed between
experimental task measures, and neuropsychological and
Table 3 presents neuropsychological test scores for
individual participants with TBI as well as between-group
Participants with TBI showed overall poorer accuracy
(69.3%) when making same/different judgments on pairs of
emotional prosody stimuli compared with controls (76.6%
accuracy rate)( F [1,34] = 7.3; p < .05) ( Figure 2 ).
Accuracy was higher in the nonsense (76.2%) then fi ltered
stimuli (69.7%) ( F [1,34] = 8.9; p < .01), although this effect
did not differ between groups ( p = .285). An analysis for
each emotion type on “same” trials only revealed no signifi -
cant differences between groups in the recognition of dif-
ferent emotion types ( p > .10).
There were no differences in MRT (Controls: 1.6 vs . TBI:
1.9 s; p > .10) or the probability of omissions (Controls: 2.8
vs . TBI: 2.2 %; p > .5).
Participants with TBI (70.7% accuracy rate) had overall
greater diffi culty labeling emotional prosody compared with
controls (86.5% accuracy rate) ( F [1,34] = 11.2; p < .01)
( Figure 3 ).
Across groups, participants were more accurate when
judging semantic (84.9%) than nonsense stimuli (73.5%)
( F [1,34] = 24.7; p < .001). A signifi cant interaction with Group
( F [1,34] = 6.1; p < .05) revealed that this effect occurred only
in the TBI group. A signifi cant Task effect revealed that partic-
ipants were better at matching prosody to words (83.1%) than
to faces (75.2%)( F [1,34] = 20.7; p < .001), and this difference
was greater for nonsense than semantic stimuli ( F [1,34] = 5.1;
p < .05). A Group × Task interaction was not signifi cant ( p =
.198), although diffi culty matching prosody to faces appeared
greater in the TBI group.
Subsidiary analyses in the matching-to-words condition,
with alpha adjusted for the number of comparisons ( α <
.0125), revealed accuracy differed between groups for non-
sense ( t  = 1.7; p < .01) but not semantic stimuli ( p >
.0125). In the matching-to-faces condition, the groups dif-
fered for both nonsense ( t  = 3.2; p < .01) and semantic
stimuli ( t  = 2.8; p < .01).
A signifi cant main effect of Emotion-Type was found
( F [3,32] = 6.1; p < .01), and this interacted with Group
( F [3,32] = 4.7; p < .01) ( Figure 4 ). Subsidiary analyses
revealed group differences for happy ( F [1,34] = 19.3; p < .001)
and afraid ( F [1,34] = 10.1; p < .01), but not angry ( p = .053) or
surprised ( p = .110). Both groups performed most poorly when
judging surprised. Anger was the easiest of the emotions for
TBI participants to identify. There was also a tendency toward
more accurate identifi cation of negative than position valence
emotions across groups ( F [1,34] = 3.4; p = .072).
Mean reaction time was overall slower in the TBI (4.514 s)
than control group (3.457 s)( F [1,33] = 13.7; p = .001), with
a tendency toward faster responses when matching emo-
tional prosody with faces (3.9 s) rather than words (4.1 s) ( p =
.116). However, there were no interactions between task,
condition, and group. There were also no differences in the
probability of omissions committed between TBI (4.5%)
and control (4.9%) groups ( p > .05).
Discrimination versus Labeling
Nonsense stimuli were presented in both emotion tasks,
therefore, a direct comparison could be made. TBI partici-
pants showed greater accuracy in the discrimination (71.3%)
task compared with labeling (61.3%), while controls per-
formed similarly across tasks (81.1% vs . 83.8%) ( F [1,34] =
10.6; p < .01). Across all conditions, overall performance in
the discrimination and labeling tasks was highly correlated
( r = .605; p < .001), as were matching-to-labels and match-
ing-to-faces within the labeling task ( r = .759; p < .001).
The TBI group scored lower than the control group on Hay-
lings overall (Median score TBI: 3 vs . Controls: 6, U = 22.5;
p < .001), inhibition response time (Median score TBI: 4 vs .
Controls: 6, U = 49.0; p < .001) and inhibition error scores
(Median score TBI: 2 vs . Controls: 7, U = 58.5; p = .001).
Eleven TBI participants (and one control participant)
obtained an abnormal score (i.e., 2 or less) for Haylings in-
hibition errors ( Table 3 )
The TBI group self-reported greater impulsivity than the
control group (73 vs . 63, F [1,36] = 8.7; p <.01). Sub-test
scores revealed a signifi cant difference in Nonplanning Im-
pulsiveness (20 vs . 25, F [1,36] = 11.2; p < .01) and almost
signifi cant differences for Motor ( p = .083) and Attentional
Impulsiveness ( p = .084).
Correlations Between Measures
Across groups, Haylings inhibition error rate was positively
related with performance on both the discrimination ( r =
0.693; p < .001) and labeling tasks ( r = 0.572; p < .001). In-
hibition error rate was also negatively related with Barratt’s
Nonplanning Impulsiveness ( r = −0.351; p < .05). Impul-
siveness scores did not correlate with accuracy scores on the
emotion recognition tasks.
A. Dimoska et al.
Table 3. Neuropsychological test scores for participants with TBI
Trails B WMS-III Faces I
Digit Symbol - Coding
Note. WTAR = Wechsler Test of Adult Reading; Trails = Trail-Making Test A and B. All scores represent standard scores based on Wechsler manuals except Trails A and B which are presented as seconds taken to
complete. *TBI signifi cantly impaired relative to control group ( p < 0.05).
1 Haylings scaled scores whereby lower scores refl ect poorer performance (see Burgess & Shallice, 1997 ), and group scores are expressed as medians.
Recognizing vocal emotion after TBI
There was a positive relationship between two neuropsy-
chological constructs, that is, working memory (Digit Span)
and verbal comprehension (Similarities), and emotion la-
beling ( r = 0.520; p < .01; r = 0.413; p < .05, respectively),
but not discrimination (both p > .05). These signifi cant effects
remained after controlling for education. No other neuropsy-
chological measures showed signifi cant relationships with
emotion perception accuracy. Notably, correlations between
measures of RT and Symbol Digit-Coding or Trail Making
Tests A and B were nonsignifi cant. Due to the relationship
observed between working memory and the emotion recogni-
tion tasks, analyses were conducted with working memory as
a covariate. Findings remained signifi cant ( p < .05).
Individual TBI Profi les
Despite a signifi cant group difference in discrimination ac-
curacy, only one TBI participant was impaired when judging
Fig. 2. Mean accuracy (%) and standard deviation ( SD ) of making
same/different judgements in the nonsense and fi ltered conditions for
each group; y -axis = 50–100%, bar = 1 SD . TBI, traumatic brain injury.
Fig. 3. Mean accuracy (%) and standard deviation ( SD ) when
matching emotional prosody to words (left) and faces (right) in the
semantic and nonsense conditions for each group. Signifi cant group
differences are indicated by asterisks ; y -axis = 50–100%, bar = 1
SD . TBI, traumatic brain injury.
Fig. 4. Mean accuracy (%) and standard deviation ( SD ) of labeling
emotional prosody for each emotion type in the control and trau-
matic brain injury (TBI) groups. Signifi cant group differences for
happy and afraid are indicated by asterisks; y -axis = 50–100%, bar =
1 SD .
nonsense stimuli and one participant was impaired when
judging fi ltered stimuli; no participants were impaired on
overall discrimination accuracy ( Table 4 ). In the labeling
task, nine participants were impaired in overall labeling ac-
curacy. When matching emotional prosody to words, four
were impaired in judging semantic stimuli and fi ve when
judging nonsense stimuli. When matching emotional prosody
to faces, seven were impaired when judging semantic stimuli
and seven when judging nonsense stimuli.
CT scans were available for 16 of the 18 TBI participants.
As our group was heterogeneous in their injuries, we could
not examine left versus right brain injuries (contrast: Pell &
Baum, 1997 ; Pell, 2006 ). However, it was interesting to note
that participants who were impaired on labeling were those
with intracerebral and subdural hemorrhages, cerebral
edema, or extensive injuries to the left or right temporal
lobes. In contrast, while four participants presented with
focal lesions in the right frontal region (Pts: 1, 8, 9, 11) only
one was impaired on the labeling task.
Four TBI participants (Pts: 1, 8, 27, 28) had received
emotion recognition training three years before testing
(Bornhofen & McDonald, 2007 ), and three of these showed
no impaired emotion recognition on the tasks. Thus, dis-
crimination and labeling accuracy were re-analyzed ex-
cluding these four participants, as well as the partially deaf
participant and fi ve corresponding control participants. The
signifi cant group and condition effects remained.
Time since injury was unrelated to any performance
measures ( p > .05). The skewed distribution toward ex-
tremely severe injury (i.e., PTA > 28 days) meant a sub-
group analysis for injury severity was not possible.
Participants with TBI were poorer at both discriminating and
labeling emotional prosody, relative to non–brain-injured
controls. Contradicting expectations, performance was not
improved when there was little or no semantic information.
Group differences were observed in both discrimination and
A. Dimoska et al.
labeling tasks where semantic information was reduced
(nonsense) or completely removed (fi ltered). In contrast,
groups were similar when judging stimuli containing seman-
tically biased information that helped identify the emotional
It is possible that removing semantic information did not
have the intended effect of reducing semantic bias, but rather
made individuals search harder for this content (Beaucousin,
Lacheret, Turbelin, Morel, Mazoyer, & Tzourio-Mazoyer,
2007; Kotz et al., 2003 ; Meyer, Alter, Friederici, Lohmann,
& Von Cramon, 2002). While we cannot determine this, our
results highlight the importance in both healthy and TBI par-
ticipants of semantic content over prosodic information (Pell &
Baum, 1997 ; Pell, 2006 ), in line with a semantic processing
bias (Besson et al., 2002 ; Grimshaw, 1998 ; Jerger et al.,
1993 ; Wambacq & Jerger, 2004 ).
Although TBI performance in the discrimination task
was poorer compared with controls, individual participants
were not abnormally poor. Same/different discrimination is
believed to involve automatic emotion recognition, medi-
ated by the ventral frontal–subcortical circuit (Adolphs,
2002 ; Kotz et al., 2003 ; Pell & Leonard, 2003 ). In our study
this ability, while less effective in TBI participants, was not
wholly impaired. In contrast, half the TBI group was im-
paired when making semantic judgments about emotional
prosody stimuli. This is consistent with research showing
that labeling emotions is more demanding for brain injured
individuals than making same/different discriminations
(Ietswaart et al., 2008 ; Pell, 2006 ; Tompkins & Flowers,
1985 ) because it requires effortful access of semantic
memory, linked with the dorsolateral prefrontal cortex
(Adolphs, 2002 ). This interpretation fi ts with the associa-
tion found between working memory and performance on
the labeling but not discrimination task. Even so, working
memory did not entirely account for group differences
which remained when memory was controlled. Rather, a
process common to discrimination and labeling (which
were highly inter-correlated) appears to be responsible.
Overall, our fi ndings suggest that automatic emotion recog-
nition is reduced in effectiveness following TBI, and that
increased semantic emotion memory demands cause further
The TBI individuals were selectively impaired when la-
beling some emotions (i.e., happy, afraid) but not others
(e.g., pleasantly surprised, angry). Pleasantly surprised was
diffi cult for both groups, while anger was easiest for the TBI
group. Spell and Frank ( 2000 ) also found TBI adults were
impaired when judging fear and accurate when judging an-
gry voices, but in contrast to us, they found that happy was
well recognized (Spell & Frank, 2000 ). No differences in
accuracy for different emotions were found in the discrimi-
nation task. This is in line with the suggestion of Ietswaart
et al. ( 2008 ) that TBI may selectively impair the semantic
component of emotion identifi cation, rather than automatic
emotion discrimination per se . The salience and distinctive-
ness of prosodic cues may be essential for effortful-semantic
categorization of emotion following TBI. Enhancing some
prosodic parameters may, therefore, improve accuracy.
Table 4. Impaired performance of individuals with TBI in emotion discrimination, inhibition, and impulsivity measures
impulsiveness scale Discrimination Task
Task - Words
Task - Faces Labeling Task
Overall Inhibition RT
Errors BIS Total Non-Plan F N
accuracy S N S N
Note. Non-Plan = Non-Planning Sub-scale, F = Filtered stimuli, N = Nonsense stimuli, S = Semantic stimuli, ** = abnormal performance score falling below
2 SD of the control group’s mean.
Recognizing vocal emotion after TBI
Our TBI participants showed a 9% drop in accuracy when
matching semantic prosody to faces rather than words (com-
pared with 2% for controls) and this effect tended toward
signifi cance. At an individual level, fi ve participants were
impaired when matching semantic prosody to faces but not
when matching to words, despite the fact that semantic la-
bels were always visible. This suggests that, for these partic-
ipants, presence of facial information degraded evaluation of
prosody. Neuroimaging has shown that the supratemporal
auditory cortex, normally activated to audio-only stimuli,
becomes suppressed during audiovisual presentations (Besle,
Fort, Delpeuch, & Giard, 2004 ). McDonald and Saunders
( 2005 ) also found more individuals were impaired judging
audiovisual than audio-only or visual-only displays of emo-
tion. Clearly further research is needed to examine how bi-
modal emotion cues of emotion are integrated. This appears
to be a unique defi cit in some adults with TBI (McDonald &
Saunders, 2005 ).
The heterogeneous make-up of the TBI participants limits
discussion of neural correlates. However, it is interesting to
note that three of the four participants presenting with focal
lesions in the right frontal region (Pts: 1, 8, 11) were not
impaired on any emotion recognition tasks, supporting a
view of bilateral contributions to emotion processing (Baum
& Pell, 1999 ; Pell & Baum, 1997 ; Pell, 2006 ; Schlanger
et al., 1976 ). Given that emotional prosody recognition is a
highly integrative process and past studies have not found a
correlation between focal injuries in TBI and emotion per-
ception impairment (Green et al., 2004 ; Ietswaart et al.,
2008 ), future studies should examine the role of diffuse
Consistent with past studies (Dujardin et al., 2004 ;
Uekermann et al., 2005 ), the TBI group had poor inhibitory
control compared with controls and this was associated with
poor emotion discrimination and labeling. This highlights the
neuroantomical and functional inter-relatedness of these do-
mains (Damasio, 1994 ; Oschner & Barrett, 2001 ; Phillips
et al., 2003 ). This relationship did not extend to self-reported
trait impulsiveness, which was related to inhibitory control
but not emotion recognition. Trait impulsivity may measure a
facet of impulsivity that is not relevant to emotion regulation.
In terms of limitations, we cannot exclude the possibility
that acoustic defi cits affected prosody perception, although
differential performance across tasks makes this unlikely.
Our sample of people with TBI was selected from those
manifesting social diffi culties during rehabilitation, so our
conclusions do not apply to the general TBI population.
Nonetheless, given that changes in social function are preva-
lent, seen in as many as 80% of adults years after their in-
juries (Brooks et al., 1986 ; Thomsen et al., 1984 ), our
fi ndings are likely to apply to a substantial proportion of
those with severe TBI. Indeed, the kinds of social problems
described of our TBI participants are typical, refl ecting
withdrawn, inert behavior, rigid thinking, garrulous disinhib-
ited social interactions, and/or general ineffi ciency processing
conversation (Hartley and Jensen, 1992 ; Lezak, 1978 ;
Thomsen, 1984 ). Self-reported defi cits should be treated
with caution as adults with TBI may have limited insight into
their behavior, although this should lead to an underestima-
tion of reported defi cits. The
diffi culties with prosody contributes to these defi cits awaits fur-
ther examination. Our group included some who had received
specifi c remediation of emotion perception which may have
affected our fi ndings although a re-analysis of the data without
these four participants did not alter the pattern of results.
In conclusion, we found an impairment of recognizing
emotional prosody may contribute to social skills defi cits
many years following a TBI. Automatic discrimination of
emotional prosody was impaired, although not abnormally
so, while additional effortful accessing of semantic memory
led to signifi cantly impaired performance in at least half the
group. Our results did not support our hypothesis that the
dual demands of processing the “what” and “ how” in vocal
speech underpins poor performance. Indeed, the participants
in this study relied upon the “what” to recognize vocal emo-
tion. Without this, they were signifi cantly impaired, suggest-
ing problems processing emotional prosody per se.
Differences between emotion types suggest that manipu-
lating salience of prosodic cues may be a way to improve
vocal emotion recognition.
extent to which
This research was supported by a project grant from the National
Health & Medical Research Council of Australia. We express our
gratitude to people with traumatic brain injuries who participated in
the studies reported here as well as to our community control par-
ticipants who gave willingly of their time. The authors have no
competing or confl icts of interest to report.
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