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Neuropsychology 2004, Vol. 18, No.

3, 572579

Copyright 2004 by the American Psychological Association 0894-4105/04/$12.00 DOI: 10.1037/0894-4105.18.3.572

Social Perception Decits After Traumatic Brain Injury: Interaction Between Emotion Recognition, Mentalizing Ability, and Social Communication
Skye McDonald and Sharon Flanagan
University of New South Wales
Thirty-four adults with severe traumatic brain injuries (TBI) and 34 matched control participants were asked to interpret videotaped conversational exchanges. Study participants were asked to judge the speakers emotions, the speakers beliefs (rst-order theory of mind), what the speakers intended their conversational partners to believe (second-order theory of mind), and what they meant by remarks that were sincere or literally untrue (i.e., a lie or sarcastic retort). The TBI group had marked difculty judging most facets of social information. They could recognize speaker beliefs only when this information was explicitly provided. In general, emotion recognition and rst-order theory of mind judgments were not related to the ability to understand social (conversational) inference, whereas second-order theory of mind judgments were related to that ability.

Severe traumatic brain injuries (TBI) result in signicantly impaired social functioning (Ponsford, Olver, & Curran, 1995; Tate, Lulham, Broe, Strettles, & Pfaff, 1989; Weddell, Oddy, & Jenkins, 1980). Such injuries typically produce lesions concentrated in the frontal and temporal lobes of the brain (Adams et al., 1985; Levin et al., 1987), with attendant diffuse axonal damage (Adams et al., 1989). Consistent with these effects are welldocumented sequelae of TBI: disorders of attention, executive functioning, and memory and information processing (e.g., Tate, Fenelon, Manning, & Hunter, 1991). Although such neuropsychological consequences of TBI are strongly related to poor social outcomes (Bond, 1975, 1976; Tate et al., 1991; Vilkki et al., 1994), traditional approaches to examining decits have been restricted to essentially nonsocial information. For example, although executive decits have been specically linked to poor social recovery in TBI (Tate et al., 1991; Tate & Broe, 1999; Vilkki et al., 1994), these decits are usually tested with tasks such as the Wisconsin Card Sorting Test (Heaton, Chelune, Talley, Kay, & Curtiss, 1993). Clearly, there is a need for more detailed examination of the ability of people with TBI to use explicitly social information, that is, to engage in effective social perception and social problem solving.

Skye McDonald and Sharon Flanagan, School of Psychology, University of New South Wales, Sydney, New South Wales, Australia. Skye McDonald is an author of and recipient of royalties from The Awareness of Social Inference Test, published by Thames Valley Test Company. This study was funded by an Australian Research Council (Discovery) Grant. We acknowledge Sally Hopkins, Tara Stern, Ingerith Martin, and Clare Saunders for their assistance in the collection of the data reported in this article. We are also indebted to the staff of the Royal Rehabilitation Centre in Ryde, New South Wales, and the Liverpool Brain Injury Unit in Liverpool, New South Wales, who assisted us with recruiting participants. Finally, we acknowledge the participants with traumatic brain injury and their families, as well as the healthy control participants, who gave willingly of their time to enable this study to proceed. Correspondence concerning this article should be addressed to Skye McDonald, School of Psychology, University of New South Wales, Sydney, New South Wales, 2052, Australia. E-mail: s.mcdonald@unsw.edu.au

Although relatively infrequently reported, an important nding is that many people with TBI have difculty recognizing emotions, particularly negative emotions, in facial expressions and/or tone of voice (Hopkins, Dywan, & Segalowitz, 2002; Jackson & Moffat, 1987; McDonald & Pearce, 1996; Milders, Fuchs, & Crawford, 2003; Prigatano & Pribram, 1982). Similar decits have also been found in individuals with localized damage in the ventralfrontal lobes (Hornack, Rolls, & Wade, 1996), as well as in those with specic amygdala damage (Broks et al., 1998; Cowland et al., 1996; Young, Hellawell, Van de Wal, & Johnson, 1996), who show differentially greater impairment for complex social emotions (e.g., guilt or admiration; Adolphs, Baron-Cohen, & Tranel, 2002). This combined evidence provides support for the contention that the amygdala and orbitofrontal cortex are part of a circuit that mediates emotion recognition (Adolphs, 2002). Although this circuit is vulnerable to TBI, there has been no research to date that has examined recognition of complex emotions and their relationship to basic emotion recognition in the TBI population. Decits in the ability to evaluate more broadly dened social information are also implicated in TBI. For example, theory of mind (ToM) judgments, that is, the ability to interpret the mental state of others, have been found to be impaired in adults with focal frontal lesions (Channon & Crawford, 2000; Happe, Malhi, & Checkley, 2001; Stone, Baron-Cohen, & Knight, 1998; Stuss, Gallup, & Alexander, 2001) and specic amygdala damage (Fine, Lumsden, & Blair, 2001; Stone, Baron-Cohen, Calder, Keane, & Young, 2003), ndings that suggest, again, a ventral frontallimbic system underlying such abilities (Stuss et al., 2001). ToM decits have also been reported in the TBI population, although results are mixed. Tasks have varied in complexity from forced-choice judgments of mental state based on photos of the eye region alone (Milders et al., 2003) to answering simple (Bara, Tirassa, & Zettin, 1997) and doubly recursive questions (Santoro & Spiers, 1994) about the thoughts of protagonists in scripted, videotaped vignettes. An important facet of ToM ability that has not been properly addressed in such studies is the extent to which people with TBI are able to make mental-state judgments based on the

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general demeanor of speakers, compared with the extent to which they are able to make such judgments based on explicit contextual knowledge about such mental states. The former skill is clearly related to other abilities to read the expression and demeanor of speakers, whereas the latter is, arguably, a reection of basic mentalizing abilities. At yet another level of social perception, adults with TBI have been found to have difculty inferring the intended meanings of verbal and nonverbal behavior when placed in context. Thus, people with TBI have been found to have difculty recognizing faux pas (Milders et al., 2003) and interpreting ambiguous advertisements (Pearce, McDonald, & Coltheart, 1998), sarcastic remarks (McDonald, 1992; McDonald & Pearce, 1996), and the nature of interpersonal relationships (Cicerone & Tanenbaum, 1997; Kendall, Shum, Halson, Bunning, & Teh, 1997; Van Horn, Levine, & Curtis, 1992). The mechanism underlying these social reasoning decits is unclear. On the one hand, it is possible that such difculties reect executive dysfunction secondary to frontal pathology, which in turn impairs the ability to infer abstract relations (Bechara, 2002). Efforts to nd correlations between social problem solving and conventional tests of executive function, however, have been only partially supported (Corrigan & Toomey, 1995; Dennis & Barnes, 1990; McDonald & Pearce, 1996; Turkstra, McDonald, & DePompei, 2001). On the other hand, no research to date has been conducted to examine the relationship between emotion processing, ToM decits, and social reasoning in the TBI population, despite their probable coexistence. This is a major shortcoming, because there is good reason to believe that both emotion processing and mentalizing ability are part and parcel of understanding social inference. For example, indirect conversational remarks such as sarcasm are typically associated with particular emotions such as derision or scorn (Sperber & Wilson, 1987). In addition, pivotal to the ability to make judgments about the intended meaning of literally untrue comments such as lies and sarcastic retorts is an ability to comprehend what different speakers know (Sullivan, Winner, & Hopeld, 1995). The detection of a lie relies on the ability to comprehend that one speaker knows the truth and the other does not. Sarcasm, on the other hand, occurs in the context in which both speakers know the truth. In summary, the extent to which different facets of social perception are disturbed in people with TBI and the extent to which each contributes to social understanding are unclear. In the current study, the relationship between these different aspects of social perception was explored in adults with severe TBI. The materials used in this study were taken from The Awareness of Social Inference Test (TASIT; McDonald, Flanagan, & Rollins, 2002). This test was developed to assess emotion recognition, ToM judgments, and social inference making as they occur in everyday settings. TASIT has alternative forms, has been tested on over 280 adults without brain damage, and produces uniformly high scores on all aspects of the test in the absence of brain damage. In contrast, it is sensitive to decits following acute TBI (McDonald, Flanagan, Rollins, & Kinch, 2003) and also predictive of real-world difculties with social encounters (McDonald, Flana-

gan, Martin, & Saunders, in press). However, the relationship between emotion recognition, ToM, and social reasoning has not yet been examined. Part 1 of TASIT assesses recognition of basic emotions as depicted in videotaped vignettes. Parts 2 and 3 comprise videotaped dialogues in which sarcastic exchanges are contrasted with sincere exchanges (Part 2) and lies (Part 3). Within Parts 2 and 3, specic probe questions tap for understanding of the speakers emotional state (focusing on subtle emotions such as annoyance, sympathy, and contempt), beliefs (i.e., rst-order ToM), and intentions (what they want their listeners to believe or feel; i.e., second-order ToM). A nal probe taps understanding of the meaning of the conversational remarks in question. Thus, the meaning of a sincere remark is the same as that literally asserted. The intended meaning of a lie is, similarly, what is literally asserted; that is, the speaker wants his or her comment to be taken at face value. The meaning of a sarcastic comment, on the other hand, is the opposite to that literally asserted. In Part 2 there is no information, apart from the demeanor of the actors, from which to gauge speaker beliefs. In Part 3 there are additional cues (in the form of prologues or visual edits) that make explicit what the speakers know to be true. These different components of TASIT enabled the following specic research questions to be addressed: 1. Are problems in basic emotion recognition following TBI related to problems understanding the more subtle emotions exhibited by speakers in conversational exchanges? 2. Can people with TBI infer what others believe (rst-order ToM) and what speakers intend listeners to believe (second-order ToM) (a) from their demeanor alone or (b) when explicit information is provided? 3. Are problems with emotion recognition and ToM associated with a general failure to understand social inference, specically the meaning of nonliteral conversational remarks, such as sarcasm?

Method Participants
Thirty-four adults (9 women and 25 men) between the ages of 21 and 64 years (M 41, SD 12) with severe TBI were recruited from the outpatient records of three metropolitan brain injury units in New South Wales, Australia, for this project. Participants were selected according to the following criteria: They had a severe TBI resulting in altered consciousness of 1 day or greater, were discharged from hospital and living in the community, were uent English speakers, did not have aphasia, and had normal sight and hearing. TASIT results for a proportion of these participants have also been reported in an independent study examining the ecological validity of TASIT (McDonald et al., in press). The mean length of posttraumatic amnesia was 76 days (SD 59), which was no different (one-sample t test) from the mean length of posttraumatic amnesia (81 days) reported in a consecutive series of 100 people with TBI who were discharged from a comparable brain-injury unit in an independent study (Tate et al., 1989). This nding indicates that this group was representative of the severity of injury typically seen in this population. All participants were tested 1 or more years after their brain injury (mean time postinjury 9 years, SD 8). As is typical of the TBI population, the group was characterized by heterogeneity of injuries sustained. Causes of injuries included motor vehicle accidents (22), falls (5), assaults (5), and work-related injuries (2). Pathology on initial admission

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Table 1 Mean Scores and Standard Deviations for TBI Participants Compared With Matched Control Participants on TASIT Part 1: Emotion Evaluation Test
Emotion Group and score Maximum score TBI group (n 34) M SD Control group (n 31) M SD Angry 4 2.6* 1.1 3.6 0.7 Disgusted 4 2.7* 1.2 3.6 0.6 Anxious 4 2.9* 1.1 3.6 0.8 Sad 4 2.7* 1.1 3.7 0.5 Surprised 4 3.1* 1.0 3.8 0.5 Happy 4 3.3* 0.9 3.6 0.6 Neutral 4 2.3* 0.9 3.1 0.8 Total 28 19.6* 4.7 25.0 2.3 .05).

Note. Asterisks indicate the TBI group was signicantly different from the matched control group ( p TBI traumatic brain injury; TASIT The Awareness of Social Inference Test.

included skull fractures (3), contusions (10), intracerebral or subarachnoid hemorrhages (13), subdural and extradural hemorrhages (4), and penetrating injuries (1). Six participants had reportedly left-focused injuries, 14 had right-focused injuries, and 10 had bilateral injuries. The injuries of 4 participants were not specied. Specic frontal-lobe lesions were reported in 17 participants. The initial evidence of cerebral pathology is only a crude measure of the nature and extent of injuries sustained, with many microscopic lesions and neuronal shearing undetectable with the clinical tools available at the time. Nevertheless, the preponderance of frontal-lobe lesions reported in these participants in the initial stages of their injuries is also typical for this group. On average, the TBI participants had achieved 13 years of education (ranging from 8 to 20 years). Two of the participants had been unemployed prior to their injuries. The remainder had been employed in occupations ranging from unskilled (6) to skilled trade or clerical (16), professional or managerial (7), or student (3). After their injuries, they experienced a signicant loss of employment status. At the time of recruitment, 27 participants were either unemployed or working as volunteers. Only 2 participants had maintained jobs in professional or clerical areas, whereas 3 had found work as unskilled workers, and 2 were students. This drop to approximately 20% employed postinjury accords with estimates in independent-outcome studies (e.g., Brooks, Campsie, Symington, Beattie, & McKinlay, 1987; McMordie, Barker, & Paolo, 1990; Ponsford et al., 1995; Tate et al., 1989), suggesting, once again, that this group represents a prole not dissimilar to that of severe TBI outcome generally. A group of 34 adults without brain injuries, who were recruited from the general community with the assistance of various community organizations (e.g., sporting clubs, church groups, and police cadets) and matched on the basis of age, education, and gender, was also tested. This group comprised 12 women and 22 men whose mean age was 36 years (SD 13) and whose mean years of education was 13 (SD 3). There was no signicant difference between the TBI group and control group for either of these variables.

vignettes, the exchange is sincerely meant. In 5 vignettes similar scripts are enacted sarcastically; for example, in a sarcastic version of the above example the woman is clearly angry with her coworker, and although on the surface she is complimenting him, she is in fact implying that he has done very little.1 In the remaining 5 vignettes, the scripts are literally paradoxical; that is, they make sense only if it is understood that one person is being sarcastic. After viewing each vignette, participants were required to answer questions about the speakers feelings, beliefs, intentions, and meaning (later referred to as feel, think, intend, and mean questions, respectively). The questions for each vignette were carefully worded and pilot tested (McDonald et al., 2003) to be simple to understand and to avoid recursive, doubly embedded phrases. Part 3: Social InferenceEnriched (SIE) test. This part comprises 16 vignettes that provide additional information before or after the dialogue of interest to set the scene. For example, two coworkers conde to each other that a party on the weekend was truly dreadful. This is followed by a scene with the host of the party in which the coworkers claim the party was a great success. In half of the vignettes, the scripts are enacted as a diplomatic lie, that of trying to make the best of a bad situation. In the remainder, the scripts are enacted sarcastically. As in Part 2, ability to interpret the vignettes correctly is assessed via a set of four questions for each vignette. The three parts of TASIT have a combined playing time of approximately 35 min. In our study, each participant was tested individually. It was explained to the participant that he or she would be shown a video of some people interacting and that he or she would be asked questions about these interactions. Practice items preceded each section to familiarize the participant with the task requirements. The video was then paused after each vignette, and the participant was asked to respond to questions concerning the content of the video.

Results Overall Findings


TASIT Part 1: EET. The performance of the two groups on Part 1 of TASIT, the EET, is summarized in Table 1, indicating both overall performance and performance on each of the seven emotions. For Part 1, data were not available for 4 control participants, so the group comprised 31 participants. A repeated measures analysis of variance (ANOVA) was used
1 Although a number of scripts in Parts 2 and 3 of TASIT appear twice, each alternate form (A or B) contains only one version of the script.

Materials and Procedure


Participants were tested on Parts 1, 2, and 3 of Form A of TASIT. Part 1: Emotion Evaluation Test (EET). This part comprises 28 vignettes in which a professional actor portrays one of seven basic emotional states (happy, sad, anxious, disgusted, surprised, angry, and neutral) while enacting a neutral script. Participants were required to decide which of the basic seven categories each emotional expression represented. Part 2: Social InferenceMinimal (SIM) test. This part comprises 15 vignettes that represent dialogues between two actors; for example, a woman complimenting a coworker on all the hard work he has done. In 5

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to reveal overall group differences. In general, the TBI participants performed less well than the control participants, F(1, 63) 34.72, p .01, and this pattern was true across all emotion categories; that is, there was no Group Emotion interaction. Emotion recognition was not signicantly associated with age or time postinjury. It was, however, signicantly associated with length of PTA (r 4.1, p .02). There was also a difference of 4.1 points between those TBI participants who were employed (n 7) versus those who were not (n 27), and it was signicant, t(18, 37) 3.07 (unequal variance), p .01. When the group was divided into participants with reported damage to the frontal lobes (n 17) and those without (n 13), emotion recognition was on average 3.3 points less in the group with anterior lesions, which was a marginally signicant difference, t(28) 1.96, p .06. There was no discernable difference between those with reportedly righthemisphere versus left-hemisphere pathology. TASIT Parts 2 and 3: Social Inference tests (SIM and SIE). The overall scores for Parts 2 (SIM) and 3 (SIE) are detailed in Table 2. Parts 2 and 3 are broken into their relevant subtests: Sincere, Simple Sarcasm, and Paradoxical Sarcasm (Part 2), and Lies and Sarcasm (Part 3). Repeated measures ANOVAs and post hoc tests were used to compare groups across the different subtests for each part. Overall, the TBI participants performed less well than the control participants on both Part 2, F(1, 66) 22.39, p .01, and Part 3, F(1, 66) 21.41, p .01. In both parts, however, there was a signicant interaction between group and subtest: Part 2, F(1, 65) 5.24, p .01; Part 3, F(1, 65) 3.97, p .05. As indicated in Table 2, TBI participants were no different from control participants in their capacity to comprehend sincere exchanges or lies. In contrast, and consistent with previous research (McDonald et al., 2003), TBI participants performed signicantly less well than their matched peers when judging what was meant by simple and paradoxical sarcastic exchanges. Performance on the Social Inference tests was not signicantly associated with age or time postinjury but was associated with length of PTA (SIM: r 4.0, p .02; SIE: r .4, p .02). Those who were unemployed postinjury scored more poorly on the SIE than those who were employed (difference 7.6), t(13,

23) 2.35 (unequal variance), p .01, but the difference on SIM was marginal (difference 5.4), t(12.11) 1.63, p .08. No differences were found on the basis of anterior versus posterior or right-hemisphere versus left-hemisphere pathology. There was signicant variability within the TBI group in terms of their performance on the three subtests of TASIT. Altogether, 19 of the 34 participants had difculty with one or more parts of TASIT. Ten produced abnormally poor scores relative to the control group on Part 1: EET; 11 were abnormally poor at judging sarcasm in Part 2: SIM; and 12 were abnormally poor at judging in Part 3: SIE. However, these generally were not the same people in each case; that is, only 4 participants had difculty with all three subtests. Probe questions. In Table 3, the average scores on the different types of probe questions for Parts 2 and 3 of TASIT are detailed. Individual t tests were used to make between-groups comparisons for each of the probe questions. The probability level was adjusted with the Bonferroni procedure to correct for the inated error rate associated with multiple comparisons. The TBI participants performed more poorly than control participants on all probe questions with the exception of think questions in Part 3. Once again, the TBI group was variable in its ability to answer the different types of questions. Eleven participants were in the normal range for all probe questions. Eight participants performed abnormally poorly on every type of probe question in Part 2, and 3 participants performed poorly on every type of question in Part 3. The remainder of the group had difculty on at least one of the questions. Overall, between 8 and 16 participants performed abnormally poorly on each probe question.

Relationship Between Ability to Judge Emotions (Part 1) and Ability to Answer Questions About Feelings (Parts 2 and 3)
To determine whether basic emotion recognition was related to the ability to recognize more subtle emotions, we entered TBI scores for all four probe questions for Parts 2 and 3 into two simultaneous linear regressions, respectively, with performance on Part 1 (EET) as the dependent variable in both. Feel questions in

Table 2 Mean Scores and Standard Deviations for TBI Participants Compared With Matched Control Participants on TASIT Parts 2 (SIM) and 3 (SIE)
Social InferenceMinimal (SIM) Group and score Maximum score TBI group (n 34) M SD Control group (n 34) M SD Sincere 20 15.7 3.4 16.1 2.6 Simple Sarcasm 20 14.2* 4.1 18.0 2.4 Paradoxical Sarcasm 20 16.0* 3.3 19.0 1.4 Total 60 45.9* 8.0 53.1 4.2 Social InferenceEnriched (SIE) Lies 32 24.6 4.9 27.0 3.3 Sarcasm 32 21.6* 5.7 26.9 4.1 Total 64 45.9* 7.4 53.9 6.0 .05).

Note. Asterisks indicate the TBI group was signicantly different from the matched control group (p TBI traumatic brain injury; TASIT The Awareness of Social Inference Test.

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Table 3 Mean Scores and Standard Deviations for Types of Probe Questions (Feel, Think, Intend, Mean) on TASIT Parts 2 (SIM) and 3 (SIE) for TBI Participants and Matched Control Participants
Social InferenceMinimal (SIM) Group and score Maximum score TBI group (n 34) M SD Control group (n 34) M SD Feel 15 11.8** 2.3 13.6 1.1 Think 15 10.8** 2.5 12.7 1.3 Intend 15 12.2** 1.9 13.4 1.2 Mean 15 11.1** 2.5 13.4 1.3 Social InferenceEnriched (SIE) Feel 16 11.4** 2.0 13.2 1.9 Think 16 12.7 2.0 13.5 1.4 Intend 16 11.1** 2.8 14.1 1.9 Mean 16 10.9** 2.5 12.9 2.0 .01).

Note. Asterisks indicate the TBI group was signicantly different from the matched control group ( p TBI traumatic brain injury; TASIT The Awareness of Social Inference Test.

Part 2 (SIM) were the only probe questions to make an independent contribution to scores on Part 1 ( .48), t 2.38, p .02. Of interest, feel questions on Part 3 (SIE) were not independently associated with Part 1. Rather, think questions made a unique contribution ( .61), t 3.20, p .01, suggesting that those who were good at judging simple emotions were also able to make simple judgments about what the speakers were thinking when given explicit contextual information.

difculties interpreting the mean questions that were over and above those related to problems with understanding emotion, beliefs, or intentions. For Part 3, poor performance on the intend .53, p .01) and feel ( .35, p .01) questions ( signicantly predicted poor performance on the mean questions. There was no effect of TBI over and above these decits.

Discussion Ability to Make ToM Judgments on the Basis of Demeanor With and Without Additional Context
A repeated measures ANOVA comparing percentage of correct responses on think (rst-order ToM) questions in Part 3 to those in Part 2 revealed a Group Part interaction, F(1, 63) 4.48, p .04. That is, the TBI group had more difculty with think questions when they made such judgments on the basis of the actors demeanor alone (Part 2) than when they were given additional contextual cues (Part 3). Control participants were equally good at both. A second ANOVA contrasting intend (second-order ToM) questions across Parts 2 and 3 revealed another signicant Group Part interaction, F(1, 63) 9.27, p .01. However, the pattern was in the reverse direction of that predicted. People with TBI found the intend questions in Part 3 more difcult than those in Part 2. On average, the people with TBI in this study had signicant difculty with social perception. As a group they were generally unimpaired in their ability to interpret the meaning of comments that were meant to be taken literally (i.e., sincere remarks and lies), but they demonstrated signicant impairments when required to infer the meaning of interpersonal exchanges between people that encompassed nonliteral (i.e., sarcastic) remarks. They also demonstrated signicant impairments in the ability to recognize the emotional and mental state of others. Although group differences were clear, the TBI group was characterized by variability. Indeed, relative to their peers, about 30% of the TBI participants experienced abnormal levels of difculty judging emotional expressions in face and voice and difculties understanding the meaning behind conversational remarks. The remainder was in the normal range. Length of PTA and postinjury employment status were associated with decits in all parts of TASIT, and the more severely injured had the greatest decits. Nevertheless, TBI did not have a uniform impact on social perception skills. Some people had particular difculties recognizing basic emotional expression but not conversational inference, and vice versa. These dissociations across the different types of tasks are consistent with the heterogenous nature of TBI in terms of pathology and neuropsychological decit. They also reinforce the notion that social perception relies on a variety of different abilities. Division of the group according to anterior and posterior pathology suggested that frontal pathology is more likely to result in emotion decits, but no such distinction was found for social inference. This analysis was, however, based on crude estimations of initial neuropathology, so further investigations using more sophisticated imaging techniques are required to examine these relationships more accurately.

Contribution of Emotion Recognition and ToM Ability to Understanding Conversational Meaning


To examine the relationship between emotion recognition, mentalizing ability, and conversational meaning, we entered scores on feeling and ToM (think and intend) probes into two simultaneous linear regressions for Parts 2 and 3, respectively, along with group membership. Total scores on the appropriate mean probe questions were entered as the dependent variable. Combinations of these variables were signicant predictors in both cases: Part 2, adjusted R2 .71, F(4, 63) 41.92, p .01; Part 3, adjusted R2 .60, F(4, 62) 25.94, p .01. For Part 2, the ability to answer intend questions signicantly predicted answers on mean questions ( .51, p .01). The presence of TBI was also an independent predictor ( .18, p .02), suggesting that the TBI group had

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Emotion Recognition for Basic and More Subtle Emotions


Within Part 1, it was found that people with TBI had difculty recognizing all basic emotional categories. This nding differs from previous reports, in which particular impairments with negative emotions have been reported (Hopkins et al., 2002; Jackson & Moffat, 1987; McDonald et al., 2003), but it does not preclude the possibility of differential impairment. Indeed, only 3 of the adults with TBI had abnormally low scores on the happy faces, whereas 15 of the TBI participants were abnormally poor at judging disgust. The ability to recognize basic emotions in Part 1 of TASIT was uniquely related to the ability to recognize more subtle social emotions in the conversational exchanges of Part 2, suggesting a common system underlying the two. This was not the case for Part 3, which required judgments of behavior that were based on a complex interplay of information. Under these circumstances, the interpretation of the speakers feelings appears to have required more than the simple recognition of basic emotional displays.

ToM Judgments With and Without Explicit Cues


The TBI participants were less able than control participants to judge speakers beliefs on the basis of the speakers demeanor (Part 2). This contrasts with the nding that people with severe TBI can make such judgments in a forced-choice paradigm that is focused on the eyes alone (Milders et al., 2003). Clearly, it is important to examine such skills under a range of conditions. Using the naturalistic stimuli of TASIT, we found that 14 of the 34 participants had scores that were abnormally low relative to the control groups performance. The TBI group improved signicantly when information in the form of a prologue or a visual edit made the speakers beliefs explicit (Part 3), although 8 of the 34 TBI participants still had abnormally low scores, suggesting additional problems with basic ToM judgments. More complex (second-order) ToM judgments about what one speaker wants another speaker to feel or believe were consistently performed poorly by the TBI group in Part 2 and even more poorly in Part 3. The ability to recognize basic emotions was neither sufcient nor necessary for complex ToM ability, although the contribution of complex emotion recognition was not examined. In addition, rst-order ToM judgments appeared to be unhelpful to complex ToM judgments because, when the beliefs of the speakers were made explicit (Part 3), participants with TBI were actually poorer at judging speaker intention than when the speakers beliefs were not made explicit (Part 2). This pattern suggests two possible explanations: Judging a speakers intentions is a mentalizing ability qualitatively different from that encompassed in basic ToM. Alternatively, it calls into play cognitive abilities other than mentalizing, for example, more general inference-making abilities.

those arising from the speakers demeanor (Part 2), the ability to interpret speakers intentions (second-order ToM) was closely associated with the ability to understand their meaning. The ability to understand either basic or complex emotions did not make an independent contribution, nor did rst-order ToM. On the other hand, there was evidence that people with TBI had some additional cognitive difculties underlying their failure to understand conversational inference. Possible contributors include information processing speed and working memory, both frequently impaired in TBI and both likely to impact the ability to make decisions regarding social information presented in video format (i.e., online). When extra contextual cues were provided that made explicit what speakers knew to be true (Part 3), TBI participants ability to interpret both the speakers feelings and intentions was related to the ability to understand what their remarks meant. Again, simply understanding what speakers believed was not as important, nor was the ability to understand basic emotions (Part 1). The reason that social emotions were important in Part 3 can only be speculated. It is possible that in the context of having clear information about what speakers believe but not what they intend, the ability to recognize subtle emotional states becomes important to override expectations based on the beliefs expressed. For example, if in a private conversation a speaker clearly expresses the belief that the boss will be angry about a work car being damaged, he or she sets up an expectation that this belief will be transmitted to the guilty party. Thus, when that same speaker utters the literally untrue comment, I am sure the boss will understand (either as a kind lie or as a sarcastic joke), the accurate interpretation of this comment is critically dependent on the listeners ability to gauge the speakers mood and attitude. In summary, in both Part 2 and Part 3 social inference making was closely associated with being able to guess the speakers intentions. The ability to estimate what different interactants in the exchange were thinking had relatively less to do with understanding social inference. The ability to judge either basic or more sophisticated social emotions was not independently important, except in situations in which the beliefs of the interactants were explicit, clearly setting up an expectation that later dialogue transgressed.

Conclusions
This study has revealed social perception decits in a signicant proportion of people with severe TBI, including decits in understanding basic emotions, subtle emotions, speakers beliefs and intentions, and the meaning of conversational inference. Although there was weak evidence for a role of frontal pathology in producing emotion (but not inferencing) decits, there is a need for better examination of the neuropathological correlates of these decits in people with TBI. Speaker intentions were closely linked to the ability to understand conversational inference. The remaining decits, although to some extent coexisting, clearly represented separate domains of abilities. Despite the importance of such abilities for normal social functioning, they have received relatively little attention in the research literature to date. Given the prevalence of psychosocial

Contribution of Emotion Recognition and ToM to Conversational Meaning


A major issue that was addressed in this study was the extent to which poor appraisal of emotional states and poor ToM abilities following TBI underpin failures to interpret conversational inference. When the only cues in the conversational exchange were

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MCDONALD AND FLANAGAN Hopkins, M. J., Dywan, J., & Segalowitz, S. J. (2002). Altered electrodermal response to facial expression after closed head injury. Brain Injury, 16, 245257. Hornack, J., Rolls, E. T., & Wade, D. (1996). Face and voice expression identication in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia, 34, 247261. Jackson, H. F., & Moffat, N. J. (1987). Impaired emotional recognition following severe head injury. Cortex, 23, 293300. Kendall, E., Shum, D., Halson, D., Bunning, S., & Teh, M. (1997). The assessment of social problem solving ability following traumatic brain injury. Journal of Head Trauma Rehabilitation, 12, 68 78. Levin, H. S., Amparo, E., Eisenberg, H. M., Williams, D. H., High, W. M., Jr., McArdle, C. B., & Weiner, R. L. (1987). Magnetic resonance imaging and computerized tomography in relation to the neurobehavioral sequelae of mild and moderate head injuries. Journal of Neurosurgery, 66, 706 713. McDonald, S. (1992). Differential pragmatic language loss following closed head injury: Ability to comprehend conversational implicature. Applied Psycholinguistics, 13, 295312. McDonald, S., Flanagan, S., Martin, I., & Saunders, C. (in press). The ecological validity of TASIT: A test of social perception. Neuropsychological Rehabilitation. McDonald, S., Flanagan, S., & Rollins, J. (2002). The Awareness of Social Inference Test. Bury St Edmonds, United Kingdom: Thames Valley Test Company. McDonald, S., Flanagan, S., Rollins, J., & Kinch, J. (2003). TASIT: A new clinical tool for assessing social perception after traumatic brain injury. Journal of Head Trauma Rehabilitation, 18, 219 238. McDonald, S., & Pearce, S. (1996). Clinical insights into pragmatic language theory: The case of sarcasm. Brain and Language, 53, 81104. McMordie, W. R., Barker, S. L., & Paolo, T. M. (1990). Return to work (RTW) after head injury. Brain Injury, 4, 5790. Milders, M., Fuchs, S., & Crawford, J. R. (2003). Neuropsychological impairments and changes in emotional and social behaviour following severe traumatic brain injury. Journal of Clinical & Experimental Neuropsychology, 25, 157172. Pearce, S., McDonald, S., & Coltheart, M. (1998). Ability to process ambiguous advertisements after frontal lobe damage. Brain and Cognition, 38, 150 164. Ponsford, J. L., Olver, J. H., & Curran, C. (1995). A prole of outcome: 2 years after traumatic brain injury. Brain Injury, 9, 110. Prigatano, G. P., & Pribram, K. H. (1982). Perception and memory of facial affect following brain injury. Perceptual and Motor Skills, 54, 859 869. Santoro, J., & Spiers, M. (1994). Social cognitive factors in brain injury associated with personality change. Brain Injury, 8, 265276. Sperber, D., & Wilson, D. (1987). Precis of Relevance: Communication and Cognition. Behavioural and Brain Sciences, 10, 697754. Stone, V. E., Baron-Cohen, S., Calder, A., Keane, J., & Young, A. (2003). Acquired theory of mind impairments in individuals with bilateral amygdala lesions. Neuropsychologia, 41, 209 220. Stone, V. E., Baron-Cohen, S., & Knight, R. T. (1998). Frontal lobe contributions to theory of mind. Journal of Cognitive Neuroscience, 10, 640 656. Stuss, D. T., Gallup, G. G., Jr., & Alexander, M. P. (2001). The frontal lobes are necessary for theory of mind. Brain, 124, 279 286. Sullivan, K., Winner, E., & Hopeld, N. (1995). How children tell a lie from a joke: The role of second order mental attributions. British Journal of Developmental Psychology, 13, 191204. Tate, R. L., & Broe, G. A. (1999). Psychosocial adjustment after traumatic brain injury: What are the important variables? Psychological Medicine, 29, 713725.

dysfunction in this population, there is clearly a need for greater investigation of the cognitive mechanisms underlying these fundamental human abilities.

References
Adams, J. H., Doyle, D., Ford, I., Gennarelli, T. A., Graham, D. I., & McLellan, D. R. (1989). Diffuse axonal injury in head injury: Denition, diagnosis and grading. Histopathology, 15, 49 59. Adams, J. H., Doyle, D., Graham, D. I., Lawrence, A. E., McLellan, D. R., Gennarelli, T. A., et al. (1985). The contusion index: A reappraisal in human and experimental nonmissile head injury. Neuropathology & Applied Neurobiology, 11, 299 308. Adolphs, R. (2002). Neural systems for recognizing emotion. Current Opinion in Neurobiology, 12, 169 177. Adolphs, R., Baron-Cohen, S., & Tranel, D. (2002). Impaired recognition of social emotions following amygdala damage. Journal of Cognitive Neuroscience, 14, 1264 1274. Bara, B. G., Tirassa, M., & Zettin, M. (1997). Neuropsychological constraints on formal theories of dialogue. Brain and Language, 59, 7 49. Bechara, A. (2002). The neurology of social cognition. Brain, 125, 1673 1675. Bond, M. R. (1975). Assessment of the psychosocial outcome after severe head injury. Paper presented at the Outcome of Severe Damage to the Central Nervous System: CIBA Foundation Symposium 34, Amsterdam, the Netherlands. Bond, M. R. (1976). Assessment of the psychosocial outcome of severe head injury. Acta Neurochirurgica, 34, 5770. Broks, P., Young, A. W., Maratos, E., Coffey, P. J., Calder, A. J., Isaac, C. L., et al. (1998). Face processing impairments after encephalitis: Amygdala damage and recognition of fear. Neuropsychologia, 36, 59 70. Brooks, N., Campsie, L., Symington, C., Beattie, A., & McKinlay, W. (1987). The effects of severe head injury on patient and relative within seven years of injury. Journal of Head Trauma Rehabilitation, 2, 113. Channon, S., & Crawford, S. (2000). The effects of anterior lesions on performance on a story comprehension test: Left anterior impairment on a theory of mind-type task. Neuropsychologia, 38, 1006 1017. Cicerone, K. D., & Tanenbaum, L. N. (1997). Disturbance of social cognition after traumatic orbitofrontal brain injury. Archives of Clinical Neuropsychology, 12, 173188. Corrigan, P. W., & Toomey, R. (1995). Interpersonal problem solving and information processing in schizophrenia. Schizophrenia Bulletin, 21, 395 403. Cowland, A. J., Young, A. W., Rowland, D., Perrett, D. I., Hodges, J. R., & Etcoff, N. L. (1996). Facial emotion after bilateral amygdala damage: Differentially severe impairment of fear. Cognitive Neuropsychology, 13, 699 745. Dennis, M., & Barnes, M. A. (1990). Knowing the meaning, getting the point, bridging the gap, and carrying the message: Aspects of discourse following closed head injury in childhood and adolescence. Brain and Language, 39, 428 446. Fine, C., Lumsden, J., & Blair, R. J. R. (2001). Dissociation between theory of mind and executive functions in a patient with early left amygdala damage. Brain, 124, 287298. Happe, F., Malhi, G. S., & Checkley, S. (2001). Acquired mind-blindness following frontal lobe surgery? A single case study of impaired theory of mind in a patient treated with stereotactic anterior capsulotomy. Neuropsychologia, 39, 8390. Heaton, R. K., Chelune, G. J., Talley, J. L., Kay, G. G., & Curtiss, G. (1993). Wisconsin Card Sorting Test manual: Revised and expanded. Odessa, FL: Psychological Assessment Resources.

SOCIAL PERCEPTION DEFICITS AFTER TBI Tate, R. L., Fenelon, B., Manning, M. L., & Hunter, M. (1991). Patterns of neuropsychological impairment after severe blunt head injury. Journal of Nervous and Mental Disease, 179, 117126. Tate, R. L., Lulham, J., Broe, T., Strettles, B., & Pfaff, A. (1989). Psychosocial outcome for the survivors of severe blunt head injury: The results from a consecutive series of 100 patients. Journal of Neurology, Neurosurgery and Psychiatry, 52, 1128 1134. Turkstra, L., McDonald, S., & DePompei, R. (2001). Social information processing in adolescents: Data from normally-developing adolescents and preliminary data from their peers with traumatic brain injury. Journal of Head Trauma Rehabilitation, 16, 469 483. Van Horn, K. R., Levine, M. J., & Curtis, C. L. (1992). Developmental levels of social cognition in head injury patients. Brain Injury, 6, 1528.

579

Vilkki, J., Ahola, K., Holst, P., Ohman, J., Servo, A., & Heiskanen, O. (1994). Prediction of psychosocial recovery after head injury with cognitive tests and neurobehavioural ratings. Journal of Clinical & Experimental Neuropsychology, 16, 325338. Weddell, R., Oddy, M., & Jenkins, D. (1980). Social adjustment after rehabilitation: A two-year follow-up of patients with severe head injury. Psychological Medicine, 10, 257263. Young, A. W., Hellawell, D. J., Van de Wal, C., & Johnson, M. (1996). Facial expression processing after amygdalotomy. Neuropsychologia, 34, 3139.

Received March 11, 2003 Revision received August 8, 2003 Accepted September 24, 2003