Affective empathy

Affective empathy refers to the ability to emotionally resonate with others’ feelings while understanding that they are distinct from one's own (Baron-Cohen & Wheelwright, Reference Baron-Cohen and Wheelwright2004). Using self-report measures such as the Balanced Emotional Empathy Scale (Mehrabian, Reference Mehrabian2000), 60–70% of adults with severe TBI self-report little to no emotional empathy compared to 30% of matched control participants (de Sousa, McDonald, & Rushby, Reference de Sousa, McDonald and Rushby2012; de Sousa et al., Reference de Sousa, McDonald, Rushby, Li, Dimoska and James2010, Reference de Sousa, McDonald, Rushby, Li, Dimoska and James2011; Williams & Wood, Reference Williams and Wood2010; Wood & Williams, Reference Wood and Williams2008). The use of self-report measures has been criticized in TBI research as these are vulnerable to loss of insight, attentional bias and cognitive impairments affecting complex language processing, attention and flexibility. Despite this, evidence suggests they can be a valid measure of emotional changes following even severe TBI (Kinsella, Moran, Ford, & Ponsford, Reference Kinsella, Moran, Ford and Ponsford1988). Furthermore, the relatively similar incidence rates using self-report across studies gives validity to the claim that empathy is reduced after TBI. Self-reported empathy is unrelated to injury severity (length of post-traumatic amnesia), time since injury or co-existing cognitive deficits (Williams & Wood, Reference Williams and Wood2010; Wood & Williams, Reference Wood and Williams2008) raising questions as to the cause of this self-perceived deficit. Emotional empathy is a complex construct entailing emotion perception, emotional resonance, self-awareness, and regulation. Consequently an examination of components may be more revealing as discussed below.

Facial emotion

Empirical research into emotion perception deficits following TBI commenced in the 1980s (Braun, Baribeau, Ethier, Daigneault, & Proulx, Reference Braun, Baribeau, Ethier, Daigneault and Proulx1989; Jackson & Moffatt, Reference Jackson and Moffat1987; Prigatano & Pribam, Reference Prigatano and Pribam1982) and since then, a plethora of studies have reported deficits in the recognition of photographs of facial expressions in adults with both acute and chronic severe TBI (Borgaro, Prigatano, Kwasnica, Alcott, & Cutter, Reference Borgaro, Prigatano, Kwasnica, Alcott and Cutter2004; Croker & McDonald, Reference Croker and McDonald2005; Green et al., Reference Green, Turner and Thompson2004; Ietswaart, Milders, Crawford, Currie, & Scott, Reference Ietswaart, Milders, Crawford, Currie and Scott2008; Knox & Douglas, Reference Knox and Douglas2009; McDonald & Saunders, Reference McDonald and Saunders2005; Milders, Fuchs, & Crawford, Reference Milders, Fuchs and Crawford2003; Milders, Ietswaart, Crawford, & Currie, Reference Milders, Ietswaart, Crawford and Currie2008; Spell & Frank, Reference Spell and Frank2000). While samples sizes in this area are typically small, a meta-analysis of 296 adults with moderate-severe TBI from 13 studies (Babbage et al., Reference Babbage, Yim, Zupan, Neumann, Tomita and Willer2011) indicated a relatively large effect size (1.1 SD) differentiating people with TBI from matched controls. Overall, it was estimated that up to 39% of people with severe TBI experience deficits in recognizing emotions from static presentations of facial expressions.

Static photographic stimuli bear little resemblance to naturally occurring facial expressions which are dynamic, evolve rapidly from one emotion to another and provide additional cues via facial movement (Bassili, Reference Bassili1978). Dissociations between recognition of static and dynamic expressions have been reported in patients with non-traumatic brain lesions (Adolphs, Tranel, & Damasio, Reference Adolphs, Tranel and Damasio2003; Humphrey, Donnelly, & Riddoch, Reference Humphrey, Donnelly and Riddoch1993) which suggests separable neural systems; ventral fronto-temporal systems mediating static images and dorsal fronto-parietal zones mediating facial movement (Adolphs et al., Reference Adolphs, Tranel and Damasio2003). As the ventral fronto-temporal lobes are especially vulnerable to TBI due to their position within the anterior and middle fossa (Bigler & Maxwell, 2011) disorders recognizing static expressions as a result of focal pathology may be expected to occur more frequently than disorders recognizing dynamic images. In one study that directly compared the two this was found to be the case, that is, 8/34 participants versus 1/34, respectively (McDonald & Saunders, Reference McDonald and Saunders2005).

Brain-behavior relationships are difficult to establish in TBI, in part because of the heterogeneity of the TBI population. Where subgroups have been compared, differences in emotion perception scores between those with frontal versus other pathology have been marginal or insignificant (Ietswaart et al., Reference Ietswaart, Milders, Crawford, Currie and Scott2008; McDonald & Flanagan, Reference McDonald and Flanagan2004). Other confounds complicate the picture. Slowed processing speed and poor cognitive flexibility interfere with emotion perception tasks, both static (Ietswaart et al., Reference Ietswaart, Milders, Crawford, Currie and Scott2008) and dynamic (McDonald & Saunders, Reference McDonald and Saunders2005) and, indeed, in one study (Ietswaart et al., Reference Ietswaart, Milders, Crawford, Currie and Scott2008) these entirely accounted for between group differences. Injury severity, indexing extent of cognitive impairment, also partially predicts poor performance (Ietswaart et al., Reference Ietswaart, Milders, Crawford, Currie and Scott2008; McDonald & Saunders, Reference McDonald and Saunders2005). Arguably, complex, dynamic display of emotions tax cognitive abilities more than static (Knox & Douglas, Reference Knox and Douglas2009) and certainly additional skills have been found to contribute to dynamic emotion recognition including premorbid intellectual ability, working memory, reasoning and new learning (McDonald et al., Reference McDonald, Bornhofen, Shum, Long, Saunders and Neulinger2006). While convergent evidence from various sources (as will be discussed below) suggests that impairment in facial emotion recognition is a real problem for many people with TBI, the correlation between indices of severity, various neuropsychological measures and behavioral responses to emotion identification does suggest that incidence figures are likely to be inflated.

Differential impairment in processing negatively valenced materials post TBI

The ventromedial frontal regions, amygdala and insula appear to be preferentially geared to rapidly orientate to and process threat related emotions (Adolphs, Reference Adolphs2002; Adolphs, Russell, & Tranel, Reference Adolphs, Russell and Tranel1999; Adolphs & Tranel, Reference Adolphs and Tranel2004; Graham, Devinsky, & LaBar, Reference Graham, Devinsky and LaBar2007; Harmer, Thilo, Rothwell, & Goodwin, Reference Harmer, Thilo, Rothwell and Goodwin2001; Phillips et al., Reference Phillips, Young, Senior, Brammer, Andrew, Calder and David1997; Sato et al., Reference Sato, Kubota, Okada, Murai, Yoshikawa and Sengoku2002). Differential impairment in the perception of negative expressions (fear, disgust, sadness, and anger) relative to positive is found in TBI studies (e.g., Braun et al., Reference Braun, Baribeau, Ethier, Daigneault and Proulx1989; Callahan, Ueda, Sakata, Plamondon, & Murai, Reference Callahan, Ueda, Sakata, Plamondon and Murai2011; Croker & McDonald, Reference Croker and McDonald2005; Dimoska et al., Reference Dimoska, McDonald, Pell, Tate and James2010; Hopkins, Dywan, & Segalowitz, Reference Hopkins, Dywan and Segalowitz2002; Jackson & Moffat, Reference Jackson and Moffat1987; McDonald, Flanagan, Rollins, & Kinch, Reference McDonald, Flanagan, Rollins and Kinch2003; Prigatano & Pribam, Reference Prigatano and Pribam1982). This could be construed as evidence for deficits to the ventromedial system although the pattern is not always seen (Ietswaart et al., Reference Ietswaart, Milders, Crawford, Currie and Scott2008; McDonald & Saunders, Reference McDonald and Saunders2005) so in these cases there must be more pervasive impairment or the contribution of other factors. Another consideration for both TBI research and more generally, is the uneven representation of positive [happy and sometimes (pleasant) surprise] and negative (angry, sad, fearful, disgust) emotions skewed further by the almost universal recognition of happy expressions. Thus, differential impairment in the recognition of negative expressions may reflect the nature of the materials rather than difficulties with particular categories of emotion per se. Evenso, throughout the psychological literature, there does appear to be a pattern whereby negative events are afforded preferential treatment over positive (Baumeister, Bratslavsky, Finkenauer, & Vohs, Reference Baumeister, Bratslavsky, Finkenauer and Vohs2001). Furthermore, other evidence (below) reinforces the view that processing of negative emotions is especially vulnerable to TBI.

Impaired physiological responsivity

Another feature of the ventromedial system is that it mediates autonomic responses to emotional stimuli even before conscious awareness (Phillips et al., Reference Phillips, Drevets, Rauch and Lane2003). This may also be compromised as a result of severe TBI. A minority self-report that their emotional experiences are dulled (Croker & McDonald, Reference Croker and McDonald2005; Hornak et al., Reference Hornak, Rolls and Wade1996) and many studies have reported reduced physiological reactivity to unpleasant stimuli, e.g., reduced modulation of the startle reflex (Sanchez-Navarro, Martınez-Selva, & Roma′n, Reference Sanchez-Navarro, Martınez-Selva and Roma′n2005; Saunders, McDonald, & Richardson, Reference Saunders, McDonald and Richardson2006), dampened skin conductance changes (arousal) and reduced facial reactivity when viewing affectively valenced pictures and films (de Sousa et al., Reference de Sousa, McDonald and Rushby2012, Reference de Sousa, McDonald, Rushby, Li, Dimoska and James2010; Soussignan, Ehrle, Henry, Schaal, & Bakchine, Reference Soussignan, Ehrle, Henry, Schaal and Bakchine2005). This has been reported for both positive and negative stimuli (de Sousa et al., Reference de Sousa, McDonald and Rushby2012; Sanchez-Navarro et al., Reference Sanchez-Navarro, Martınez-Selva and Roma′n2005; Soussignan et al., Reference Soussignan, Ehrle, Henry, Schaal and Bakchine2005) but also specifically to negative (Angrilli, Palomba, Cantagallo, Maietti, & Stegagno, Reference Angrilli, Palomba, Cantagallo, Maietti and Stegagno1999; de Sousa et al., Reference de Sousa, McDonald, Rushby, Li, Dimoska and James2010; Saunders et al., Reference Saunders, McDonald and Richardson2006). In some reports, changes in physiological responses to negative images corresponded to subjective reports that they did not find the stimuli arousing (de Sousa et al., Reference de Sousa, McDonald and Rushby2012, Reference de Sousa, McDonald, Rushby, Li, Dimoska and James2010; Saunders et al., Reference Saunders, McDonald and Richardson2006) although a dissociation between physiological changes and subjective report has also been reported (Sanchez-Navarro et al., Reference Sanchez-Navarro, Martınez-Selva and Roma′n2005; Soussignan et al., Reference Soussignan, Ehrle, Henry, Schaal and Bakchine2005).

Simulation following TBI

Simulation appears to be intrinsic to emotion perception. Adults typically demonstrate facial mimicry (Dimberg & Lundquist, Reference Dimberg and Lundquist1990; Dimberg & Petterson, Reference Dimberg and Petterson2000; Dimberg & Thunberg, Reference Dimberg and Thunberg1998), changes in skin conductance (Merckelbach, van Hout, van den Hout, & Mersch, Reference Merckelbach, van Hout, van den Hout and Mersch1989; Vrana & Gross, Reference Vrana and Gross2004) and subjective experience (Hess & Blairy, Reference Hess and Blairy2001; Wild, Erb, & Bartels, Reference Wild, Erb and Bartels2001) when viewing facial expressions. In turn, facial movements alter emotional experience (Adelman & Zajonc, 1989; Levenson et al., 1990) and the emotional state of the observer influences recognition of emotional states in others (Neidenthal, Brauer, Halberstadt, & Innes-Ker, Reference Neidenthal, Brauer, Halberstadt and Innes-Ker2001). At a neural level, the mirror neuron system in the premotor cortex is activated when viewing facial expressions (Carr, Iacoboni, Dubeau, Maxzziotta, & Lenzi, Reference Carr, Iacoboni, Dubeau, Maxzziotta and Lenzi2003; Kilts, Egan, Gideon, Ely, & Hoffman, Reference Kilts, Egan, Gideon, Ely and Hoffman2003). Activation of the somatosensory cortex also occurs, thought to provide the viewer with sensory cues “as if” the expression were their own (Adolphs, Damasio, Tranel, Cooper, & Damasio, Reference Adolphs, Damasio, Tranel, Cooper and Damasio2000) while autonomic changes reflect ventromedial activation.

In TBI, specific impairment in the early automatic mimicry of angry expressions relative to happy has been reported (McDonald, Li, et al., Reference McDonald, Li, De Sousa, Rushby, Dimoska, James and Tate2011) along with reduced skin conductance changes (Blair & Cipolotti, Reference Blair and Cipolotti2000; de la Plata et al., Reference de la Plata, Garces, Kojori, Grinnan, Krishnan, Pidikiti and Diaz-Arrastia2011; Hopkins et al., Reference Hopkins, Dywan and Segalowitz2002). Impairment is specific to angry expressions providing further evidence for differential impairment with negatively valenced emotions. It also discounts explanations based upon motor paralysis or deficits in mirroring, both of which should affect all emotions. It is consistent with an impairment of processing mediated by the ventromedial system.

Relation between simulation and emotion processes

Simulation is argued to be an implicit component of emotion recognition, providing cues that aid recognition (Goldman & Sripada, Reference Goldman and Sripada2005; Neidenthal et al., Reference Neidenthal, Brauer, Halberstadt and Innes-Ker2001). However, evidence for the simulation theory in TBI studies is weak. On the one hand, subjective reports of altered emotional experience after TBI do correlate with emotion perception accuracy (Croker & McDonald, Reference Croker and McDonald2005) and poor emotion perception and impaired emotional responses can co-occur in individual patients (Blair & Cipolotti, Reference Blair and Cipolotti2000). But, in general, correlations between mimicry and/or skin conductance and emotion perception have, to date, been insignificant (McDonald, Li, et al., Reference McDonald, Li, De Sousa, Rushby, Dimoska, James and Tate2011; McDonald, Rushby, et al., Reference McDonald, Rushby, Li, de Sousa, Dimoska, James and Togher2011). This lack of concordance is also seen in normal populations (Blairy, Herrera, & Hess, Reference Blairy, Herrera and Hess1999; Hess & Blairy, Reference Hess and Blairy2001) and casts doubt on the role of simulation in emotion perception. Simulation does, however, have a clearer role in empathy, providing both a vicarious empathic reaction (McIntosh, Reference McIntosh1996) and a communicative role, conveying an understanding of the situation. For example, mimicry has been found to vary systematically with the extent to which the participant knows s/he is being observed (Bavelas, Black, Chovil, Lemery, & Mullett, Reference Bavelas, Black, Chovil, Lemery and Mullett1988; Bavelas, Black, Lemery, & Mullett, Reference Bavelas, Black, Lemery and Mullett1986). There is evidence that impaired automatic mimicry is related to low emotional empathy in both people with TBI (de Sousa et al., Reference de Sousa, McDonald, Rushby, Li, Dimoska and James2011) and normal adults (Sonnby-Borgström, Jönsson, & Svensson, Reference Sonnby-Borgström, Jönsson and Svensson2003). Deficits in motor mimicry also extend to the capacity to make emotional expressions whether spontaneous or posed. This is not a motor impairment per se as happy expressions are normal (Dethier, Blairy, Rosenberg, & McDonald, Reference Dethier, Blairy, Rosenberg and McDonald2012).

Impairments in self-awareness and self-regulation

Self-awareness and self-regulation are necessary to emotional empathy so as to recognize one's own emotional experience, to see it as separate from the other and to control it effectively (Decety & Meyer, Reference Decety and Meyer2008). Self-awareness appears to be impaired in severe TBI although empirical evidence comes from a scattered, relatively small literature. People with severe TBI reportedly have impaired sensitivity to internal somatic states, specifically their own heartbeat (Hynes, Stone, & Kelso, Reference Hynes, Stone and Kelso2011). They also report less congruent mood changes when adopting a body posture consistent with an angry or sad emotional state compared to happy (Reference Dethier, Blairy, Rosenberg and McDonaldDethier, Blairy, Rosenberg, & McDonald, in press).

Poor self-awareness is also documented in studies of alexithymia., that is, difficulties identifying and describing one's emotions and physiological reactions. Using the Toronto Alexithymia Scale (Bagby, Parker, & Taylor, Reference Bagby, Parker and Taylor1994), between 32 and 58% of convenience samples of people with TBI self-report alexithymia (Allerdings & Alfano, Reference Allerdings and Alfano2001; Henry, Phillips, Crawford, Theodorou, & Summers, Reference Henry, Phillips, Crawford, Theodorou and Summers2006; Koponen et al., Reference Koponen, Taiminen, Honkalampi, Joukamaa, Viinamäki, Kurki and Tenovuo2005; McDonald, Rosenfeld, et al., Reference McDonald, Rosenfeld, Henry, Bornhofen, Tate and Togher2011; Williams et al., Reference Williams, Galas, Light, Pepper, Ryan, Kleinmann and Donovick2001; Wood & Williams, Reference Wood and Williams2007) compared to the much lower incidence in the general population (7–15%) (Koponen et al., Reference Koponen, Taiminen, Honkalampi, Joukamaa, Viinamäki, Kurki and Tenovuo2005; Pasini, Chiale, & Serpia, Reference Pasini, Chiale and Serpia1992). Furthermore, alexithymia post TBI is reportedly associated with empathy (Williams & Wood, Reference Williams and Wood2010). Although this is consistent with expectations based on theory, caution regarding the validity of the construct of alexithymia (literally “without words for emotions”) in the TBI population is required. Given its strong association with poor verbal and working memory capabilities (Wood & Williams, Reference Wood and Williams2007) it is not entirely clear what alexithymia represents in cognitively impaired people with TBI.

Loss of self-awareness is intrinsically related to self-regulation. Indeed, alexithymia and poor self-regulation are linked in many clinical populations (Connelly & Denney, Reference Connelly and Denney2007; Taylor, Bagby, & Parker, Reference Taylor, Bagby and Parker1997). Disorders of emotion regulation are common following TBI, manifest as apathy (disorder of drive) or poor frustration tolerance and disinhibition (disorders of control) (Kinsella et al., Reference Kinsella, Packer and Olver1991; Tate, Reference Tate1999) and these too, have been linked to both alexithymia (Koponen et al., Reference Koponen, Taiminen, Honkalampi, Joukamaa, Viinamäki, Kurki and Tenovuo2005) and empathy (de Sousa et al., Reference de Sousa, McDonald and Rushby2012) although, once again, the research is scant and preliminary.

Mood disorders

A major consideration for emotion processing in severe TBI is the prevalence of depression and anxiety (Bombardier et al., Reference Bombardier, Fann, Temkin, Esselman, Barber and Dikmen2010). In non-brain injured populations, depression impairs emotion perception (Langenecker et al., Reference Langenecker, Bieliauskas, Rapport, Zubieta, Wilde and Berent2005; Leppänen, Milders, Bell, Terriere, & Hietanen, Reference Leppänen, Milders, Bell, Terriere and Hietanen2004) and empathy (Cusi, MacQueen, Spreng, & McKinnon, Reference Cusi, MacQueen, Spreng and McKinnon2011) and has similarly altered brain circuits to those discussed in relation to TBI (Cusi, Nazarov, Holshausen, MacQueen, & McKinnon, Reference Cusi, Nazarov, Holshausen, MacQueen and McKinnon2012). Many TBI studies have addressed this confound by either matching groups for depression and anxiety or examining the contribution statistically. These found that mood disorders were not the major contributor to impairment in emotion perception (Ietswaart et al., Reference Ietswaart, Milders, Crawford, Currie and Scott2008; Milders et al., Reference Milders, Ietswaart, Crawford and Currie2008) or empathy (de Sousa et al., Reference de Sousa, McDonald, Rushby, Li, Dimoska and James2010; Wood & Williams, Reference Wood and Williams2008) although they were co-morbid with alexithymia (Wood & Williams, Reference Wood and Williams2007).

Overall, it is reasonable to conclude that deficits in emotion perception and empathy are a consequence of TBI. However, these are unlikely to be uniform, representing a complex admixture of impairment arising from structural lesions underpinning emotion processes, mood disorders, and cognitive impairments, overlaid upon pre-existing personality attributes. Future research may identify subtypes of emotion processing disorders in TBI but at this time, the evidence is too exploratory and the numbers too few.

Cognitive empathy

Cognitive empathy is normally assessed using self-report scales such as the Interpersonal Reactivity Scale (Davis, Reference Davis1983), the Empathy Scale (Hogan, Reference Hogan1969) and the Brock Adaptive Functioning Questionnaire (Hopkins et al., Reference Hopkins, Dywan and Segalowitz2002). Using these, individuals with TBI self-report lower cognitive empathy than do matched controls (de Sousa et al., Reference de Sousa, McDonald, Rushby, Li, Dimoska and James2010; Grattan & Eslinger, Reference Grattan and Eslinger1989; Wells, Dywan, & Dumas, Reference Wells, Dywan and Dumas2005). In these convenience samples (the study by Grattan & Eslinger had a mixed neurological group, including TBI), the incidence of impaired cognitive empathy was around 50% (de Sousa et al., Reference de Sousa, McDonald, Rushby, Li, Dimoska and James2010; Grattan & Eslinger, Reference Grattan and Eslinger1989) and was associated with high distress in care-givers (Wells et al., Reference Wells, Dywan and Dumas2005).

ToM tasks

ToM is conventionally measured using laboratory tasks, typically relying upon comprehension of stories, cartoons, photos and videos. Adults and children with severe TBI often fare poorly on these. In a recent meta-analysis based upon 173–354 adults with acquired brain injury, roughly 50% of whom had TBI, effect sizes for ToM tasks were moderate to large (0.5–0.7) and this was true for the TBI group alone (Martin-Rodriguez & Leon-Carrion, Reference Martin-Rodriguez and Leon-Carrion2010). Tasks include comprehension of complex stories that require knowing that one of the protagonists is operating on a false belief or has committed a faux pas (Bibby & McDonald, Reference Bibby and McDonald2005; Geraci, Surian, Ferraro, & Cantagallo, Reference Geraci, Surian, Ferraro and Cantagallo2010; Milders et al., Reference Milders, Fuchs and Crawford2003; Milders, Ietswaart, Crawford, & Currie, Reference Milders, Ietswaart, Crawford and Currie2006; Milders et al., Reference Milders, Ietswaart, Crawford and Currie2008; Spikman, Timmerman, Milders, Veenstra, & van der Naalt, Reference Spikman, Timmerman, Milders, Veenstra and van der Naalt2012; Stone, Baron-Cohen, & Knight, Reference Stone, Baron-Cohen and Knight1998; Turkstra, Williams, Tonks, & Frampton, Reference Turkstra, Williams, Tonks and Frampton2008), appreciating jokes based upon understanding the character's thoughts (Bibby & McDonald, Reference Bibby and McDonald2005; Milders et al., Reference Milders, Ietswaart, Crawford and Currie2006, Reference Milders, Ietswaart, Crawford and Currie2008; Spikman et al., Reference Spikman, Timmerman, Milders, Veenstra and van der Naalt2012), and predicting the intentions of characters in cartoon sequences (Havet-Thomassin, Allain, Etcharry-Bouyx, & Le Gall, Reference Havet-Thomassin, Allain, Etcharry-Bouyx and Le Gall2006; Muller et al., Reference Muller, Simion, Reviriego, Galera, Mazaux, Barat and Pierre-Alain2010). People with TBI also have difficulty making judgments about mental states based upon the eye region of the face (Geraci et al., Reference Geraci, Surian, Ferraro and Cantagallo2010; Havet-Thomassin et al., Reference Havet-Thomassin, Allain, Etcharry-Bouyx and Le Gall2006; Henry, Phillips, Crawford, Ietswaart, & Summers, Reference Henry, Phillips, Crawford, Ietswaart and Summers2006; Turkstra et al., Reference Turkstra, Williams, Tonks and Frampton2008) or deducing thoughts and intentions of speakers in video vignettes (McDonald & Flanagan, Reference McDonald and Flanagan2004; Turkstra, Dixon, & Baker, Reference Turkstra, Dixon and Baker2004).

Pragmatics

ToM plays a critical role in pragmatics, that is, language use. For example, when giving instructions, the speaker needs to think about the task from the listener's point of view and structure the explanation accordingly. When asking a favor they need to anticipate potential objections when framing their request. On occasion they may need to avoid offence by hinting what is on their mind. The incidence of aphasia post TBI is generally low (2–30% (Heilman, Safran, & Geschwind, Reference Heilman, Safran and Geschwind1971; Sarno, Reference Sarno1980, Reference Sarno1984, Reference Sarno1988; Sarno & Levita, Reference Sarno and Levita1986), yet 43% of mothers, when surveyed, reported language impairment (Kinsella et al., Reference Kinsella, Packer and Olver1991). This suggests there were additional difficulties using language effectively. In the absence of aphasia, difficulties with language use have also been documented on tasks that require tailoring responses to the listener's needs (McDonald, Reference McDonald1993; McDonald & Pearce, Reference McDonald and Pearce1995, Reference McDonald and Pearce1998; McDonald & Van Sommers, Reference McDonald and Van Sommers1993; Turkstra, McDonald, & Kaufmann, Reference Turkstra, McDonald and Kaufmann1996).

ToM is pivotal to comprehension of pragmatic inference. Speakers often allude to what they mean indirectly, or politely lie when diplomacy is required. Alternatively, they may assert the opposite to what they mean to ridicule or scorn (i.e., be sarcastic). To comprehend pragmatic inference, listeners need to impute what the speaker intends by their remarks from facial and body cues and also an understanding of the context. Children, adolescents and adults with severe TBI are reportedly poor at comprehending pragmatic inference in text and in videoed vignettes (Channon & Crawford, Reference Channon and Crawford2010; Channon, Pellijeff, & Rule, Reference Channon, Pellijeff and Rule2005; Dennis, Purvis, Barnes, Wilkinson, & Winner, Reference Dennis, Purvis, Barnes, Wilkinson and Winner2001; McDonald & Flanagan, Reference McDonald and Flanagan2004; McDonald et al., Reference McDonald, Flanagan, Rollins and Kinch2003; McDonald & Pearce, Reference McDonald and Pearce1996; Shamay-Tsoory, Tomer, & Aharon-Peretz, Reference Shamay-Tsoory, Tomer and Aharon-Peretz2005; Turkstra et al., Reference Turkstra, Dixon and Baker2004; Turkstra, McDonald, & DePompei, Reference Turkstra, McDonald and DePompei2001). In comparison to other ToM tasks, performances on pragmatic inference tasks yield the largest effect size (0.87) (Martin-Rodriguez & Leon-Carrion, Reference Martin-Rodriguez and Leon-Carrion2010). Furthermore, there is a significant relation between impairments in ToM, cognitive empathy and comprehension of sarcasm (Channon et al., Reference Channon, Pellijeff and Rule2005; McDonald & Flanagan, Reference McDonald and Flanagan2004; Shamay, Tomer, & Aharon-Peretz, Reference Shamay, Tomer and Aharon-Peretz2002). Other types of pragmatic communication have also been reported to be impaired, such as understanding inferred meanings in real-world ambiguous advertisements which rely upon a play on words (Pearce, McDonald, & Coltheart, Reference Pearce, McDonald and Coltheart1998), or making judgments about the social skills of conversational partners (such as whether they are able to share the conversation equally) (Turkstra et al., Reference Turkstra, Dixon and Baker2004). It is inevitable that language problems per se will compound difficulties with pragmatic inference. Most experimental tasks have control tasks with similar language demands but still reveal problems specific to pragmatic inference. Potentially more difficult to partial out, is the reliance of such tasks on working memory and information processing speed (McDonald et al., Reference McDonald, Bornhofen, Shum, Long, Saunders and Neulinger2006).

Relation between ToM and non-social reasoning

One approach to establishing modularity is to examine the association between ToM performance and standard neuropsychological tests. An inherent confound is that different ToM tasks (e.g., stories vs. photographs) rely differentially upon visual attention, language, etc. They also vary in complexity making disparate demands upon flexibility, working memory, learning and abstract reasoning, abilities that are often compromised as a result of TBI. Research samples are often small, making it even more difficult to find general patterns across studies. Unsurprisingly, evidence for the independence of ToM is mixed.

Several research studies have reported a lack of association between measures of cognitive processes, especially executive function and ToM (Havet-Thomassin et al., Reference Havet-Thomassin, Allain, Etcharry-Bouyx and Le Gall2006; Muller et al., Reference Muller, Simion, Reviriego, Galera, Mazaux, Barat and Pierre-Alain2010; Spikman et al., Reference Spikman, Timmerman, Milders, Veenstra and van der Naalt2012). However, this is not a universal finding and, indeed, individual measures of working memory, processing speed, inhibition and flexibility have been correlated with ToM performance (Bibby & McDonald, Reference Bibby and McDonald2005; Channon & Crawford, Reference Channon and Crawford2010; Dennis, Agostino, Roncadin, & Levin, Reference Dennis, Agostino, Roncadin and Levin2009; Havet-Thomassin et al., Reference Havet-Thomassin, Allain, Etcharry-Bouyx and Le Gall2006; Henry, Phillips, Crawford, Ietswaart, et al., Reference Henry, Phillips, Crawford, Ietswaart and Summers2006; Milders et al., Reference Milders, Ietswaart, Crawford and Currie2006; Turkstra, Reference Turkstra2008) and cognitive empathy (Grattan & Eslinger, Reference Grattan and Eslinger1989; Shamay-Tsoory, Tomer, Goldsher, Berger, & Aharon-Peretz, Reference Shamay-Tsoory, Tomer, Goldsher, Berger and Aharon-Peretz2004). The strength of associations that are reported also varies. In Dennis et al. (Reference Dennis, Agostino, Roncadin and Levin2009), a study of school aged children with TBI, it was concluded that poor ToM was entirely accounted for by cognitive inhibition and working memory deficits, that is, the ToM requirements were non-domain specific. On the other hand, Bibby and McDonald (Reference Bibby and McDonald2005) examining adults with severe TBI found that while simple first order ToM (i.e., understanding what a person thinks) was not reliant upon working memory and general inferencing capacity, more complex, second order ToM tasks (i.e., understanding what one person thinks about another person's thoughts) were, suggesting that the former may be tapping into a particular ToM impairment.

An alternative approach is to compare performance on a mental inference task with a similar task that requires non-mental inferences. Here too, results are equivocal, that is, both verbal and pictorial non-mental inference analogue tasks are frequently impaired (Bibby & McDonald, Reference Bibby and McDonald2005; Martin & McDonald, Reference Martin and McDonald2005; Milders et al., Reference Milders, Ietswaart, Crawford and Currie2006; Muller et al., Reference Muller, Simion, Reviriego, Galera, Mazaux, Barat and Pierre-Alain2010) although not always (Channon & Crawford, Reference Channon and Crawford2010; Milders et al., Reference Milders, Fuchs and Crawford2003; Muller et al., Reference Muller, Simion, Reviriego, Galera, Mazaux, Barat and Pierre-Alain2010). Failure on non-mental inferences does not preclude additional requirements in the ToM version of the task. The clearest way to reveal specific ToM deficits would be to statistically control for performance on non-mental inferencing when examining ToM performance. This is rarely reported but when it has been, it seems that much of the deficits in ToM tasks can be explained by similar deficits on other inference making tasks although, again, not for simple ToM (Bibby & McDonald, Reference Bibby and McDonald2005). In general, it would appear that there are common processes required for social and non-social tasks, depending upon the medium and response requirements (spoken, written, etc.), but there are unique requirements called into play when making ToM judgments.

Neural accounts

A recent approach to ToM is to use functional neuroimaging during simple tasks that require thinking about mental states. In healthy adults this paints a complex picture of composite processes (Frith & Frith, Reference Frith and Frith2010, Reference Frith and Frith2003; Schmitz, Rowley, Kawahara, & Johnson, Reference Schmitz, Rowley, Kawahara and Johnson2006). The temporo-parietal junction is activated (Castelli, Frith, Happé, & Frith, Reference Castelli, Frith, Happé and Frith2002) when viewing animated movement (such as when viewing light points attached to actors filmed in the dark; Heberlein, Adolphs, Tranel, & Damasio, Reference Heberlein, Adolphs, Tranel and Damasio2004) and people readily infer intention from such cues, even when viewing inanimate objects programmed to move and interact (Heider & Simmel, 1944). Greater activation occurs in the right temporo-parietal junction when oneself is agent (Decety & Meyer, Reference Decety and Meyer2008). The medial prefrontal cortex is consistently implicated in any task requiring the participant to think about themselves, regardless of its medium (verbal, visual, emotional, spatial) (Northoff et al., Reference Northoff, Heinzel, de Greck, Bermpohl, Dobrowolny and Panksepp2006) and also when thinking about others who are similar to self (Mitchell, Banaji, & Macrae, Reference Mitchell, Banaji and Macrae2005b) raising the specter of simulation, that is, self-reference, when understanding the mental state of others.

Posterior dorsal regions of the (especially left) medial prefrontal cortex, attributed to action monitoring and updating (Amodio & Frith, Reference Amodio and Frith2006) are engaged when considering psychological attributes (Mitchell, Banaji, & Macrae, Reference Mitchell, Banaji and Macrae2005a, Reference Mitchell, Banaji and Macrae2005b), especially from the viewpoint of a third person (D'Argembeau et al., Reference D'Argembeau, Ruby, Collette, Degueldre, Balteau, Luxen and Salmon2007). Inferior dorsolateral and orbitofrontal regions, known to play a role in inhibition of inappropriate responses (Collette et al., Reference Collette, Van der Linden, Delfiore, Degueldre, Luxen and Salmon2001; Nigg, Reference Nigg2001) are also activated when considering the perspective of another and may reflect the need to inhibit one's own perspective to do so (D'Argembeau et al., Reference D'Argembeau, Ruby, Collette, Degueldre, Balteau, Luxen and Salmon2007; Ruby & Decety, Reference Ruby and Decety2004). Finally, temporal pole activation (especially left) is common (D'Argembeau et al., Reference D'Argembeau, Ruby, Collette, Degueldre, Balteau, Luxen and Salmon2007; Frith & Frith, Reference Frith and Frith2003) possibly reflecting the role of semantic processing, autobiographical recall, etc., to place information in context. In all, neuroimaging research suggests that ToM engages numerous processes for attributing mental states, perspective taking and contextualization mediated by a neural network including ventromedial, dorsolateral, and orbital frontal lobes, the temporo-parietal junction and the temporal poles.

It might be assumed that a similar functional imaging approach would advance understanding of ToM abilities in TBI. Such studies have been undertaken (Newsome et al., Reference Newsome, Scheibel, Hanten, Chu, Steinberg, Hunter and Levin2010; Schmitz et al., Reference Schmitz, Rowley, Kawahara and Johnson2006; Schroeter, Ettrich, Menz, & Zysset, Reference Schroeter, Ettrich, Menz and Zysset2010) but their validity is questionable. They reveal a complex picture of impaired processes and compensatory activation that is difficult to unravel. Structural imaging in TBI, arguably, provides a clearer picture of brain-behavior relations. Shamay-Tsoory and colleagues have conducted several such studies, excluding patients with diffuse axonal injuries. They reported that, consistent with normal imaging, ToM deficits are especially severe following ventromedial lesions, although are also seen with extensive dorsolateral frontal pathology (Shamay-Tsoory & Aharon-Peretz, Reference Shamay-Tsoory and Aharon-Peretz2007; Shamay-Tsoory, Aharon-Peretz, & Perry, Reference Shamay-Tsoory, Aharon-Peretz and Perry2009; Shamay-Tsoory et al., Reference Shamay-Tsoory, Tomer and Aharon-Peretz2005). The extent to which these findings generalize, however, is limited by the exclusion of diffuse pathology, given its prevalence in severe TBI.

Finally, an interesting issue from both a conceptual and clinical perspective, is the extent to which deficits in cognitive versus emotional empathy occur independently. Dissociations have been reported after TBI (de Sousa et al., Reference de Sousa, McDonald, Rushby, Li, Dimoska and James2010; Eslinger, Satish, & Grattan, Reference Eslinger, Satish and Grattan1996) and neuroanatomically, there is argument for both overlap and potential dissociation. Both cognitive and affective empathy appear to recruit ventromedial frontal systems (Shamay-Tsoory et al., Reference Shamay-Tsoory, Tomer, Goldsher, Berger and Aharon-Peretz2004). Within the medial prefrontal cortex, cognitive processing of self and others appears to differentially engage ventral and dorsal regions while emotional resonance and empathy seems to rely upon the anterior cingulate and insula (Shamay-Tsoory, Reference Shamay-Tsoory2011) in combination with the amygdala (Carr et al., Reference Carr, Iacoboni, Dubeau, Maxzziotta and Lenzi2003; Phillips, Reference Phillips2003) and the mirror neuron system in the inferior frontal gyrus (Nummenmaa, Hirvonen, Parkkola, & Hietanen, Reference Nummenmaa, Hirvonen, Parkkola and Hietanen2008; Shamay-Tsoory et al., Reference Shamay-Tsoory, Aharon-Peretz and Perry2009).