Theory of Mind (ToM) refers to the ability to attribute mental states to self and others, including knowledge, beliefs and intentions (Premack and Woodruff, 1978
). Other researchers have also included understanding feelings within the definition of ToM (Shamay-Tsoory et al., 2005
). It is likely that ToM is a multidimensional process, requiring the integration of a number of components (Amodio and Frith, 2006
). One recent model (Shamay-Tsoory et al., 2010
; ) distinguishes cognitive from affective sub-processes of ToM. Cognitive ToM refers to the ability to make inferences about beliefs and motivations, while affective ToM refers to the ability to infer what a person is feeling. According to this model, cognitive ToM is a prerequisite for affective ToM, which also requires intact empathy processing (an ability to share and understand the emotional states of others; Singer et al., 2009
). Successful affective ToM processing, therefore, requires the integration of cognitive ToM and empathy. The first aim of the current study was to investigate the neural bases of cognitive and affective ToM using fMRI. Given recent evidence of continued development of the neural bases of ToM between adolescence and adulthood (Blakemore, 2008
), a second aim was to explore the nature of this development in more detail by including an adolescent comparison group and an affective ToM condition.
Fig. 1 The model of the relationship between cognitive ToM, affective ToM and empathy proposed by Shamay-Tsoory et al. (2010). Cognitive ToM is a prerequisite for affective ToM, which also requires cognitive and emotional (or affective) aspects of empathy. Figure (more ...)
fMRI studies exploring the neural bases of ToM have identified a network of regions that are commonly co-activated when participants are asked to think about their own or others’ mental states, including posterior superior temporal sulcus at the temporoparietal junction (pSTS/TPJ), temporal poles, precuneus and medial prefrontal cortex (mPFC) (Frith, 2007
). However, these studies have not explored the distinction between cognitive and affective ToM. A series of lesion studies by Shamay-Tsoory and colleagues (Shamay-Tsoory et al., 2005
; Shamay-Tsoory and Aharon-Peretz, 2007
) has shown that patients with lesions to ventromedial PFC (vmPFC) show impairment on ToM tasks involving an affective component (e.g. understanding the affective state behind an ironic remark), but do not show impairment on similar ToM tasks without an affective component (e.g. understanding the motivation behind an ironic remark in a non-affective context). Due to the fact that the lesions studied were not anatomically discrete, the reported damage in the vmPFC group extended well into both the medial and orbital PFC. Nevertheless, Shamay-Tsoory and Aharon-Peretz (2007)
note that the region of greatest damage in this sample was the ventral portion of the medial PFC. These findings support the view that vmPFC may be required for affective but not cognitive ToM. This is a plausible hypothesis given that this region is well placed to integrate cognitive and affective information due to its extensive connections with regions involved in affective processing including the amygdala, temporal pole and anterior insula (Shamay-Tsoory et al., 2006
). Basic emotional (or affective) processing such as emotion perception and recognition is not an explicit component of the Shamay-Tsoory model, but we would argue that it is necessary (although not sufficient) for empathy processes which contribute to successful affective ToM ().
Evidence from fMRI regarding the role of the vmPFC in affective ToM is currently mixed. Using drawings depicting emotional vs
neutral social scenarios, Krämer et al. (2009)
found activation in vmPFC [Tal: −3 38 −9]. Simply viewing social scenarios (two people) relative to a single person activated the typical ToM network (including a more dorsal region of mPFC), but did not activate vmPFC. However, this study did not explicitly require participants to mentalize; nor did it directly compare cognitive and affective ToM. In another study Völlm and colleagues compared the neural response during cartoons requiring cognitive ToM (understanding intentions) vs
cartoons requiring empathy (Völlm et al., 2006
). A conjunction analysis showed that both tasks activated the ToM network. The empathy condition activated mPFC (BA 10) to a greater extent than did the cognitive ToM condition; however, the peak of this activation fell in the dorsal portion of BA 10 [Tal: 9 53 14], and as such cannot truly be considered to be vmPFC.
The current study aimed to test several predictions arising from the model of cognitive and affective ToM put forward by Shamay-Tsoory et al. (2010)
. The use of fMRI with healthy participants allowed several predictions to be tested that are inaccessible to lesion methods. For example, the model predicts that cognitive and affective ToM should activate similar structures, but that affective ToM should additionally recruit regions hypothesized to integrate cognitive and affective information (including empathy processing) in order to predict outcomes (such as mPFC and vmPFC; Amodio and Frith, 2006
; Shamay-Tsoory et al., 2007
), as well as those subserving empathic responding [such as insula (Singer et al., 2009
) and amygdala (Völlm et al., 2006
)]. Testing these predictions in a sample of healthy participants was the first aim of the present study.
The second aim was to explore the development of cognitive and affective ToM between adolescence and adulthood. There is some behavioural evidence that the development of cognitive ToM precedes that of affective ToM. For example, while children can pass second-order false belief tasks (understanding what person A understands about what person B thinks) from the age of 6 or 7 years (Perner and Wimmer, 1985
), the ability to represent what person A understands about what person B feels (for example, in the understanding of social faux pas) appears later, between the ages of 9 and 11 years (Baron-Cohen et al., 1999
). Developmental fMRI studies further suggest that the neural substrates of ToM continue to develop during adolescence, long after children are able to perform complex cognitive and affective ToM tasks. For example, a meta-analysis by Blakemore (2008)
found that adolescents activated mPFC (BA 10) to a greater extent than did adults on a number of tasks requiring inferences about mental states: both cognitive ToM, e.g. understanding intentions (Blakemore et al., 2007
), and affective ToM, e.g. irony comprehension (Wang, et al., 2006
) and understanding social emotions (Burnett et al., 2009
). However, no previous fMRI study has explicitly looked at similarities and differences in the neural processing of cognitive and affective ToM between adolescence and adulthood. Therefore, it is unclear whether the previously observed differential activation of mPFC between adolescence and adulthood is attributable to late development of a process that is shared between cognitive and affective ToM, or whether it reflects particularly protracted development in regions subserving more complex ToM demands, requiring the integration of cognitive ToM with empathy processing.
The third aim of the present study was to explore the relationship between ToM and self-reported ability to empathize, since the model by Shamay-Tsoory et al. (2010)
suggests that affective ToM requires the integration of cognitive ToM and empathy. However, empathy is itself not a unitary construct, and there is considerable disagreement as to how the different dimensions of empathy should be defined. For the purposes of the present study, we explore potential relationships between cognitive and affective ToM, and cognitive and affective (or emotional) dimensions of empathy. We use the definitions of cognitive/affective empathy adopted by Jolliffe and Farrington's (2006)
Basic Empathy Scale (BES), with cognitive empathy defined as ‘understanding another's emotions’ and affective empathy as ‘affect congruence’, i.e. sharing another's emotions and being aware that the other person is the source of one's own affective state (de Vignemont and Singer, 2006
). In adopting these definitions, the BES attempts to avoid confusing cognitive empathy with perspective taking (taking another's point of view), and affective empathy with sympathy (concern for the target person). Since this scale has not been used previously in relation to ToM ability, we aimed to characterize potential relationships, particularly between empathy subscales and affective ToM.
The current study used a cartoon vignette paradigm with separate conditions for cognitive ToM, affective ToM and a physical causality control condition. This allowed neural responses to each ToM subtype (cognitive and affective) to be explored relative to a control condition that did not require mental state attribution (physical causality), as well as to each other. The cartoon paradigm, adapted from Völlm et al. (2006)
, was chosen because it makes few demands on reading ability. As discussed above, Völlm and colleagues originally investigated the distinction and overlap between neural responses to ToM vs
empathy. However, the cartoon scenarios used in the present study more closely followed the cognitive/affective ToM dichotomy as outlined by Shamay-Tsoory et al. (2010)
. Cognitive ToM cartoons required participants to understand beliefs or intentions, while affective ToM cartoons required participants to understand feelings, in order to select the appropriate story ending.
We tested only males for several reasons. First, although no previous studies have investigated the neural processing of cognitive vs
affective ToM in an adolescent group, several studies investigating ToM processing in adolescents exist, but some have focused on females only (e.g. Blakemore et al., 2007
; Burnett et al., 2009
). Therefore, more data on the development of this ability in males is needed. Second, differing trajectories of structural brain development between males and females during adolescence (Giedd et al., 1999
; Raznahan et al., 2010
) suggests that averaging results across both sexes might result in noisy data that are not representative of either sex. Finally, prominent conditions associated with difficulties in either cognitive or affective ToM (e.g. autism spectrum disorders and psychopathy) are more commonly reported in males (Blair et al., 2005
; Baird et al., 2006
). Data on typical neural circuitry underpinning these abilities in healthy males, therefore, provides a backdrop for potential future studies on disordered populations.
We predicted that, across all participants, cognitive and affective ToM cartoons would elicit responses in the ‘classic’ ToM network (pSTS/TPJ, precuneus, temporal poles, mPFC), but that affective ToM would be associated with a greater or additional response in regions integrating cognitive and affective information (mPFC and vmPFC) and those involved in basic affective processing (e.g. amygdala) and empathy (e.g. insula). We further predicted that developmental differences between adolescents and adults in the neural processing of ToM would be most pronounced for affective ToM, in line with previous behavioural evidence suggesting that affective ToM may develop later, and consistent with the Shamay-Tsoory model suggesting that affective ToM requires the integration of cognitive ToM and empathy. Finally, we conducted exploratory analyses to assess whether the neural processes associated with cognitive and affective ToM would be differentially related to cognitive and affective components of empathy as measured by self-report.