FMRI correlates of social emotion processing in both groups

5.4.1.1 Anterior rostral MPFC

Social emotions require a representation of the mental states of others (mentalising). That is, social emotions require insight into the emotions, beliefs and opinions of other people—whether they are physically present, imagined, or perhaps represented by the concept of societal norms (Moll, de Oliveira-Souza, et al., 2005; Moll, Zahn, et al., 2005). For example, guilt is experienced when one believes that one’s actions warrant disapproval or punishment, or that they have caused harm to another individual. In contrast, basic emotions such as ‘visceral’ fear and disgust entail a lesser degree of mentalising, since they only require insight into one’s own instantaneous internal state. In line with this distinction between social and basic emotions, the current study found that both age groups activated brain regions involved in mentalising, namely, the arMPFC and the pSTS/TPJ (Amodio & Frith, 2006; Frith & Frith, 2003; Saxe & Kanwisher, 2003), during social vs. basic emotion processing. In a recent review paper, Olsson and Ochsner (2008) have drawn attention to the partial overlap between brain regions involved in social cognition and in social emotion. The results of the current study concur with this picture.

Parts of the arMPFC, which has been identified as the portion of MPFC most consistently active in studies involving mental state attribution (MNI y-coordinates from 30 to 60; z-coordinates from 0 to 40; Amodio & Frith, 2006; Gilbert et al., 2006), were active in both groups for social vs. basic emotion. This result is

therefore in agreement with a large body of evidence. More narrowly, this result is in agreement with studies of social emotion in adults, which have reported activity

within the arMPFC (Takahashi et al., 2004; Berthoz et al., 2002; Moll et al., 20028).

This finding is consistent with the notion that a cognitive process, that is, mental state attribution, is involved in certain emotional tasks including imagining social emotion situations (cf. Olsson & Ochsner, 2008). This is not surprising, given the current stimuli were explicitly designed to maximise the difference in mentalising requirement between social and basic emotion conditions. The current pattern of results in arMPFC does not shed any light on the cognitive components of social emotional processing (see Poldrack, 2008, re. reverse inference). They do, however, support the notion that arMPFC is associated with mentalising in an emotional context, whereas many previous adult and developmental studies have focussed on mentalising in an unemotional context (e.g. den Ouden et al., 2005, Blakemore et al., 2007).

The implication of the current finding in arMPFC depends on what role the arMPFC plays in mentalising. It has been proposed that the cognitive role of arMPFC in mentalising is to ‘decouple mental states from physical reality’ (Frith, 2007). Recent evidence from Gilbert et al. (S. Gilbert, personal communication) supports this

notion9. An alternative, not necessarily incompatible view of the role of arMPFC is

that it represents the motivational relevance (Moll, de Oliveira-Souza, et al., 2005; Moll, Zahn, et al., 2005), the value (Rushworth et al., 2007) or changing action values (Matsumoto et al. 2007) of social behaviors. A broader conceptualization of the role of MPFC in general (not just the anterior rostral portion), which has just been put forward in the literature, is that this large region of the brain is concerned with representing ‘fuzzy’, inexact and shifting realities – including social information, which is highly context-dependent and mutable (Mitchell, 2009). The

8

Although see Moll et al. (2005a), who did not report activity in arMPFC during social/moral disgust (indignation) vs. basic visceral disgust

9

An fMRI study conducted by S. Gilbert et al. (personal communication) used a multivariate technique to map the representation of distinct mental states in arMPFC and other regions of the brain. Patterns of activity corresponding to distinct mental states could not be identified in arMPFC (although this region was generally activated during mentalising conditions). However, patterns of activity corresponding to distinct mental states could be identified in the medial temporal lobe. One explanation for this finding could be that the arMPFC enables

mentalising, drawing information on specific mental state representations from medial temporal regions of the brain.

current study was not designed to distinguish between these possibilities. However, a role for arMPFC in self-relevant social information, needed for social actions, would be consistent with the social vs. basic contrast in the current study.

An alternative explanation for the finding that arMPFC is more active in social than basic emotions, is that the social emotion condition is more engaging and evocative (see Mitchell, 2009). Although we found no evidence for higher emotion ratings in social than basic emotions (in fact, the opposite was found), self-rated emotion is a notoriously slippery and unreliable measure. This explanation, however, is also compatible with the notion that arMPFC is representing self-relevant social information, as this information is engaging. Clearly, further work is needed on the precise role of the arMPFC in social-emotional tasks, and implications for models of social cognitive functioning and emotion processing.

Finally, several previous studies have demonstrated activity within child and adolescent arMPFC during mentalising relative to control conditions (Blakemore et al., 2007; Moriguchi et al., 2007; Wang et al., 2006). These previous studies have variously investigated mentalising using intentional vs. physical causality statements, animated shapes moving in a manner that suggest characters with intentions, and judgments of sincere vs. sarcastic statements. The current result extends this developmental finding to show that arMPFC is also active in adolescent participants during mentalising in a strongly emotional context.

5.4.1.2 Posterior superior temporal sulcus/ temporo-parietal junction

Adults and adolescents activated the pSTS/TPJ for social vs. basic emotion, with activity greater on the left than on the right. The left TPJ is consistently reported for its involvement in mentalising tasks, and is thought to play a role in reasoning about the beliefs of others (Samson et al., 2004; Frith & Frith, 2003; Saxe & Kanwisher, 2003). Elsewhere, it has been argued that pSTS/TPJ represents a prediction error (or ‘pay attention!’) signal for updating social information (Hampton et al., 2008; Kawawaki et al., 2006). This is not in consistent with the current result.

The pSTS/TPJ has been reported to be activated during mentalising in adolescents (Blakemore et al., 2007; Moriguchi et al., 2007). Activity within this region in the social relative to basic emotion condition may be related to the need for representing

or reasoning about other people’s beliefs when imagining social vs. basic emotion situations.