The current study addressed 2 questions on the nature of BOLD responses to self- or other referential comments of a critical, neutral, or complimentary nature. First, does GSP-related hyperresponsiveness to social stimuli occur for any valence language or is it specific to negative comments? Second, is it generalized or is it for self-referential language only? Our data indicated that GSP-related hyperresponsiveness occurs specifically to negative comments, particularly negative self-referential comments.
Previous work implicates emotion-relevant hyperresponsiveness in GSP for one class of social stimuli, facial expressions.4-6,8,9,11,36
Specifically, research shows that GSP involves greater responding than in healthy subjects to a variety of facial expressions, including negative (harsh, angry, fearful, or disgusted),4-6,8,9,11
expressions. However, little work has directly examined the neural response to other classes of social stimuli in GSP. Because neutral or positive valence faces might convey threat to patients with GSP, alternative stimulus classes may allow more refined explication of valence effects. The current data demonstrate such effects. Specifically, herein we extend the previous work using faces by showing emotion-relevant increased responses in GSP to another class of social stimuli, language-based praise and criticism. We also extend the previous work by showing that hyperresponsiveness occurs specifically to self-referential criticism rather than to broader classes of stimuli.
Prior work shows that self-directed praise or criticism can increase embarrassment. Given that embarrassment is a concern in GSP, one might expect patients with GSP to show greater BOLD responses than healthy subjects to self-directed praise as well as criticism. However, this was not seen. For all regions identified by group×referential target×valence interactions, patients with GSP showed significantly increased BOLD responses, relative to HCs, only to self-directed criticism. Interestingly, valence ratings provided by the 2 groups also demonstrated more negative ratings in GSP only for self-directed criticism. Arousal ratings collected subsequent to the study from 15 additional healthy individuals who did not participate in the fMRI study showed no significant difference between the arousal ratings for the positive and negative comments. These data suggest that our results are unlikely to be affected by differential levels of baseline arousal for positive and negative comments.
Previous work has reported increased amygdala response in patients with GSP to facial expressions.4,5,11
In the current study, we found similarly increased amygdala BOLD response in the patients with GSP relative to the HCs to self-referential criticism, another class of social stimuli. However, we also observed strong selective differential responses in GSP to self-referential criticism within the MPFC (BA 8, BA 9). Such MPFC differences may reflect primary amygdala-activation differences, with reverberating influences on the MPFC further emphasizing the critical role of the amygdala in GSP. Alternatively, given that prior work implicates the MPFC in self-representations,23-29
the MPFC may modulate amygdala engagement to initiate and maintain aspects of GSP. Thus, GSP-related dysfunction may, at least partly, reflect negative attitude toward the self, particularly in response to social stimuli, as instantiated in the MPFC.
In this regard, there are data to suggest that a subdivide might be made between the ventral and dorsal regions of the MPFC, with the ventral MPFC particularly associated with self-referential/relevant processing24,26-28,37
and the dorsal MPFC associated more with mentalizing about other people's mental states.37-40
In the current study, patients with GSP, relative to HCs, showed significantly elevated responses to self-referential criticism in more dorsal regions of the MPFC (x, y, z=18, 49, 33; 16, 35, 48; and –26, 35, 38). This may suggest enhanced fostering of representation of the other individuals’ mental states, particularly when patients with GSP manifest concern about others’ views of the patient. However, future work is clearly needed to further investigate this issue to determine the role and importance of MPFC functioning in GSP. Future work also should consider the other factors that might account for the differences observed herein. For example, monitoring of physiological parameters, such as carbon dioxide or heart rate during EPI acquisition, might reveal the degree to which the BOLD differences observed herein reflected differences in peripheral physiology. Nevertheless, prior studies suggest that such physiological differences are unlikely to account for the current results. That is, prior research finds only weak associations between individual differences in social anxiety and peripheral physiology,41-43
with no evidence of such differences on a task such as the one used herein. Regardless, this issue has not received systematic investigation across different emotive conditions within a balanced factorial design.
It is worth briefly considering cognitive models of GSP. These emphasize the role of cognitive processes in the maintenance of the disorder.30,31
For example, the Clark and Wells30
model identifies 4 processes that contribute to the maintenance of this anxiety: self-schemata, self-focused attention, in-situation safety behaviors, and anticipatory and postevent processing. The fourth maintaining factor, postevent processing, appears of most relevance to the current data. Postevent processing refers to the tendency for individuals with social phobia to engage in a detailed review or “post mortem” of events following a social interaction. This conceptualization is similar to the Rapee and Heimberg31
suggestion that social anxiety is generated and maintained by retrospective rumination. Work has shown that patients with GSP maintain negative appraisals of task performance over time (in contrast to healthy individuals who show increased positivity over their performance with time44
). Retrospective rumination is thought to be initiated by information elicited from external and internal cues during the social event itself.31
In the current study, the patients with GSP showed significantly heightened amygdala and MPFC responses to negative “social” self-referential appraisals. In short, it is possible that the amygdala and MPFC mediate postevent processing/retrospective rumination, maintaining a negative self-referential evaluation in response to cues (in the current case, externally generated explicit cues).
In summary, we found that the neural response in GSP to social comments was increased specifically to self-referential comments, and in particular self-referential comments that were critical. The regions implicated in this increased neural response included regions of the MPFC and the amygdala. Given that MPFC regions are involved in representations of the self, it might be suggested that these regions, together with the amygdala, play a primary role in the development and maintenance of GSP and that the pathology in the disorder at least partly reflects a negative attitude toward the self, particularly in response to social stimuli—that in GSP what engages the mind is others’ criticism. This highly context-dependent response in GSP helps constrain existing models of the disorder and may thus guide future therapeutic formulations in the treatment of the disorder.