The goal of the present study was to investigate behavioral and brain responses in patients with SAD versus HC when reacting to three socio-emotional tasks (faces, criticism, beliefs). As we expected, at the behavioral level all three tasks induced heightened negative reactivity in SAD versus HC participants. However, we found no evidence of between-group differences in amygdala and insula BOLD responses. Both SAD and HC had increased left and right amygdala responses in all three tasks, and increased left and right insula responses in 2 of the 3 tasks (Criticism and Beliefs).
How might this discrepancy between our current results and previous work on emotion-related brain responses in SAD be explained? One possibility is that differences in the experimental tasks used played a crucial role . To date, most studies have used static facial expression stimuli to examine neural processing of interpersonal threat cues. Studies that have investigated social stimuli other than faces have yielded mixed results [16, 17, 44, 45]. For example, no differential recruitment of the amygdala and insula in SAD and HC were found when listening to angry versus neutral voices , when performing a social situation task , or when playing a ‘decision making’ game with others .
In our study, we used three distinct types of socio-emotional tasks with relatively high levels of complexity. The Faces task used a static emotional facial expression with the addition of looming (i.e., the appearance of approaching the perceiver). The Criticism task used dynamic videos of an actor delivering socially critical comments. The Beliefs task used participant-generated negative self-beliefs embedded in an autobiographical script about a socially painful interpersonal situation. In addition, all three tasks paradigms had longer stimulus presentation durations (9–12 sec) than have been used in most prior studies.
It is possible that the increased stimulus complexity and presentation durations in our study increased the likelihood that healthy subjects would evaluate the stimuli as threatening, and thus may have yielded emotion reactivity related brain responses similar to those generated by the patients with SAD. In addition to the stimuli used to elicit emotional responses, other design parameters such as whether the participants are instructed to simply look at the stimuli, or whether they have to perform a task, and whether the task is implicit or explicit, may have contributed to the observed findings .
A second possible explanation of our findings builds upon the first, and suggests that at least in the complex socio-emotional contexts we employed in our study (and which characterize many everyday life contexts), increased negative emotion ratings in SAD may be related to exaggerated cognitive biases, including negative self-reflective and ruminative processes. It is also possible that there are differential tendencies to implement spontaneous (uninstructed) emotion regulation directed at the emotion experience in HC versus SAD patients. This could have yielded lower levels of negative emotion ratings in HC. Thus, if the normative pattern shown in HC is to engage in automatic emotion regulation, then one feature of SAD is the absence of such un-cued, automatic activation of emotion regulation. Therefore, maladaptive cognitive processes, such as rumination, suppression, and self-criticism, and ineffective emotion regulation, in SAD may lead to exaggerated negative emotion experience.
If such accounts are correct, we might expect other brain regions (in addition to amygdala and insula) to show differential response patterns between SAD and HC when exposed to socio-emotional stimuli. Indeed, whole brain analyses revealed SAD versus HC differences in several brain regions, specifically, increased frontal, occipital, and temporal cortical activity in SAD versus HC during the Faces and Criticism tasks, and decreased frontal activity in SAD versus HC during the Beliefs task (Table 3). These regions have been shown to be involved in emotion regulation (middle frontal gyrus) , recognition of faces (middle temporal gyrus) , language processing (superior temporal gyrus), memory (lingual gyrus, parahippocampus), and social cognition (medial frontal gyrus, superior temporal gyrus) . In SAD, though not much discussed, abnormal activity in these regions has been related to difficulties in reasoning , mentalizing abilities , and impaired perception of self and others [50–52]. Additionally, the whole brain analyses further support our findings of no between-group differences in amygdala and insula activity when reacting to the socio-emotional tasks.
Congruent with these findings, in a recent study, Doehrmann and colleagues (2012) examined the association between responses to cognitive-behavioral therapy for SAD and pre-treatment brain activations to social (facial) and nonsocial (scene) stimuli . They found pre-treatment activity in visual cortical regions correlated with treatment outcome, and no association with treatment outcome in the amygdala, despite its robust activation to all experimental conditions. The authors explained these results by emphasizing dysfunctional emotion regulation, and specifically attentional deployment, in SAD. They suggested that CBT is perhaps particularly successful in patients with better emotion regulation capacities, which is correlated with already stronger responses to angry faces in visual regions. Thus, in addition to showing no abnormality in baseline amygdala response in SAD, this study suggests that brain regions more related to emotion regulation and not to emotion reactivity, might be the core deficit in SAD, and the focus of change during treatment.
More generally, our finding of increased negativity in SAD compared to HC when facing emotional stimuli, with no such SAD versus HC differences in the amygdala and insula responses, could suggest that self-report of negative emotion is less tightly coupled with increased limbic activity than is typically thought, at least in the context of social anxiety. This hypothesis accords with the findings of Mauss and colleagues , namely, a decoupling of subjective emotion and physiological measures and objective physiological responses in high and low socially anxious participants when giving an impromptu speech. The authors suggested that the findings of increased physiological activation during the speech in all participants (and not only in participants who reported increased experience of anxiety) leaves open the possibility that physiological activation might be necessary for the experience of anxiety, but such activation is clearly not sufficient to explain inter-individual variation in anxiety experience. The results of the current study strengthen the conclusions of Mauss and her colleagues. It might be that the relation between subjective feeling and physiological response is more complex than a simple ‘amygdala = emotion’ equation would suggest.
It also bears comment that in the current study, examination of between task effects enabled us to examine whether the behavioral and neural results were related to a particular type of socio-emotional stimuli. Although all three tasks were successful in terms of inducing higher emotional responses in SAD, compared to HC, it seems that no task activated all emotion generation brain regions consistently. Our results indicate that different contexts, i.e. different “anxiety-inducing” experimental probes may have quite different effects, behaviorally and neurally. Behaviorally, the Beliefs task yielded the highest negative emotion reactions in both SAD and HC. Thus, the idiographic, participant-generated negative self-beliefs were the most potent emotional probe, most likely because of their self-relevance or personal salience. These probes were also the most ecologically valid type of stimuli in our study, as negative self-focused automatic thoughts are usually the focus of most forms of psychological interventions for SAD. Interestingly, the Beliefs task, which elicited the greatest negative emotion responses, did not elicit the greatest brain responses. Specifically, right amygdala responses were equally high for Criticism and Faces, and lower for Beliefs (with no differential task effects in the left amygdala) in SAD patients. BOLD responses in the left and right insula were highest when reacting to Criticism > Beliefs > Faces in both SAD and HC.
Contrary to our hypothesis, social anxiety symptom severity was not correlated with negative emotion ratings, and was associated only with greater left insula activation during the Faces task, with no association with amygdala response. This finding accords with the findings of Schmidt and colleagues  of a positive correlation between insula activity and symptom severity in SAD patients, despite no differential effect in the insula between SAD and HC, during explicit processing of verbal threat-related stimuli. The association with symptom severity suggests that within patients with SAD, symptom severity matters. Thus, during the Faces task, even though as a group SAD patients had insula responses comparable to the HC group, greater social anxiety symptom severity within patients was found to be associated with increased neural responses. A recent study by Furmark and colleagues further supports the importance of looking beyond only meeting diagnostic criteria for SAD. They found that both patients with SAD and HC had increased left amygdala activation in response to angry compared with neutral faces, but that genotype (serotonergic polymorphisms) and not diagnosis explained a significant portion of the variance in amygdala responsiveness .