Social anxiety disorder (SAD) is defined by a marked and persistent fear of social or performance situations in which the person is exposed to unfamiliar people, or possible scrutiny by others [1
]. When interacting with others, people with SAD experience intense anxiety accompanied by physical symptoms such as blushing, heart racing, sweating, trembling, and nausea, as well as stuttering and trouble concentrating [2
]. SAD is one of the most common anxiety disorders, with a lifetime prevalence of up to 13% [3
]. When untreated, SAD can lead to elevated social isolation, depression, anxiety, and alcohol and/or substance abuse [4
Models of SAD have highlighted the role of emotional hyper-reactivity in feared social situations. Exaggerated emotional responses are thought to arise from maladaptive appraisals of the social situation that transform innocuous social cues into interpersonal threats [5
]. This hyper-reactivity often leads to attempts to escape from or avoid the anxiety-provoking object or situation [2
To study the behavioral and brain aspects of this emotional hyper-reactivity, most studies have employed negatively valenced facial expressions as socio-emotional probes. Behaviorally, these studies show hyper-arousal and increased emotional distress in patients with SAD when exposed to negative face stimuli [2
]. Neurally, however, the findings are less clear.
The amygdala, which plays a critical role in the recognition of fear in facial expressions [6
], was a natural target in studies of the neural basis of emotional reactivity in SAD. It was suggested that the heightened emotional responses in SAD patients were associated with increased amygdala activity [7
]. Amaral [8
] proposed a model based on lesion studies in monkeys, which suggested that the amygdala performs a protective function, namely, allowing the organism to detect and avoid danger. This model provided a rationale for theories implicating the amygdala in the neuropathology of SAD.
Many studies have indeed demonstrated heightened amygdala responses in patients with SAD when viewing angry, fearful and even neutral facial expressions [7
]. However, other studies, some using stimuli other than faces, failed to detect differential amygdala activation between patients with SAD and HC [13
]. For example, Quadflieg and colleagues (2008) have found that both SAD patients and HC recruit the amygdala when listening to angry compared to neutral prosody [17
]. Similarly, Goldin and colleagues (2009) found increased amygdala responses to harsh facial expressions with longer stimulus presentation times (6 seconds) in both SAD patients and healthy controls [16
]. Other studies have even found decreased
amygdala responses in SAD patients compared to HC. For example, Kilts and colleagues (2006) have found decreased amygdala responses during both script-driven imagery of anxiety-provoking social situations and a mental arithmetic task in SAD [14
A second limbic region that is thought to play a prominent role in SAD neuropathology is the insula. The insula is interconnected with the amygdala, thalamus, and orbitofrontal cortex [18
], regulates the autonomic nervous system [19
], and is involved in the recognition and experience of aversive states [20
] and threat processing [21
]. Thus, hyper-reactivity of the insula in SAD patients might be responsible for the generation of fear responses to social aversive stimuli.
A recent meta-analysis identified four functionally distinct sub-regions in the human insula implicated in social-emotional, sensorimotor, olfacto-gustatory, and cognitive brain networks [22
]. The ventral part of the insula was associated with the social-emotional domain. This ventral region was active in 195 experiments of emotion generation (paradigms of “induction, imagination or recall of own happiness, fear, anxiety, anger, sadness, or disgust”) and 120 empathy related experiments (paradigms of judging emotions in faces or attending to pain in others). This differentiation matches previous cytoarchitectonic studies in non-human primates that found differences between the anterior-basal agranular, allocortical, and posterior granular parts of the insula [23
]. The anterior-ventral region is involved in the generation and mediation of feeling as a response to environmental stimuli and affective states [24
], and in the recognition of emotions in faces [25
]. In SAD, increased activity in this insula region was associated with visualization of angry and disgusted faces [13
], viewing of images with negative emotional content [27
], and anticipation of a public speaking task [28
]. However, several studies did not find such activity differences [17
] and others found decreased
activity in the insula during a public speaking task [30
] and during an implicit learning test [31
Thus, despite the clear focus of neuroimaging studies on the amygdala and insula as key regions in SAD pathology, findings are mixed. One explanation for these mixed findings might be related to factors such as different stimuli and experimental designs used to elicit emotional responses (mainly emotional faces until a few years ago, and images, written words, and auditory stimuli more recently), small patients groups, differences in exclusion criteria (e.g., different psychiatric co-morbidity), and other experimental parameters.
However, another explanation could be a lack of concordance between the behavioral and physiological components of anxiety. This idea was raised by Mauss and colleagues in a study of non-clinical social anxiety [32
]. In this study, anxiety experience, subjectively perceived physiological activation, and objectively measured physiological activation were assessed in high and low trait social anxiety participants using an impromptu speech paradigm. The study found no differences in physiological responding between high and low trait social anxiety, despite clear differences between the two groups in their subjective experience of anxiety and their perceived physiological activation. Although this study did not measure brain responses, and did not employ a clinical sample, it did raise an important question about the widely assumed link between behavioral and physiological responses in the context of social anxiety.
In light of the mixed literature on the neural correlates of emotion reactivity in SAD, the goal of the present study was to examine both behavioral responses and BOLD signal changes in SAD compared to HC when reacting to distinct types of socio-emotional stimuli. To test whether behavior and brain responses vary by context, we used three different socio-emotional tasks: 1) viewing looming harsh faces (Faces), 2) watching dynamic videos of actors delivering social criticism (Criticism), and 3) reading negative self-beliefs (Beliefs). These tasks mirror the specific types of interpersonal evaluations and negative thoughts that are especially salient in patients with SAD. As suggested by the literature, we focused on the amygdala and the insula regions, but also performed whole-brain analyses to examine the involvement of other brain networks in SAD.
We hypothesized that, compared to HC, patients with SAD would have (1) greater self-reported negative emotion reactivity for each of the three tasks; and (2) greater BOLD responses in the amygdala and insula. In secondary analyses, we examined the differential effect of each socio-emotional task on negative emotion reactivity and neural responses in SAD and HC, and whether – among SAD participants – negative emotion reactivity and neural responses were associated with social anxiety symptom severity.