An Evolutionary Perspective on Social Anxiety Disorder
(This article was first published by the Lundbeck Institute in the Institute Magazine no. 6, 2003.)
Social behaviour in animals, and SAD in humans, appear to be governed by similar neurobiological mechanisms
Apart from specific phobia, social anxiety disorder (SAD) or social phobia is the most common of the anxiety disorders. However, its pathogenesis remains poorly understood.
Evolutionary approaches to social anxiety may offer a useful theoretical perspective, and interesting overlaps between animal models of social behaviour and clinical findings with SAD patients may offer some support for the role of distal evolutionary mechanisms in SAD.
Clinical features and prevalence of SAD
The essential feature of SAD is an excessive fear of humiliating or embarrassing oneself while being exposed to public scrutiny or to unfamiliar people, resulting in intense anxiety upon exposure to social performance situations. Feared social situations are either avoided as much as possible or create significant distress (APA, 2000).
Physical manifestations of anxiety in the feared situations include a shaky voice, clammy hands, tremors and blushing. In the generalized sub-type of SAD, anxiety is associated with most social situations (including both formal performance situations such as giving a speech or speaking at a meeting, and informal social interactions such as initiating conversations, attending parties or dating); in the non-generalized sub-type, anxiety occurs only in specific social situations, such as public speaking, or eating/drinking in public, or writing in public.
Prevalence rates for SAD range from 3% to 16% in various studies (Davidson et al., 1993a; Kessler et al., 1994), depending on the diagnostic instrument used and the range of social fears assessed by these measures. SAD causes a marked reduction in the patient's quality of life and significant disability in functioning, which in turn results in substantial economic costs to both the patient and society (Stein and Kean, 2000).
Evolutionary functions of social anxiety
Some degree of social anxiety may be adaptive in several ways. Firstly, human and non-human primates need to be prepared to fear angry, threatening or rejecting faces (Mineka and Zinbarg, 1995; Stein and Bouwer, 1997).
Social anxiety alerts us to potential threats and signals the need to activate effective coping responses. Additionally, displays of social anxiety may also serve as a coping strategy in the face of threat.
In addition to the role of social anxiety in signalling and defending against potential threats, it has been argued that making a good impression on others may have an important survival function.
Humans have evolved to compete for attractiveness, in order to elicit important social resources and investments from others. Some degree of social anxiety may help people to "police" their social behaviours, thus preventing social sanction or exclusion (Gilbert, 2001).
The evolutionary function of social anxiety is perhaps most clearly illustrated by the phenomenon of blushing, a common feature of SAD. Darwin (1872) provided an extensive description of the blushing response in humans, noting that it involved a reddening of the face, neck and ears in response to "thinking of what others think of us".
Similarly, a more recent comprehensive review defines blushing as "a spontaneous reddening or darkening of the face, ears, neck and upper chest that occurs in response to perceived social scrutiny or evaluation" (Leary and Meadows, 1991).
What is the function of blushing in situations of perceived social evaluation or threat? In the animal world, dominant and submissive status are signalled by a range of mechanisms. One such mechanism, termed appeasement displays, play an important role in indicating acceptance of the status quo to a dominant conspecific (De Waal, 1989).
Humans have presumably also evolved efficient mechanisms for recognizing thoughts and emotions in other humans and responding accordingly. The blushing response, lowered gaze and nervous grin commonly displayed by SAD patients in anxiety-provoking social situations are arguably reminiscent of appeasement displays in animals.
Indeed, a range of data indicate that patients with SAD misperceive information about the need for social appeasement (e.g. they have an exaggerated view of the low status of the self and the high status of others, overestimation of the social threat; Gilbert, 2001), while empirical studies have demonstrated that displays of embarrassment do mitigate the negative reactions of others (Leary et al., 1992).
A false appeasement alarm, or a dysfunction in otherwise adaptive appeasement signals, may therefore underlie SAD (Stein, 2003; Stein and Bouwer, 1997).
Furthermore, the demographics of blushing and SAD have substantial overlap: given that appeasement displays are more likely in subordinate members of a species, from an evolutionary perspective it is perhaps not surprising that both SAD and blushing appear to be more common in women (who still occupy a socially subordinate or submissive position in many cultures) and that SAD typically has its onset in childhood or adolescence (a developmental stage associated with low social status).
Neurocircuitry and neurobiology of SAD
Some support for these evolutionary theories can cautiously be drawn from findings on proximate psychobiological mechanisms in SAD. While the neurobiological underpinnings of SAD are still poorly understood (M. Stein, 1998), it appears that similar neurobiological mechanisms may underlie social behaviour in both humans and animals.
A range of structures have been suggested to mediate social cognition, including the amygdala and temporal regions, the striatum, and the prefrontal and cingulate cortex (Adolphs, 2001). There are interesting data showing that SAD patients demonstrate selective activation of the amygdala when exposed to fear-relevant stimuli (Birbaumer et al., 1998) or tasks (Tillfors et al., 2001), and show abnormal patterns of amygdala activations during aversive conditioning (Schneider et al., 1999).
Conversely, after lesions of the amygdala (for example, in Klüver-Bucy syndrome) there may be inappropriate loss of social fear. There is also growing evidence that striatal neurocircuits play a role in SAD: patients with SAD have a greater reduction in putamen volume with aging (Potts et al., 1994), reduced choline and creatinine signal-to-noise ratios in subcortical, thalamic and caudate areas (Davidson et al., 1993b), and decreased N-acetyl-aspartate (NAA) levels and a lower ratio of NAA to other metabolites in cortical and subcortical regions (Davidson et al., 1993b; Tupler et al., 1997).
Finally, increased dorso-lateral pre-frontal cortex activity has been reported during symptom provocation in a PET study of SAD patients.
Given the potential involvement of the above regions in SAD, it can be postulated that the serotonin system, which extends to both amygdala and cortico-striatal neurocircuits, plays an important role in the mediation of social anxiety.
Serotonin plays a central role in mediating social behaviour in animal models: reduction of serotonin function leads to avoidance of affiliative social behaviours in primates, while enhancement of serotonergic function results in increased pro-social behaviours (Raleigh et al., 1983); and free-ranging primates with low levels of the serotonin metabolite CSF 5-HIAA have less social competence and emigrate from their social groups earlier (Mehlman et al., 1995; Raleigh et al., 1985).
In addition, however, it appears that changes in status result in a change in serotonergic function: removal of dominant animals from the group results in significant decreases in serotonin levels (Raleigh et al, 1984). The relationships between social behaviour and serotonin status are therefore complex and bi-directional.
In humans, there are also some (not altogether consistent) data to suggest that increasing serotonergic activity is associated with an increase in social affiliation (Knutson et al., 1998). A role for serotonin in SAD has been suggested by the results of pharmacological challenges with serotonergic agents (Tancer et al., 1994) and by the successful treatment of SAD with the selective serotonin re-uptake inhibitors (SSRIs) (van der Linden et al., 2000).
While little is known about the effects of SSRIs on the functional neuroanatomy of SAD, there is some evidence that SSRI treatment leads to reduced activity in amygdala-hippocampal-, frontal- and cingulated regions in SAD patients (Furmark et al., 2002; van der Linden et al., 1999).
There is more substantial evidence for the involvement of the dopaminergic system in social anxiety. Animal studies have found that dopamine levels are reduced in timid mice (Mayleben et al., 1992) and that striatal dopamine D2 binding is decreased in lower social status monkeys (Grant et al., 1988) (although, as in the case of serotonin, the relationship between social status and dopamine function are complex rather than unidirectional).
In humans, low cerebro-spinal fluid dopamine is correlated with introversion among depressed patients, while homovanillic acid (a dopamine metabolite) is lower in panic disorder patients with SAD than in those without. Patients treated with dopamine blocking agents may develop an increase in social anxiety symptoms (Pallanti et al., 1999).
Furthermore, there is an association between low striatal D2 binding and detachment, and between certain dopamine D2 and dopamine transporter polymorphisms and avoidant/schizoid behaviour.
Functional brain imaging studies have further demonstrated that striatal dopamine re-uptake site densities are markedly lower in SAD patients than normal controls (Tiihonen et al., 1997), and that striatal D2 receptor binding is lower in SAD patients than in controls (Schneier et al., 2001), suggesting that SAD is characterized by decreased dopamine function.
While social anxiety may serve an adaptive function in recognizing and responding to social threat, and in eliciting important resources, SAD may constitute a "false alarm" that activates appeasement responses in the absence of threat.
Social behaviour in animals, and SAD in humans, appear to be governed by similar neurobiological mechanisms. Evolutionary perspectives therefore provide a useful impetus towards the development of a solid theoretical framework for approaching SAD, and animal models offer potential as a means to better understand its pathogenesis.
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Published on CNSforum 14 Feb 2005