Review
Social fearfulness in the human brain

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Abstract

Social fearfulness is expressed on a continuum of severity from moderate distress to incapacitating fear. The present article focuses on the brain states associated with this broad dimension of social anxiety in humans. In total, 70 published studies are summarized documenting the neural correlates of social anxiety during states of rest, threat-related cognitive-affective activation, and acute symptom provocation. Neural exaggeration in limbic (amygdala) and paralimbic (insula) regions appears to be associated with functional outcomes involving increased attention for and processing of social threat. Evidence is also reviewed showing that social anxiety is characterized by atypical functional connectivity in certain brain networks. Despite a higher prevalence of social anxiety disorder among females, males have been overrepresented in the published clinical studies (constituting approximately 56% of the total participants). We evaluate the prospects of nonhuman animal models of social anxiety and discuss several promising directions for future research. The review highlights the need to adopt an integrative, network-based approach to the study of the neural substrates underlying social anxiety.

Highlights

► Social fearfulness exists on a continuum of severity. ► The neural correlates of social anxiety are reviewed and future directions outlined. ► Neural substrates of social anxiety involve dysfunctional networks.

Introduction

Psychologists and psychiatrists have long recognized that the varieties of human fears and phobias are not entirely arbitrary but rather seem circumscribed by a limited group of categories (Marks, 1969), including natural/situational triggers (e.g., darkness, heights), dangerous predators (e.g., snakes, spiders) and threatening conspecifics (American Psychiatric Association, 2000). Perhaps not surprisingly these categories consistently emerge as stable factors in structural analyses of human fears (Arrindell et al., 1991) and are also anticipated by ethological perspectives on animal behavior (Öhman et al., 1985). Taken together, the sum of these considerations suggest that phobic content is at least partially shaped by the evolution of core brain circuits and networks that influence what qualifies as an ‘emotionally competent stimulus’1 (Damasio, 2003) capable of activating fear-related responses.

This review is devoted to a broad consideration of the brain states that are associated with social anxiety, encompassing both its subsyndromal and clinical manifestations. Social anxiety refers to fear and avoidance of interpersonal interactions, especially those that carry a potential for social evaluation or scrutiny from others. As a diagnostic entity, social anxiety disorder (SAD) constitutes one of the most common psychiatric illnesses, with lifetime prevalence rates estimated to be as high as 12% of the general population (Kessler et al., 2005). The experience of SAD, while highly distressing in itself, also constitutes a risk factor for other emotional difficulties, including mood disorders and substance abuse (Weiller et al., 1996). However, SAD probably represents the most extreme variant of a more general dimension of social fearfulness. As with many other fears, the experience of social anxiety most likely exists on a continuum that ranges in intensity from relatively mild to severely disabling (Rosen and Schulkin, 1998). Although some individuals with social anxiety may be able to endure social interactions with a degree of discomfort and distress, for others, the fears may be sufficiently powerful to induce active behavioral avoidance of almost all such encounters, resulting in marked disability and psychiatric impairment. A functional perspective suggests that the extreme manifestations of social anxiety represent maladaptations of a behavioral system that evolved as a means of regulating dominance/submissiveness hierarchies in complex primate societies (Öhman, 1986, Öhman, 2009). Among higher primates, there is an increasing danger to survival associated with threats from conspecifics, including the threat of disapproval, rejection and ostracism from one's community. In this way, social fears have become incorporated into the human psychological repertoire, alongside fears of predators (e.g., snakes and spiders) and other potentially harmful stimuli.

At the outset, it is important to recognize the diversity of research traditions (each with its associated lexicon) that have made contributions to the study of social anxiety, ranging from psychiatry and clinical psychology to personality and developmental psychology as well as the non-human animal literature. One consequence of this diversity is that the field has yet to agree upon a consistent and unequivocal nomenclature in referring to the various phenotypical expressions of social fearfulness, which has often led to a lack of conceptual clarity and perhaps, delays in scientific progress (Schmidt and Buss, 2010). The perspective adopted in this review posits the existence of a general social anxiety spectrum (illustrated in Fig. 1) that encompasses everything from shyness (moderate distress in some social situations) to a clinical diagnosis of SAD. Our view is shared with previous evolutionary (Hermans and van Honk, 2006), developmental (Pérez-Edgar and Fox, 2005) and clinical (Hofmann et al., 2004) treatments of social anxiety and fearfulness. Although such a perspective is not without some controversy (e.g., Heiser et al., 2009, Kagan, 1994), it accounts for the observation that these various phenomena share many common neural, behavioral, and cognitive correlates (Pérez-Edgar and Fox, 2005). A dimensional perspective on social fearfulness also represents a pragmatic approach for the purposes of the present review and encourages the integration of experimental findings across various laboratories.

A growing number of research studies have recently emerged that have considerably expanded our knowledge concerning the psychobiological correlates of social anxiety (see Hermans and van Honk, 2006, Mathew et al., 2001, Pérez-Edgar and Fox, 2005, Schmidt and Schulkin, 1999, for reviews). The aim of this review article is to provide a broad overview of the neuroscience literature on social anxiety (for a recent review of contextual and environmental contributions to social anxiety, see Brook and Schmidt, 2008) and suggest several promising lines of inquiry for continued investigation. In the first section, we present a summary of the neural systems that support complex socio-emotional functions and whose dysregulation may contribute to social anxiety. Second, we chart the developmental precursors of adult social anxiety as reflected in a particular temperamental style of responding to novelty that emerges within the first months of post-natal life. Third, we review a series of studies concerning neuronal and cognitive activity during resting conditions and in response to subtle forms of cognitive-affective activation and acute symptom provocation in socially anxious adults and adolescents. Fourth, we discuss sex differences in the prevalence of social anxiety and highlight potential biological substrates that may be important for understanding increased prevalence of social fearfulness among females. Fifth, we briefly assess the viability of non-human animal models for the study of social anxiety. Finally, we conclude with a consideration of promising directions for future research.

Section snippets

Functional neuroanatomy of emotion

Here we briefly review the functional neuroanatomy underlying the experience, expression and regulation of emotions, since the same neuronal substrates are involved in the neurobiology of social behaviors and social anxiety (Adolphs, 2003). To date, much of our detailed knowledge about the so-called emotional brain originates from non-human animal studies, which permit invasive procedures such as the placement of selective lesions, the application of focal electrical stimulation, and surgical

Developmental considerations

There is considerable interest in clarifying the developmental course and precursors to clinical manifestations of social anxiety since anxiety disorders in general are increasingly being conceptualized as developmental in nature (Leonardo and Hen, 2008). Behavioral inhibition constitutes the earliest antecedent of subsequent social anxiety disorder (Fox et al., 2005a, Fox et al., 2005b). Behavioral inhibition refers to an early appearing temperamental style characterized by extreme wariness

Adult studies

The neural correlates of social anxiety in adults can be profitably studied by recording brain activity under a variety of different laboratory settings6

Sex differences in social anxiety: biological considerations

Previous epidemiological research has established that the risk for SAD is more than doubled among females (Wells et al., 1994). By contrast, the samples included in neuroimaging studies of SAD consist primarily of males (approximately 56% of the total participants in the clinical studies summarized in Table 1). Although Irle et al. (2010) reported some sex-related differences in amygdala volume (reduced only among male patients with SAD), other studies either did not report significant effects

Non-human animal models: implications for understanding human social anxiety

Non-human animal models provide a unique opportunity to uncover the neurobiological mechanisms involved in the origins and maintenance of psychiatric disorders. Findings from several non-human animal models could inform questions related to the psychobiology of social anxiety (see Mathew et al., 2001, for a review). The subordination stress model bears the most resemblance, at least superficially, to human social anxiety. Social subordination stress in monkeys leads to withdrawal-related

Future directions and conclusions

The perspective we have adopted is that the experience and expression of social anxiety exists on a continuum of severity from moderate distress to incapacitating fear. There are several promising directions for continued research on the psychobiological bases of this general social anxiety spectrum that warrant special consideration.

Conclusion

As this review has illustrated, fruitful research on the neuroscience of social fearfulness involves the integration of many separate experimental paradigms and methods derived from basic and clinical research. Converging evidence from electrical, magnetic and nuclear imaging, helps to direct theoretical frameworks about the neurobiological substrates of social anxiety. As complex brain function is increasingly understood to be the outcome of flexible and distributed neural interactions (e.g.,

Acknowledgements

This research was supported by operating grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Social Science and Humanities Research Council of Canada (SSHRC) awarded to Louis Schmidt, and a Vanier doctoral scholarship from NSERC awarded to Vladimir Miskovic under the direction of Louis Schmidt.

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