Social anxiety disorder: A critical overview of neurocognitive research - a summary of an article by Cremers & Roelofs

Social anxiety disorder: A critical overview of neurocognitive research.
Cremers, H. R., & Roelofs, K. (2016).
WIREs Cognitive Science, 7, 218-232
doi: 10.1002/wcs.1390

Abstract

Social anxiety disorder is a common disorder characterized by a persistent and excessive fear of one or more social or performance situations.
Behavioural inhibition is one of the early indicators of social anxiety and may advance into a certain personality structure and the development of maladaptive cognitive biases.

Several large-scale brain networks related to emotion, motivation, cognitive control, and self-referential processing have been identified, and are affected in social anxiety.
Social anxiety is also characterized by increased cortisol response and lower testosterone levels.
These neuroendocrine systems are related to altered connectivity patterns.

Introduction

Social anxiety disorder (SAD) is characterized by a persistent fear of one or more social or performance situations with exposure to unfamiliar people or to possible scrutiny by others.
A person with SAD fears that he or she will act in a way that will be humiliating or embarrassing.
Expose to the feared situations  almost invariably provokes anxiety.
Social situations are either avoided or endured with intense anxiety or distress.

Development, cognition, and treatment

The diagnosis of SAD requires that the condition interferes substantially with the person’s normal routine.

Research on personality traits and the development of social anxiety stresses the dimensional nature of social anxiety.
Traits related to emotional processing, much as neuroticism and extraversion are critical.

  • Neuroticism
    Regarded as a vulnerability marker in the development of SAD
  • Extraversion
    Regarded a ‘protective’ factor in the development of SAD

The heritability of social anxiety can, to a large extend, be explained by the heritability of these personality traits.

The relationship between personality factors and (social) anxiety development may be interpreted in a merely probabilistic manner.
Personality traits may simply capture some aspects of (social) anxiety and therefore naturally show covariation.

A three-factor solution for social anxiety

  • Social interaction fears
  • Observation fears
  • Public speaking fears

Such factors just pertain to the population, not the individual.

Developmental and cognitive models

Behavioural inhibition (BI): a temperamental trait referring to reactions of a child when confronted with novel situations and unfamiliar people.
One of the earliest developmental indications of social anxiety.

During the course of a child’s development, social anxiety may progress from such initial behavioural indicators, to increasing levels of self-consciousness and preoccupation with peer feedback and exclusion.
Important elements

  • Low perceived emotional control
  • Post-event rumination
  • Avoidance
  • Use of safety behaviours

When confronted with challenging social situations, individuals with SAD shift their attention toward their anxiety, view themselves negatively as a social object, overestimate the negative consequences of a social encounter, believe that they have little control over their emotional response, and view their social skills as inadequate to effectively cope with the social situation.
In order to avoid social mishaps, individuals with SAD revert to maladaptive coping strategies, including avoidance and safety behaviours followed by post-event rumination, which leads to further social apprehension in the future.

SAD is a heterogenous condition.
Naturally there are many different possible ‘routes’ to the development of similar social anxiety symptoms, while comparable predisposing factors may lead to very different symptom outcomes.
Distal factors (such as genes) and proximal ones (current stressors) create a complex interplay in the development of social anxiety.

Treatment

Social anxiety can be treated relatively well, with both pharmaco- and psychotherapy.
Cognitive behavioural therapy had the largest symptom reduction effect.

A considerable number of patients does not respond adequately to treatment.

Neurobiology

There has been a steady increase of functional magnetic resonance imaging (fMRI) research into the neural mechanism underlying social anxiety.

Large-scale networks

fMRI studies are increasingly utilizing large-scale network approaches to delineate the neurobiology of psychiatric symptoms.
Brain network perspectives address the interplay and organizational principles of many, rather than a single brain region as the neurobiological foundation of complex psychological functions.
Several distributed brain networks have robustly been identified.
The emotion, motivation, cognitive control, and default mode networks (DMNs) are relevant to particular symptoms of social anxiety and are linked to resilience and vulnerability to adverse and stressful events.

The hypothalamic-pituitary-gonadal (HPG) and hypothalamic-pituitary-adrenal (HPA) axes, and their respective end products, testosterone and cortisol, play an important role in regulation of social emotional behaviour.

  • Socially submissive and anxious behaviour is associated with high cortisol and low testosterone
  • Social dominance and aggression is typically associated with high testosterone and low cortisol levels

Patients with SAD show alterations in these neuroendocrine systems consistent with the social submissiveness pattern.
These hormones also interact with emotion- and motivational-related brain networks.

The emotion network

The amygdala is a core region in emotion processing, and a hub region in the emotion network.
The amygdala is argued to detect relevant information in the surroundings more broadly and is essential in the processing of salient or ambiguous stimuli.

There is an abundance of evidence for the importance of the amygdala in the processing of social cues, regardless of a specific valence.
Social anxiety studies have shown amygdala hyper-activation especially in response to socially threatening facial expression.

The bed nucleus of the stria terminalis (BNST) is part of the ‘extended amygdala’ and is critical in sustained threat responses, and has been related to anxious temperament.

Several brainstem nuclei are important for neuroendocrine and neurotransmitter control and relsease.
Serotonin is a key neurotransmitter of the emotion network.
The insula and fusiform gyrus show hyper-activation in social anxiety and can be considered other central parts of the emotion network.

Evidence exists for hyper-activation of the emotion circuit.

Conclusion

The amygdala plays a critical role in salience, vigilance-avoidance and stress processing.
Amygdala activity constitutes a potential biomarker for social anxiety.
But future research needs to address concerns regarding the role of the amygdala and the emotion network and social anxiety.

The motivation network

The motivation network comprises of a set of brain regions in the brainstem, striatum, and medial prefrontal cortex (mPFC) integral to mesolimbic dopaminergic activity.
The ventral tegmental area (VTA) is the main brainstem source of dopamine and is connected to regions of the ventral striatum.
The ventral striatum encompasses the nucleus accumbens, and ventral parts of the putamen and caudate nucleus.

Functionally, the ventral and dorsal striatum are argued to be best distinguished by their mPFC connectivity to the medial orbitofrontal cortex/anterior cingulate cortex and dorsolateral PFC.

Considerable debate is still going on about the type of functions related to the motivation network.
Dopamine serves to promote complex functions such as reinforced learning and reward anticipation.
Different dopaminergic neurons are involved in motivational valence and motivational salience.

Several studies have shown alterations in dopaminergic activity in SAD, but both increases and decreases are found.

  • There is an overall increased striatal responsiveness in social anxiety
  • Social anxiety is associated with stronger striatal activation for monetary rewards, but weaker activation for social rewards
    • This could reflect a dissociation between these two types of incentives

The natural preference to obtain a social reward is weakened in SAD.

The cognitive control network

The PFC is involved in several higher-order cognitive functions, generally referred to as cognitive control, including control of social emotional action.
The PFC is crucial for modifying emotional responses.

The PFC has many connections to regions that are part of the emotion and motivation networks and can hence exert a regulatory role over various processes in these areas.
The human capacity to voluntarily regulate emotional responses may be mediated by phylogenetically older fear networks.
A reduction of this prefrontal emotion regulatory capacity may form the basis of various (other) anxiety disorders.

Deficiencies in emotion regulatory capacities are a hallmark feature of social (and many other) anxiety disorders.
Patients with SAD show reduced regulatory-related activity and connectivity, which can be reversed with CBT.

There is complexity and heterogeneity of prefrontal functioning across patients.
There is a decreased cognitive-control network mediated, emotion regulatory capacity in social anxiety.

SAD patients show increased prefrontal activity during salient face processing, which has been argued to reflect a compensatory mechanism to regulate overactive subcortical regions, or simply increased attention for such salient stimuli.

The default mode network

The default mode network uses most of its energy at rest and shows a pattern of large-scale network organisation.

The DMN traditionally encompassing the posterior cingulate and medial prefrontal regions forms a particular circuit, which is more active during rest than during cognitive performance.
The DMN is related to processes like mind-wandering and self-referential processing.
The DMN is strongly connected to social-affective areas.

The DMN has been implicated in a wide variety of psychiatric disorders including social anxiety, which fits with cognitive models emphasizing disturbed self-evaluative and referential processes.

The role of the vmPFC is of specific interest since it plays such an integral role in all four networks, including the DMN.
One may speculate that in social anxiety the balance in vmPFC functioning is shifted toward default-mode related self-referential processing and away from cognitive control functions, like amygdala regulation.

Neurodocrine circuitries

Recent studies in SAD patients have demonstrated increased cortisol stress responses in SAD compared to healthy and PTSD controls.
Basal testosterone levels are decreased in female patients with SAD.

Testosterone was associated with higher extraversion and lower neuroticism.
High cortisol responses are associated with increased social avoidance tendencies.
Cortisol facilitates threat avoidance.
Single dose testosterone administration can alleviate avoidance tendencies even in patients with SAD.
Testosterone may exert its effects by biasing the amygdala specifically to social threat approach.
Testosterone furthermore exerts its effects by action on dopaminergic projections from the amygdala to the striatum. It typically reduces HPA axis activity previously found to be related to social avoidance in patients with SAD.
The HPA and HPG axis may be disregulated in SAD, and have effects on brain networks relevant for SAD.
Several other hormones and peptides are also related to social submissiveness and avoidance in SAD, such as oxytocin, progesterone, and vasopressing.

Discussion

A general picture of the large-scale network underpinnings of social anxiety

  • Hyper-responsive emotion network, both in response to social threatening stimuli and at rest
  • A perhaps surprisingly active motivational system, particularly in obtaining non-social rewards and avoiding social punishment, reflective of a distincitive pattern of motivational drives in social anxiety
  • A diminished cognitive control and emotion regulation network, both during instructed and unprompted social stressful situations, but yet a heightened prefrontal threat attention system
  • A strongly active and extensively connected ‘default-mode’ or self-referential network both at rest and during self-referential critique

The testosterone/cortisol ration is related to PFC-amygdala decoupling, higher amygdala activity, higher striatal activity, and amygdala-striatal projections.

Individuals may vary in the brain mechanism underlying similar social anxiety symptoms.

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