Differential modulation of neural activity throughout the distributed neural system for face perception in patients with Social Phobia and healthy subjects

doi:10.1016/j.brainresbull.2008.08.003

Brain Research Bulletin

Volume 77, Issue 5, 25 November 2008, Pages 286-292

https://doi.org/10.1016/j.brainresbull.2008.08.003 Get rights and content

Abstract

Social Phobia (SP) is a marked and persistent fear of social or performance situations in which the person is exposed to unfamiliar people or to possible scrutiny by others. Faces of others are perceived as threatening by social phobic patients (SPP). To investigate how face processing is altered in the distributed neural system for face perception in Social Phobia, we designed an event-related fMRI study in which Healthy Controls (HC) and SPP were presented with angry, fearful, disgusted, happy and neutral faces and scrambled pictures (visual baseline). As compared to HC, SPP showed increased neural activity not only in regions involved in emotional processing including left amygdala and insula, as expected from previous reports, but also in the bilateral superior temporal sulcus (STS), a part of the core system for face perception that is involved in the evaluation of expression and personal traits. In addition SPP showed a significantly weaker activation in the left fusiform gyrus, left dorsolateral prefrontal cortex, and bilateral intraparietal sulcus as compared to HC. These effects were found not only in response to emotional faces but also to neutral faces as compared to scrambled pictures. Thus, SPP showed enhanced activity in brain areas related to processing of information about emotional expression and personality traits. In contrast, brain activity was decreased in areas for attention and for processing other information from the face, perhaps as a result of a feeling of wariness.

These results indicate a differential modulation of neural activity throughout the different parts of the distributed neural system for face perception in SPP as compared to HC.

Introduction

Faces are perhaps the most prominent social cue [30], [31]. Social Phobia patients (SPP) process faces differently from healthy control (HC) subjects. According to the Diagnostic and Statistic Manual of Psychiatric Disorders-IV TR [4], Social Phobia (SP) is ‘a marked and persistent fear of social or performance situations in which the person is exposed to unfamiliar people or possible scrutiny by others’.

A significant behavioral effect in SPP while processing social relevant stimuli, and in particular toward face processing, has been previously demonstrated. Specifically, behavioral studies have reported that SPP tend to judge neutral faces as negative [56], to remember critical faces better than accepting ones [39], and to scan faces with a different pattern of eye movements than that used by HC [32]. These results suggest that SPP view still images of faces with a negative or wary attitude.

Actually, several functional studies have investigated face perception in SPP. Birbaumer et al. [10] described an increased response in the amygdala in SPP while processing neutral human faces. A study by Stein et al. [48] showed stronger activation of left allocortex (including the amygdala and uncus) in SPP as compared with HC while watching angry and contemptuous faces as compared to happy faces. Other studies have shown that the degree of amygdala activation during the perception of faces with negative expressions is directly correlated with the severity of symptoms in SPP [43], and even with the degree of normal social anxiety in healthy subjects [33], [49]. Finally, a differential temporal dynamic pattern of activity was found in SPP as compared to HC in the amygdala bilaterally but not in the fusiform gyrus while subjects viewed faces with different emotional expressions (happy, fearful, or angry) [13]. Other studies examined other areas of the limbic system and showed, for example, a higher activation of the anterior cingulate cortex in SPP in response to disgust faces as compared to neutral faces [6]. One event-related study compared angry vs. neutral faces and showed hyperactivation of the insula in SPP as compared to HC [50].

Altogether, these studies suggest that the insula, the amygdala, and other limbic structures play a fundamental role in how SPP process faces differently as compared to controls. Studies in healthy volunteers indicate that the amygdala is involved in the recognition of face expression – particularly fear – in evaluating personality traits, in particular trustworthiness, and in maintaining a vigilant or wary state [1], [9], [12], [23], [30], [41], [52], [55]. The insula is recruited during the perception of disgust and in strong emotions – both negative, such as feeling cheated [46], and positive emotions, such as romantic [7] and maternal [36] love – perhaps related to its role in representing visceral sensation [17].

Because the amygdala, insula, and other limbic structures play a role in the emotional response to faces, these brain regions are considered to be a component of the ‘extended system’ for face perception, which includes non-visual areas extracting information from faces [25], [30], [31]. Previous studies of face processing in SPP have focused their attention on this part of the distributed neural system for face perception. Along with the ‘extended system’ for extracting additional face information, including emotions, the neural system for face perception includes also a ‘core system’ for visual face processing. The core system can be further divided into components that are primarily involved in the recognition of identity (fusiform gyrus), or in the perception of changeable aspects of faces, such as eye gaze and emotional expression. Judgments of personality traits, such as trustworthiness [54], appear to involve more the component for perception of changeable aspects, namely the superior temporal sulcus (STS), perhaps because of its role in evaluating expression [22] and intention [3], [26].

Previous fMRI studies of Social Phobia that used face stimuli were not intended to investigate abnormalities in face perception but, rather, because they are effective stimuli for evoking social threat.

Therefore, we decided to investigate the neural basis of altered face processing in SPP in the broader context of the distributed neural system for face perception by adopting a fast event-related experiment in which subjects viewed faces with different emotional expressions, including a neutral expression, and scrambled pictures for a low-level visual baseline.

Results revealed a redistributed activity in different parts of the face perception system in SPP. Patients with SPP showed stronger activity in components of the system that are involved more in the evaluation of expression and the formation of inferences about personal traits, in addition to stronger activity in areas associated with emotional response, and weaker activity in other components associated with attention to faces and recognition of identity.

Section snippets

Social Phobic patients

Eight right-handed subjects (4M/4F) (mean age 39 ± 7 years) with a diagnosis of Social Phobia according to the DSM-IV-TR [4] criteria were recruited. SPP were without psychiatric comorbidity and other medical conditions. No patient was receiving any pharmacological or psychotherapeutic treatment at the time of recruitment and at the time of the fMRI session.

Healthy controls

Seven right-handed healthy control subjects (4M/3F) (mean age 30 ± 7 years) were recruited as well. HC subjects did not have any psychiatric or

Clinical scale results

SPP as compared to HC had significantly higher levels of social anxiety, as assessed with the IAS (mean ± S.E.: 49.3 ± 1.42 vs. 33.7 ± 0.71, p < 0.01), the AAS (mean ± S.E.: 40.7 ± 1.41 vs. 23.5 ± 2.20, p < 0.01), and the LSSP (mean ± S.E.: 69.6 ± 1.01 vs. 24.7 ± 1.25, p < 0.01). No differences were found in state anxiety, as assessed by STAI-x1, between pre- and post-scan sessions, and between the two groups of subjects (mean ± S.E.: HC-pre 36.3 ± 0.9; HC-post 38.4 ± 1.3; SPP-pre 35.6 ± 1.2; SPP-post 38.7 ± 1.0; HC-pre vs.

Discussion

The results showed a differential response to faces throughout the distributed neural system for face perception [25], [30], [31] in SPP, as compared to HC. Specifically, the response to faces in SPP was stronger as compared to HC in bilaterally STS, the core system perceptual area that has been associated with perception of expression [22], [54], the evaluation of the intentions and personality traits of others [26], [55], and more generally with social evaluation of others [3]. Activation was

Conflict of interest

None.

Acknowledgments

This research was partially supported by the Fondazione IRIS (Castagneto Carducci (LI), Italy) and by e-SMILER (experimental brain Study on eMotional Interaction Leading to Enhanced Robots) grant 05/138 from the Fondazione Cassa di Risparmio di Pisa. The authors wish to thank Giulio Perugi, Researcher in Psychiatry at the School of Medicine, University of Pisa for his support in recruiting social phobia patients, and Luigi Landini, Professor at the Faculty of Engineering, University of Pisa

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Research reportDifferential modulation of neural activity throughout the distributed neural system for face perception in patients with Social Phobia and healthy subjects

Abstract

Introduction

Section snippets

Social Phobic patients

Healthy controls

Clinical scale results

Discussion

Conflict of interest

Acknowledgments

Trends Cogn. Sci.

Behav. Res. Ther.

Biol. Psychiatry

Brain Res. Bull.

Neuron

Biol. Psychiatry

Neuroimage

Psychiatry Res.

Comput. Biomed. Res.

Neuropsychologia

Brain Res. Bull.

Neuropsychologia

Neuron

Neuroimage

Trends Cogn. Sci.

Biol. Psychiatry

Psychiatry Res.

Biol. Psychiatry

Behav. Res. Ther.

Neuroimage

Biol. Psychiatry

Biol. Psychiatry

Neuron

Biol. Psychiatry

Neuron

Behav. Res. Ther.

Effects of gaze on amygdala sensitivity to anger and fear faces

Science

Amygdala damage impairs emotional memory for gist but not details of complex stimuli

Nat. Neurosci.

Research report
Differential modulation of neural activity throughout the distributed neural system for face perception in patients with Social Phobia and healthy subjects