Research reportDifferential modulation of neural activity throughout the distributed neural system for face perception in patients with Social Phobia and healthy subjects
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
References (57)
- et al.
Social perception from visual cues: role of the STS region
Trends Cogn. Sci.
(2000) - et al.
Attentional bias to threat in social phobia: facilitated processing of threat or difficulty disengaging attention from threat?
Behav. Res. Ther.
(2003) - et al.
Increased activation of the anterior cingulate cortex during processing of disgust faces in individuals with social phobia
Biol. Psychiatry
(2005) - et al.
Processing the socially relevant parts of faces
Brain Res. Bull.
(2007) - et al.
Response and habituation of the human amygdala during visual processing of facial expression
Neuron
(1996) - et al.
Time-varying amygdala response to emotional faces in generalized social phobia
Biol. Psychiatry
(2007) - et al.
Movement and mind: a functional imaging study of perception and interpretation of complex intentional movement patterns
Neuroimage
(2000) - et al.
Amygdala activation in the processing of neutral faces in social anxiety disorder: is neutral really neutral?
Psychiatry Res.
(2006) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages
Comput. Biomed. Res.
(1996)- et al.
Facial expression and gaze-direction in human superior temporal sulcus
Neuropsychologia
(2007)
Neural response to the visual familiarity of faces
Brain Res. Bull.
Neural systems for recognition of familiar faces
Neuropsychologia
Brain areas active during visual perception of biological motion
Neuron
Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces
Neuroimage
The distributed human neural system for face perception
Trends Cogn. Sci.
Human neural systems for face recognition and social communication
Biol. Psychiatry
Face to face: visual scanpath evidence for abnormal processing of facial expressions in social phobia
Psychiatry Res.
Mothers’ neural activation in response to pictures of their children and other children
Biol. Psychiatry
Recognition bias for critical faces in social phobics
Behav. Res. Ther.
Human amygdala responses to fearful eyes
Neuroimage
An insular view of anxiety
Biol. Psychiatry
Association between amygdala hyperactivity to harsh faces and severity of social anxiety in generalized social phobia
Biol. Psychiatry
Contributions of the amygdala to emotion processing: from animal models to human behavior
Neuron
Effect of task conditions on brain responses to threatening faces in social phobics: an event-related functional magnetic resonance imaging study
Biol. Psychiatry
Both of us disgusted in My insula: the common neural basis of seeing and feeling disgust
Neuron
Social anxiety, fear of negative evaluation and the detection of negative emotion in others
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.
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