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Influence of the fusiform gyrus on amygdala response to emotional faces in the non-clinical range of social anxiety

  • J. Pujol (a1), B. J. Harrison (a1) (a2), H. Ortiz (a1) (a3), J. Deus (a4), C. Soriano-Mas (a1), M. López-Solà (a1) (a5), M. Yücel (a2), X. Perich (a6) and N. Cardoner (a7)...

Social anxiety often involves a combination of hypervigilance and avoidance to potentially warning signals including the facial expression of emotions. Functional imaging has demonstrated an increase in amygdala response to emotional faces in subjects with social anxiety. Nevertheless, it is unclear to what extent visual areas processing faces influence amygdala reactivity in different socially anxious individuals. We assessed the influence of the fusiform gyrus activation on amygdala response to emotional faces in the non-clinical range of social anxiety.


Twenty-two normal subjects showing a wide range in social anxiety scores were examined using functional magnetic resonance imaging (fMRI) during the processing of happy and fearful faces. A dimensional analysis approach was used involving voxel-wise mapping of the correlation between subjects' social anxiety scores and amygdala activation, before and after controlling for fusiform gyrus activation.


We observed that only after controlling for subjects' level of activation of the fusiform gyrus was there an association between social anxiety ratings and amygdala response to both happy and fearful faces. The fusiform gyrus influence was more robust during the fear condition. Of note, fusiform gyrus response to fearful faces showed a negative correlation with additional behavioral assessments related to avoidance, including social anxiety scores, harm avoidance and sensitivity to punishment.


Relevant interactions among the emotional face-processing stages exist in the non-clinical range of social anxiety that may ultimately attenuate amygdala responses. Future research will help to establish the role of this effect in a clinical context.

Corresponding author
*Address for correspondence: J. Pujol, M.D., Department of Magnetic Resonance, CRC Corporació Sanitària, Hospital del Mar, Passeig Marítim 25–29, 08003 Barcelona, Spain. (Email:
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Adolphs, R, Spezio, M (2006). Role of the amygdala in processing visual social stimuli. Progress in Brain Research 156, 363378.
Birbaumer, N, Grodd, W, Diedrich, O, Klose, U, Erb, M, Lotze, M, Schneider, F, Weiss, U, Flor, H (1998). fMRI reveals amygdala activation to human faces in social phobics. Neuroreport 9, 12231226.
Bogels, SM, Mansell, W (2004). Attention processes in the maintenance and treatment of social phobia: hypervigilance, avoidance and self-focused attention. Clinical Psychology Review 24, 827856.
Brett, M (2007). The MNI brain and the Talairach Atlas ( Accessed 1 June 2007.
Brett, M, Anton, JL, Valabregue, R, Poline, JB (2002). Region of interest analysis using an SPM toolbox. 8th International Conference on Functional Mapping of the Human Brain, 2–6 June 2002, Sendai, Japan, p. 497. NeuroImage 16, no. 2, Abstract 497 [available on CD-ROM].
Campbell, DW, Sareen, J, Paulus, MP, Goldin, PR, Stein, MB, Reiss, JP (2007). Time-varying amygdala response to emotional faces in generalized social phobia. Biological Psychiatry 62, 455463.
Cooney, RE, Atlas, LY, Joormann, J, Eugene, F, Gotlib, IH (2006). Amygdala activation in the processing of neutral faces in social anxiety disorder: is neutral really neutral? Psychiatry Research 148, 5559.
Fairhall, SL, Ishai, A (2007). Effective connectivity within the distributed cortical network for face perception. Cerebral Cortex 17, 24002406.
First, MB, Spitzer, RL, Gibbon, M, Williams, JB (2007). Structured Clinical Interview for DSM-IV-RS Axis 1 Disorders – Non-Patient Edition (SCID-I/NP). Biometrics Research, New York State Psychiatric Institute: New York.
Friston, KJ, Buechel, C, Fink, GR, Morris, J, Rolls, E, Dolan, RJ (1997). Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6, 218229.
Furmark, T, Tillfors, M, Everz, P, Marteinsdottir, I, Gefvert, O, Fredrikson, M (1999). Social phobia in the general population: prevalence and sociodemographic profile. Social Psychiatry and Psychiatric Epidemiology 34, 416424.
Garner, M, Mogg, K, Bradley, BP (2006). Orienting and maintenance of gaze to facial expressions in social anxiety. Journal of Abnormal Psychology 115, 760770.
Garrett, AS, Menon, V, MacKenzie, K, Reiss, AL (2004). Here's looking at you, kid: neural systems underlying face and gaze processing in fragile X syndrome. Archives of General Psychiatry 61, 281288.
Greist, JH (1995). The diagnosis of social phobia. Journal of Clinical Psychiatry 56 (Suppl. 5), 512.
Gutierrez-Zotes, JA, Bayon, C, Montserrat, C, Valero, J, Labad, A, Cloninger, CR, Fernandez-Aranda, F (2004). Temperament and Character Inventory Revised (TCI-R). Standardization and normative data in a general population sample [in Spanish]. Actas Españolas de Psiquiatría 32, 815.
Hariri, AR, Bookheimer, SY, Mazziotta, JC (2000). Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport 11, 4348.
Hariri, AR, Mattay, VS, Tessitore, A, Kolachana, B, Fera, F, Goldman, D, Egan, MF, Weinberger, DR (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science 297, 400403.
Haxby, JV, Hoffman, EA, Gobbini, MI (2000). The distributed human neural system for face perception. Trends in Cognitive Science 4, 223233.
Horley, K, Williams, LM, Gonsalvez, C, Gordon, E (2004). Face to face: visual scanpath evidence for abnormal processing of facial expressions in social phobia. Psychiatry Research 127, 4353.
Ishai, A, Schmidt, CF, Boesiger, P (2005). Face perception is mediated by a distributed cortical network. Brain Research Bulletin 67, 8793.
Kanwisher, N, McDermott, J, Chun, MM (1997). The fusiform face area: a module in human extrastriate cortex specialized for face perception. Journal of Neuroscience 17, 43024311.
Lancaster, JL, Tordesillas-Gutierrez, D, Martinez, M, Salinas, F, Evans, A, Zilles, K, Mazziotta, JC, Fox, PT (2007). Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Human Brain Mapping 28, 11941205.
Lancaster, JL, Woldorff, MG, Parsons, LM, Liotti, M, Freitas, CS, Rainey, L, Kochunov, PV, Nickerson, D, Mikiten, SA, Fox, PT (2000). Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping 10, 120131.
Liebowitz, MR (1987). Social phobia. Modern Problems of Pharmacopsychiatry 22, 141173.
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 12331239.
Mennin, DS, Fresco, DM, Heimberg, RG, Schneier, FR, Davies, SO, Liebowitz, MR (2002). Screening for social anxiety disorder in the clinical setting: using the Liebowitz Social Anxiety Scale. Journal of Anxiety Disorders 16, 661673.
Morris, JS, Ohman, A, Dolan, RJ (1999). A subcortical pathway to the right amygdala mediating ‘unseen’ fear. Proceedings of the National Academy of Sciences USA 96, 16801685.
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97113.
Paulus, MP, Feinstein, JS, Castillo, G, Simmons, AN, Stein, MB (2005). Dose-dependent decrease of activation in bilateral amygdala and insula by lorazepam during emotion processing. Archives of General Psychiatry 62, 282288.
Phan, KL, Fitzgerald, DA, Nathan, PJ, Tancer, ME (2006). Association between amygdala hyperactivity to harsh faces and severity of social anxiety in generalized social phobia. Biological Psychiatry 59, 424429.
Phan, KL, Wager, T, Taylor, SF, Liberzon, I (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16, 331348.
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception. I: The neural basis of normal emotion perception. Biological Psychiatry 54, 504514.
Rauch, SL, Whalen, PJ, Shin, LM, McInerney, SC, Macklin, ML, Lasko, NB, Orr, SP, Pitman, RK (2000). Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biological Psychiatry 47, 769776.
Rossion, B, Dricot, L, Devolder, A, Bodart, JM, Crommelinck, M, De Gelder, B, Zoontjes, R (2000). Hemispheric asymmetries for whole-based and part-based face processing in the human fusiform gyrus. Journal of Cognitive Neuroscience 12, 793802.
Sergent, J, Ohta, S, MacDonald, B (1992). Functional neuroanatomy of face and object processing. A positron emission tomography study. Brain 115, 1536.
Somerville, LH, Kim, H, Johnstone, T, Alexander, AL, Whalen, PJ (2004). Human amygdala responses during presentation of happy and neutral faces: correlations with state anxiety. Biological Psychiatry 55, 897903.
Sorger, B, Goebel, R, Schiltz, C, Rossion, B (2007). Understanding the functional neuroanatomy of acquired prosopagnosia. Neuroimage 35, 836852.
Speilberger, C (1983). Manual for the State-Trait Anxiety Inventory (Form Y). Consulting Psychologists: Palo Alto, CA.
Stein, JL, Wiedholz, LM, Bassett, DS, Weinberger, DR, Zink, CF, Mattay, VS, Meyer-Lindenberg, A (2007 a). A validated network of effective amygdala connectivity. Neuroimage 36, 736745.
Stein, MB, Goldin, PR, Sareen, J, Zorrilla, LT, Brown, GG (2002). Increased amygdala activation to angry and contemptuous faces in generalized social phobia. Archives of General Psychiatry 59, 10271034.
Stein, MB, Simmons, AN, Feinstein, JS, Paulus, MP (2007 b). Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. American Journal of Psychiatry 164, 318327.
Stein, MB, Stein, DJ (2008). Social anxiety disorder. Lancet 371, 11151125.
Stein, MB, Torgrud, LJ, Walker, JR (2000). Social phobia symptoms, subtypes, and severity: findings from a community survey. Archives of General Psychiatry 57, 10461052.
Straube, T, Kolassa, IT, Glauer, M, Mentzel, HJ, Miltner, WH (2004). Effect of task conditions on brain responses to threatening faces in social phobics: an event-related functional magnetic resonance imaging study. Biological Psychiatry 56, 921930.
Straube, T, Mentzel, HJ, Miltner, WH (2005). Common and distinct brain activation to threat and safety signals in social phobia. Neuropsychobiology 52, 163168.
Talairach, J, Tournoux, P (1988). Co-Planar Stereotaxic Atlas of the Human Brain. Theime Medical Publishers: New York.
Tillfors, M, Furmark, T, Marteinsdottir, I, Fischer, H, Pissiota, A, Langstrom, B, Fredrikson, M (2001). Cerebral blood flow in subjects with social phobia during stressful speaking tasks: a PET study. American Journal of Psychiatry 158, 12201226.
Torrubia, R, Avila, C, Molto, J, Caseras, X (2001). The Sensitivity to Punishment and Reward Questionnaire (SPSRQ) as a measure of Gray's anxiety and impulsivity dimensions. Personality and Individual Differences 31, 837862.
Veit, R, Flor, H, Erb, M, Hermann, C, Lotze, M, Grodd, W, Birbaumer, N (2002). Brain circuits involved in emotional learning in antisocial behavior and social phobia in humans. Neuroscience Letters 328, 233236.
Vuilleumier, P, Richardson, MP, Armony, JL, Driver, J, Dolan, RJ (2004). Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nature Neuroscience 7, 12711278.
Wechsler, D (1981). Manual for the Wechsler Adult Intelligence Scale (WAIS-R). The Psychological Corporation: New York.
Yoon, KL, Fitzgerald, DA, Angstadt, M, McCarron, RA, Phan, KL (2007). Amygdala reactivity to emotional faces at high and low intensity in generalized social phobia: a 4-Tesla functional MRI study. Psychiatry Research 154, 9398.
Zubeidat, I, Salinas, JM, Sierra, JC (2008). Exploration of the psychometric characteristics of the Liebowitz Social Anxiety Scale in a Spanish adolescent sample. Depression and Anxiety 25, 977987.
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