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Learning from other people's fear: amygdala-based social reference learning in social anxiety disorder

  • K. S. Blair (a1), M. Otero (a1), C. Teng (a1), M. Geraci (a1), E. Lewis (a1), N. Hollon (a1), R. J. R. Blair (a1), Monique Ernst (a1), C. Grillon (a1) and D. S. Pine (a1)...



Social anxiety disorder involves fear of social objects or situations. Social referencing may play an important role in the acquisition of this fear and could be a key determinant in future biomarkers and treatment pathways. However, the neural underpinnings mediating such learning in social anxiety are unknown. Using event-related functional magnetic resonance imaging, we examined social reference learning in social anxiety disorder. Specifically, would patients with the disorder show increased amygdala activity during social reference learning, and further, following social reference learning, show particularly increased response to objects associated with other people's negative reactions?


A total of 32 unmedicated patients with social anxiety disorder and 22 age-, intelligence quotient- and gender-matched healthy individuals responded to objects that had become associated with others’ fearful, angry, happy or neutral reactions.


During the social reference learning phase, a significant group × social context interaction revealed that, relative to the comparison group, the social anxiety group showed a significantly greater response in the amygdala, as well as rostral, dorsomedial and lateral frontal and parietal cortices during the social, relative to non-social, referencing trials. In addition, during the object test phase, relative to the comparison group, the social anxiety group showed increased bilateral amygdala activation to objects associated with others’ fearful reactions, and a trend towards decreased amygdala activation to objects associated with others’ happy and neutral reactions.


These results suggest perturbed observational learning in social anxiety disorder. In addition, they further implicate the amygdala and dorsomedial prefrontal cortex in the disorder, and underscore their importance in future biomarker developments.


Corresponding author

*Address for correspondence: K. S. Blair, Ph.D., Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, 15K North Drive, Room 115A, MSC 2670, Bethesda, MD 20892-2670, USA. (Email:


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Aktar, E, Majdandzic, M, de Vente, W, Bogels, SM (2013). The interplay between expressed parental anxiety and infant behavioural inhibition predicts infant avoidance in a social referencing paradigm. Journal of Child Psychology and Psychiatry 54, 144156.
Amir, N, Klumpp, H, Elias, J, Bedwell, JS, Yanasak, N, Miller, LS (2005). Increased activation of the anterior cingulate cortex during processing of disgust faces in individuals with social phobia. Biological Psychiatry 57, 975981.
Amodio, DM, Frith, CD (2006). Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience 7, 268277.
Blair, KS, Geraci, M, Devido, G, McCaffrey, D, Gang, C, Vythilingam, M, Ng, P, Hollon, NG, Jones, M, Blair, RJR, Pine, DS (2008 a). Neural response to self- and other referential praise and criticism in generalized social phobia. Archives of General Psychiatry 65, 11761184.
Blair, KS, Geraci, M, Hollon, N, Otero, M, DeVido, J, Majestic, C, Jacobs, M, Blair, RJ, Pine, DS (2010). Social norm processing in adult social phobia: atypically increased ventromedial frontal cortex responsiveness to unintentional (embarrassing) transgressions. American Journal of Psychiatry 167, 15261532.
Blair, KS, Geraci, M, Korelitz, K, Otero, M, Towbin, K, Ernst, M, Leibenluft, E, Blair, RJ, Pine, DS (2011 a). The pathology of social phobia is independent of developmental changes in face processing. American Journal of Psychiatry 168, 12021209.
Blair, KS, Geraci, M, Otero, M, Majestic, C, Odenheimer, S, Jacobs, M, Blair, RJ, Pine, DS (2011 b). Atypical modulation of medial prefrontal cortex to self-referential comments in generalized social phobia. Psychiatry Research 193, 3845.
Blair, KS, Shaywitz, J, Smith, BW, Rhodes, R, Geraci, M, Jones, M, McCaffrey, D, Vythilingam, M, Finger, E, Mondillo, K, Jacobs, M, Charney, D, Blair, RJR, Drevets, WC, Pine, DS (2008 b). Response to emotional expressions in generalized social phobia (GSP) and generalized anxiety disorder (GAD): evidence for separate disorders. American Journal of Psychiatry 165, 11931202.
Blair, RJR (2003). Facial expressions, their communicatory functions and neuro-cognitive substrates. Philosophical Transactions of the Royal Society of London Biological Sciences 358, 561572.
Cox, RW (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research 29, 162173.
Ekman, P, Friesen, WV (1976). Pictures of Facial Affect. Consulting Psychologists Press: Palo Alto, CA.
Evans, KC, Wright, CI, Wedig, MM, Gold, AL, Pollack, MH, Rauch, SL (2008). A functional MRI study of amygdala responses to angry schematic faces in social anxiety disorder. Depression and Anxiety 25, 496505.
First, M, Spitzer, R, Gibbon, M, Williams, J (1997). Structured Clinical Interview for DSM-IV. American Psychiatric Press: Washington, DC.
Fisak, B Jr., Grills-Taquechel, AE (2007). Parental modeling, reinforcement, and information transfer: risk factors in the development of child anxiety? Clinical Child and Family Psychology Review 10, 213231.
Gamble, AL, Rapee, RM (2010). The time-course of attention to emotional faces in social phobia. Journal of Behavior Therapy and Experimental Psychiatry 41, 3944.
Goldin, PR, Gross, JJ (2010). Effects of mindfulness-based stress reduction (MBSR) on emotion regulation in social anxiety disorder. Emotion 10, 8391.
Graham, R, Labar, KS (2012). Neurocognitive mechanisms of gaze-expression interactions in face processing and social attention. Neuropsychologia 50, 553566.
Hermann, C, Ziegler, S, Birbaumer, N, Flor, H (2002). Psychophysiological and subjective indicators of aversive pavlovian conditioning in generalized social phobia. Biological Psychiatry 52, 328337.
Hooker, CI, Germine, LT, D'Esposito, M (2006). Amygdala response to facial expressions reflects emotional learning. Journal of Neuroscience 26, 89158922.
Jeon, D, Kim, S, Chetana, M, Jo, D, Ruley, HE, Lin, SY, Rabah, D, Kinet, JP, Shin, HS (2010). Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nature Neuroscience 13, 482488.
Klinnert, MD, Emde, RN, Butterfield, P, Campos, JJ (1986). Social referencing: the infant's use of emotional signals from a friendly adult with mother present. Developmental Psychology 22, 427432.
Meffert, H, Brislin, SJ, White, SF, Blair, JR (2015). Prediction errors to emotional expressions: the roles of the amygdala in social referencing. Social Cognitive and Affective Neuroscience 10, 537544.
Mineka, S, Cook, M (1993). Mechanisms involved in the observational conditioning of fear. Journal of Experimental Psychology: General 122, 2338.
Mineka, S, Zinbarg, R (2006). A contemporary learning theory perspective on the etiology of anxiety disorders: it's not what you thought it was. American Psychology 61, 1026.
Mitchell, JP, Macrae, CN, Banaji, MR (2006). Dissociable medial prefrontal contributions to judgments of similar and dissimilar others. Neuron 50, 655663.
Moriya, J, Tanno, Y (2011). The time course of attentional disengagement from angry faces in social anxiety. Journal of Behavior Therapy and Experimental Psychiatry 42, 122128.
Muris, P, Steerneman, P, Merckelbach, H, Meesters, C (1996). The role of parental fearfulness and modeling in children's fear. Behavior Research and Therapy 34, 265268.
Northoff, G, Heinzel, A, de Greck, M, Bermpohl, F, Dobrowolny, H, Panksepp, J (2006). Self-referential processing in our brain – a meta-analysis of imaging studies on the self. NeuroImage 31, 440457.
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.
Schneider, F, Weiss, U, Kessler, C, Muller-Gartner, HW, Posse, S, Salloum, JB, Grodd, W, Himmelmann, F, Gaebel, W, Birbaumer, N (1999). Subcortical correlates of differential classical conditioning of aversive emotional reactions in social phobia. Biological Psychiatry 45, 863871.
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.
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. Thieme: Stuttgart.
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.


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Learning from other people's fear: amygdala-based social reference learning in social anxiety disorder

  • K. S. Blair (a1), M. Otero (a1), C. Teng (a1), M. Geraci (a1), E. Lewis (a1), N. Hollon (a1), R. J. R. Blair (a1), Monique Ernst (a1), C. Grillon (a1) and D. S. Pine (a1)...


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