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

Published online by Cambridge University Press:  01 August 2016

K. S. Blair ,
M. Otero ,
C. Teng ,
M. Geraci ,
E. Lewis ,
N. Hollon ,
R. J. R. Blair ,
Monique Ernst ,
C. Grillon  and
D. S. Pine
K. S. Blair*
Affiliation:
Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
M. Otero
Affiliation:
Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
C. Teng
Affiliation:
Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
M. Geraci
Affiliation:
Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
E. Lewis
Affiliation:
Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
N. Hollon
Affiliation:
Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
R. J. R. Blair
Affiliation:
Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
Monique Ernst
Affiliation:
Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
C. Grillon
Affiliation:
Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
D. S. Pine
Affiliation:
Department of Health and Human Services, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
*
*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: peschark@mail.nih.gov)
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Abstract

Background

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?

Method

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.

Results

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.

Conclusions

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.

Keywords

Amygdalaemotionsimagingmedial prefrontal cortexsocial anxiety
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 14 , October 2016 , pp. 2943 - 2953
Copyright
Copyright © Cambridge University Press 2016 

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References

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, 144–156.Google Scholar
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, 975–981.Google Scholar
Amodio, DM, Frith, CD (2006). Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience 7, 268–277.CrossRefGoogle ScholarPubMed
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, 1176–1184.Google Scholar
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, 1526–1532.CrossRefGoogle ScholarPubMed
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, 1202–1209.Google Scholar
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, 38–45.Google Scholar
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, 1193–1202.Google Scholar
Blair, RJR (2003). Facial expressions, their communicatory functions and neuro-cognitive substrates. Philosophical Transactions of the Royal Society of London Biological Sciences 358, 561–572.Google Scholar
Cox, RW (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research 29, 162–173.Google Scholar
Ekman, P, Friesen, WV (1976). Pictures of Facial Affect. Consulting Psychologists Press: Palo Alto, CA.Google Scholar
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, 496–505.Google Scholar
First, M, Spitzer, R, Gibbon, M, Williams, J (1997). Structured Clinical Interview for DSM-IV. American Psychiatric Press: Washington, DC.Google Scholar
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, 213–231.Google Scholar
Gamble, AL, Rapee, RM (2010). The time-course of attention to emotional faces in social phobia. Journal of Behavior Therapy and Experimental Psychiatry 41, 39–44.CrossRefGoogle ScholarPubMed
Goldin, PR, Gross, JJ (2010). Effects of mindfulness-based stress reduction (MBSR) on emotion regulation in social anxiety disorder. Emotion 10, 83–91.Google Scholar
Graham, R, Labar, KS (2012). Neurocognitive mechanisms of gaze-expression interactions in face processing and social attention. Neuropsychologia 50, 553–566.Google Scholar
Hermann, C, Ziegler, S, Birbaumer, N, Flor, H (2002). Psychophysiological and subjective indicators of aversive pavlovian conditioning in generalized social phobia. Biological Psychiatry 52, 328–337.Google Scholar
Hooker, CI, Germine, LT, D'Esposito, M (2006). Amygdala response to facial expressions reflects emotional learning. Journal of Neuroscience 26, 8915–8922.CrossRefGoogle Scholar
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, 482–488.CrossRefGoogle ScholarPubMed
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, 427–432.CrossRefGoogle Scholar
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, 537–544.Google Scholar
Mineka, S, Cook, M (1993). Mechanisms involved in the observational conditioning of fear. Journal of Experimental Psychology: General 122, 23–38.Google Scholar
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, 10–26.CrossRefGoogle Scholar
Mitchell, JP, Macrae, CN, Banaji, MR (2006). Dissociable medial prefrontal contributions to judgments of similar and dissimilar others. Neuron 50, 655–663.Google Scholar
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, 122–128.CrossRefGoogle ScholarPubMed
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, 265–268.Google Scholar
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, 440–457.CrossRefGoogle Scholar
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, 424–429.CrossRefGoogle ScholarPubMed
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, 863–871.Google Scholar
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, 1027–1034.Google Scholar
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, 921–930.Google Scholar
Straube, T, Mentzel, HJ, Miltner, WH (2005). Common and distinct brain activation to threat and safety signals in social phobia. Neuropsychobiology 52, 163–168.Google Scholar
Talairach, J, Tournoux, P (1988). Co-planar Stereotaxic Atlas of the Human Brain. Thieme: Stuttgart.Google Scholar
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, 233–236.Google Scholar
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