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Neural response to the observable self in social anxiety disorder

Published online by Cambridge University Press:  16 August 2012

J. Pujol*
Affiliation:
Institut d'Alta Tecnologia-PRBB, CRC Mar, Hospital de Mar, Barcelona, Spain
M. Giménez
Affiliation:
Institut d'Alta Tecnologia-PRBB, CRC Mar, Hospital de Mar, Barcelona, Spain
H. Ortiz
Affiliation:
Institut d'Alta Tecnologia-PRBB, CRC Mar, Hospital de Mar, Barcelona, Spain
C. Soriano-Mas
Affiliation:
Department of Psychiatry, Bellvitge University Hospital-IDIBELL, Barcelona, Spain Carlos III Health Institute, Ministry of Science and Innovation, CIBERSAM, Spain
M. López-Solà
Affiliation:
Institut d'Alta Tecnologia-PRBB, CRC Mar, Hospital de Mar, Barcelona, Spain Carlos III Health Institute, Ministry of Science and Innovation, CIBERSAM, Spain
M. Farré
Affiliation:
Human Pharmacology and Neurosciences, Hospital del Mar Research Institute (IMIM), Red RTA, Barcelona, Spain Department of Pharmacology, Therapeutics, and Toxicology, School of Medicine, Autonomous University of Barcelona, Spain
J. Deus
Affiliation:
Institut d'Alta Tecnologia-PRBB, CRC Mar, Hospital de Mar, Barcelona, Spain Department of Clinical and Health Psychology, Autonomous University of Barcelona, Spain
E. Merlo-Pich
Affiliation:
Neuronal Targets DPU, Respiratory CEDD, GlaxoSmithKline SpA, King of Prussia, PA, USA
B. J. Harrison
Affiliation:
Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne, Australia
N. Cardoner
Affiliation:
Department of Psychiatry, Bellvitge University Hospital-IDIBELL, Barcelona, Spain Carlos III Health Institute, Ministry of Science and Innovation, CIBERSAM, Spain
R. Navinés
Affiliation:
Human Pharmacology and Neurosciences, Hospital del Mar Research Institute (IMIM), Red RTA, Barcelona, Spain Clinical Institute of Neuroscience, Hospital Clínic-IDIBAPS, CIBERSAM, Barcelona, Spain
R. Martín-Santos
Affiliation:
Clinical Institute of Neuroscience, Hospital Clínic-IDIBAPS, CIBERSAM, Barcelona, Spain Department of Psychiatry and Clinical Psychobiology, University of Barcelona, Spain
*
*Address for correspondence: Dr J. Pujol, Department of Magnetic Resonance, CRC Mar, Hospital del Mar, Passeig Marítim 25–29, 08003 Barcelona, Spain. (Email: [email protected])

Abstract

Background

Distorted images of the observable self are considered crucial in the development and maintenance of social anxiety. We generated an experimental situation in which participants viewed themselves from an observer's perspective when exposed to scrutiny and evaluation by others.

Method

Twenty patients with social anxiety disorder (SAD) and 20 control subjects were assessed using functional magnetic resonance imaging (fMRI) during the public exposure of pre-recorded videos in which they were each shown performing a verbal task. The examiners acted as the audience in the experiment and rated performance. Whole-brain functional maps were computed using Statistical Parametric Mapping.

Results

Robust activation was observed in regions related to self-face recognition, emotional response and general arousal in both study groups. Patients showed significantly greater activation only in the primary visual cortex. By contrast, they showed significant deactivation or smaller activation in dorsal frontoparietal and anterior cingulate cortices relevant to the cognitive control of negative emotion. Task-related anxiety ratings revealed a pattern of negative correlation with activation in this frontoparietal/cingulate network. Importantly, the relationship between social anxiety scores and neural response showed an inverted-U function with positive correlations in the lower score range and negative correlations in the higher range.

Conclusions

Our findings suggest that exposure to scrutiny and evaluation in SAD may be associated with changes in cortical systems mediating the cognitive components of anxiety. Disorder severity seems to be relevant in shaping the neural response pattern, which is distinctively characterized by a reduced cortical response in the most severe cases.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2012

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References

APA (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn, text revision (DSM-IV-TR). American Psychiatric Association: Washington, DC.Google Scholar
Barrett, LF, Mesquita, B, Ochsner, KN, Gross, JJ (2007). The experience of emotion. Annual Review of Psychology 58, 373403.CrossRefGoogle ScholarPubMed
Bishop, S, Duncan, J, Brett, M, Lawrence, AD (2004). Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli. Nature Neuroscience 7, 184188.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Blair, KS, Geraci, M, Otero, M, Majestic, C, Odenheimer, S, Jacobs, M, Blair, RJ, Pine, DS (2011). Atypical modulation of medial prefrontal cortex to self-referential comments in generalized social phobia. Psychiatry Research 193, 3845.CrossRefGoogle ScholarPubMed
Campbell-Sills, L, Simmons, AN, Lovero, KL, Rochlin, AA, Paulus, MP, Stein, MB (2011). Functioning of neural systems supporting emotion regulation in anxiety-prone individuals. NeuroImage 54, 689696.CrossRefGoogle ScholarPubMed
Caseras, X, Mataix-Cols, D, Trasovares, MV, López-Solà, M, Ortriz, H, Pujol, J, Soriano-Mas, C, Giampietro, V, Brammer, MJ, Torrubia, R (2010). Dynamics of brain responses to phobic-related stimulation in specific phobia subtypes. European Journal of Neuroscience 32, 14141422.CrossRefGoogle ScholarPubMed
Clark, DM, Wells, A (1995). A cognitive model of social phobia. In Social Phobia: Diagnosis, Assessment, and Treatment (ed. Heimberg, R. G., Liebowitz, M. R., Hope, D. A. and Schneier, F. R.), pp. 6993. Guilford Press: New York.Google Scholar
Devue, C, Brédart, S (2011). The neural correlates of visual self-recognition. Consciousness and Cognition 20, 4051.CrossRefGoogle ScholarPubMed
Edelmann, RJ, Baker, SR (2002). Self-reported and actual physiological responses in social phobia. British Journal of Clinical Psychology 41, 114.CrossRefGoogle ScholarPubMed
Etkin, A, Wager, TD (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry 164, 14761488.CrossRefGoogle ScholarPubMed
Gerlach, AL, Mourlane, D, Rist, F (2004). Public and private heart rate feedback in social phobia: a manipulation of anxiety visibility. Cognitive Behaviour Therapy 33, 3645.CrossRefGoogle ScholarPubMed
Gerlach, AL, Wilhelm, FH, Gruber, K, Roth, WT (2001). Blushing and physiological arousability in social phobia. Journal of Abnormal Psychology 110, 247258.CrossRefGoogle ScholarPubMed
Giménez, M, Pujol, J, Ortiz, H, Soriano-Mas, C, López-Solà, M, Farré, M, Deus, J, Merlo-Pich, ME, Martín-Santos, R (2012). Altered brain functional connectivity in relation to perception of scrutiny in social anxiety disorder. Psychiatry Research. Published online: 18 July 2012. doi:10.1016/j.pscychresns.2011.10.008.CrossRefGoogle ScholarPubMed
Goldin, PR, Manber, T, Hakimi, S, Canli, T, Gross, JJ (2009 a). Neural bases of social anxiety disorder: emotional reactivity and cognitive regulation during social and physical threat. Archives of General Psychiatry 66, 170180.CrossRefGoogle ScholarPubMed
Goldin, PR, Manber-Ball, T, Werner, K, Heimberg, R, Gross, JJ (2009 b). Neural mechanisms of cognitive reappraisal of negative self-beliefs in social anxiety disorder. Biological Psychiatry 66, 10911099.CrossRefGoogle ScholarPubMed
Grossman, P, Wilhelm, FH, Kawachi, I, Sparrow, D (2001). Gender differences in psychophysiological responses to speech stress among older social phobics: congruence and incongruence between self-evaluative and cardiovascular reactions. Psychosomatic Medicine 63, 765777.CrossRefGoogle ScholarPubMed
Gur, RC, Gur, RE, Resnick, SM, Skolnick, BE, Alavi, A, Reivich, M (1987). The effect of anxiety on cortical cerebral blood flow and metabolism. Journal of Cerebral Blood Flow and Metabolism 7, 173177.CrossRefGoogle ScholarPubMed
Guy, W (ed)(1976). Clinical Global Impressions (CGI) Scale. ECDEU Assessment Manual for Psychopharmacology. US Department of Health, Education, and Welfare: Rockville, MD.Google Scholar
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 5662.CrossRefGoogle ScholarPubMed
Heimberg, RG, Hope, DA, Dodge, CS, Becker, RE (1990). DSM-III-R subtypes of social phobia. Comparison of generalized social phobics and public speaking phobics. Journal of Nervous and Mental Disease 178, 172179.CrossRefGoogle ScholarPubMed
Heiser, NA, Turner, SM, Beidel, DC, Roberson-Nay, R (2009). Differentiating social phobia from shyness. Journal of Anxiety Disorders 23, 469476.CrossRefGoogle ScholarPubMed
Hofmann, SG, Newman, MG, Ehlers, A, Roth, WT (1995). Psychophysiological differences between subgroups of social phobia. Journal of Abnormal Psychology 104, 224231.CrossRefGoogle ScholarPubMed
Horley, K, Williams, LM, Gonsalvez, C, Gordon, E (2003). Social phobics do not see eye to eye: a visual scanpath study of emotional expression processing. Journal of Anxiety Disorders 17, 3344.CrossRefGoogle ScholarPubMed
Kilts, CD, Kelsey, JE, Knight, B, Ely, TD, Bowman, FD, Gross, RE, Selvig, A, Gordon, A, Newport, DJ, Nemeroff, CB (2006). The neural correlates of social anxiety disorder and response to pharmacotherapy. Neuropsychopharmacology 31, 22432253.CrossRefGoogle ScholarPubMed
Levin, AP, Saoud, JB, Strauman, T, Gorman, JM, Fyer, AJ, Crawford, R, Liebowitz, MR (1993). Responses of ‘generalized’ and ‘discrete’ social phobics during public speaking. Journal of Anxiety Disorders 7, 207221.CrossRefGoogle Scholar
Lieberman, MD, Cunningham, WA (2009). Type I and type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience 4, 423428.CrossRefGoogle ScholarPubMed
Liebowitz, MR (1987). Social phobia. Modern Problems of Pharmacopsychiatry 22, 141173.CrossRefGoogle ScholarPubMed
Lorberbaum, JP, Kose, S, Johnson, MR, Arana, GW, Sullivan, LK, Hamner, MB, Ballenger, JC, Lydiard, RB, Brodrick, PS, Bohning, DE, George, MS (2004). Neural correlates of speech anticipatory anxiety in generalized social phobia. NeuroReport 5, 27012705.Google Scholar
Mauss, IB, Wilhelm, FH, Gross, JJ (2004). Is there less to social anxiety than meets the eye? Emotion experience, expression, and bodily responding. Cognition and Emotion 18, 631662.CrossRefGoogle Scholar
McTeague, LM, Shumen, JR, Wieser, MJ, Lang, PJ, Keil, A (2011). Social vision: sustained perceptual enhancement of affective facial cues in social anxiety. NeuroImage 54, 16151624.CrossRefGoogle ScholarPubMed
Nakao, T, Sanematsu, H, Yoshiura, T, Togao, O, Murayama, K, Tomita, M, Masuda, Y, Kanba, S (2011). fMRI of patients with social anxiety disorder during a social situation task. Neuroscience Research 69, 6772.CrossRefGoogle ScholarPubMed
Ochsner, KN, Gross, JJ (2005). The cognitive control of emotion. Trends in Cognitive Science 9, 242249.CrossRefGoogle ScholarPubMed
Phillips, ML, Ladouceur, CD, Drevets, WC (2008). A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry 13, 829857.CrossRefGoogle ScholarPubMed
Pujol, J, Harrison, BJ, Ortiz, H, Deus, J, Soriano-Mas, C, López-Solà, M, Yücel, M, Perich, X, Cardoner, N (2009). Influence of the fusiform gyrus on amygdala response to emotional faces in the non-clinical range of social anxiety. Psychological Medicine 39, 11771187.CrossRefGoogle ScholarPubMed
Quadflieg, S, Mohr, A, Mentzel, HJ, Miltner, WH, Straube, T (2008). Modulation of the neural network involved in the processing of anger prosody: the role of task-relevance and social phobia. Biological Psychology 78, 129137.CrossRefGoogle ScholarPubMed
Roth, DA, Heimberg, RG (2001). Cognitive-behavioral models of social anxiety disorder. Psychiatric Clinics of North America 24, 753771.CrossRefGoogle ScholarPubMed
Sabatinelli, D, Keil, A, Frank, DW, Lang, PJ (2012). Emotional perception: correspondence of early and late event-related potentials with cortical and subcortical functional MRI. Biological Psychiatry. Published online: 26 April 2012. doi:10.1016/j.biopsycho.2012.04.005.Google ScholarPubMed
Sabatinelli, D, Lang, PJ, Keil, A, Bradley, MM (2007). Emotional perception: correlation of functional MRI and event-related potentials. Cerebral Cortex 17, 10841091.Google ScholarPubMed
Schmidt, S, Mohr, A, Miltner, WH, Straube, T (2010). Task-dependent neural correlates of the processing of verbal threat-related stimuli in social phobia. Biological Psychology 84, 304312.CrossRefGoogle ScholarPubMed
Schmitz, J, Krämer, M, Tuschen-Caffier, B, Heinrichs, N, Blechert, J (2011). Restricted autonomic flexibility in children with social phobia. Journal of Child Psychology and Psychiatry 52, 12031211.CrossRefGoogle ScholarPubMed
Shah, SG, Klumpp, H, Angstadt, M, Nathan, PJ, Phan, KL (2009). Amygdala and insula response to emotional images in patients with generalized social anxiety disorder. Journal of Psychiatry and Neuroscience 34, 296302.Google ScholarPubMed
Sheehan, DV, Lecrubier, Y (1999). M.I.N.I. Mini International Neuropsychiatric Interview. Spanish version 5.0.0 edited by Ferrendo, L., Bobes, J. M. and Gilbert, J.. Instituto IAP: Madrid.Google Scholar
Spielberger, C (1983). Manual for the State-Trait Anxiety Inventory (Form Y). Consulting Psychologists: Palo Alto, CA.Google Scholar
Spitzer, RL, Kroenke, K, Williams, JB (1999). Validation and utility of a self-report version of PRIME-MD: the PHQ primary care study. Journal of the American Medical Association 282, 17371744.CrossRefGoogle ScholarPubMed
Staugaard, SR (2010). Threatening faces and social anxiety: a literature review. Clinical Psychology Review 30, 669690.CrossRefGoogle ScholarPubMed
Straube, T, Schmidt, S, Weiss, T, Mentzel, HJ, Miltner, WH (2009). Dynamic activation of the anterior cingulate cortex during anticipatory anxiety. NeuroImage 44, 975981.CrossRefGoogle ScholarPubMed
Tillfors, M, Furmark, T, Marteinsdottir, I, Fischer, H, Pissiota, A, Långström, 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.CrossRefGoogle ScholarPubMed
Van Ameringen, M, Mancini, C, Szechtman, H, Nahmias, C, Oakman, JM, Hall, GB, Pipe, B, Farvolden, P (2004). A PET provocation study of generalized social phobia. Psychiatry Research 132, 1318.CrossRefGoogle ScholarPubMed
Wardenaar, KJ, Vreeburg, SA, van Veen, T, Giltay, EJ, Veen, G, Penninx, BW, Zitman, FG (2011). Dimensions of depression and anxiety and the hypothalamo-pituitary-adrenal axis. Biological Psychiatry 69, 366373.CrossRefGoogle ScholarPubMed
Wechsler, D (1987). The Wechsler Memory Scale – Revised. Psychological Corporation: San Antonio, TX.Google Scholar
Wild, J, Clark, DM, Ehlers, A, McManus, F (2008). Perception of arousal in social anxiety: effects of false feedback during a social interaction. Journal of Behavior Therapy and Experimental Psychiatry 39, 102116.CrossRefGoogle ScholarPubMed
Yerkes, RM, Dodson, JD (1908). The relation of strength of stimulus to rapidity of habit-formation. Journal of Comparative Neurology and Psychology 18, 459482.CrossRefGoogle Scholar
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