Emotion regulation in social anxiety disorder: behavioral and neural responses to three socio-emotional tasks

Biology of Mood & Anxiety Disorders

Michal Ziv¹  Philippe R Goldin¹  Hooria Jazaieri¹  Kevin S Hahn¹  James J Gross¹ 

[1] Department of Psychology, Stanford University, Jordan Hall, Bldg. 420, 94305-2130 Stanford, CA, USA

关键词: Temporal dynamics;    DMPFC;    fMRI;    Reappraisal;    Emotion regulation;    Social anxiety;   

Others  :  791822
DOI  :  10.1186/2045-5380-3-20

 received in 2013-05-27, accepted in 2013-10-23,  发布年份 2013

【 摘 要 】

Background

Social anxiety disorder (SAD) is thought to involve deficits in emotion regulation, and more specifically, deficits in cognitive reappraisal. However, evidence for such deficits is mixed.

Methods

Using functional magnetic resonance imaging (fMRI) of blood oxygen-level dependent (BOLD) signal, we examined reappraisal-related behavioral and neural responses in 27 participants with generalized SAD and 27 healthy controls (HC) during three socio-emotional tasks: (1) looming harsh faces (Faces); (2) videotaped actors delivering social criticism (Criticism); and (3) written autobiographical negative self-beliefs (Beliefs).

Results

Behaviorally, compared to HC, participants with SAD had lesser reappraisal-related reduction in negative emotion in the Beliefs task. Neurally, compared to HC, participants with SAD had lesser BOLD responses in reappraisal-related brain regions when reappraising faces, in visual and attention related regions when reappraising criticism, and in the left superior temporal gyrus when reappraising beliefs. Examination of the temporal dynamics of BOLD responses revealed late reappraisal-related increased responses in HC, compared to SAD. In addition, the dorsomedial prefrontal cortex (DMPFC), which showed reappraisal-related increased activity in both groups, had similar temporal dynamics in SAD and HC during the Faces and Criticism tasks, but greater late response increases in HC, compared to SAD, during the Beliefs task. Reappraisal-related greater late DMPFC responses were associated with greater percent reduction in negative emotion ratings in SAD patients.

Conclusions

These results suggest a dysfunction of cognitive reappraisal in SAD patients, with overall reduced late brain responses in prefrontal regions, particularly when reappraising faces. Decreased late activity in the DMPFC might be associated with deficient reappraisal and greater negative reactivity.

Trial registration

ClinicalTrials.gov identifier: NCT00380731

【 授权许可】

   
2013 Ziv et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Stein MB, Stein DJ: Social anxiety disorder. Lancet 2008, 371:1115-1125.
• [2]Hofmann SG: Cognitive mediation of treatment change in social phobia. J Consult Clin Psychol 2004, 72:393-399.
• [3]Goldin PR, Manber-Ball T, Werner K, Heimberg R, Gross JJ: Neural mechanisms of cognitive reappraisal of negative self-beliefs in social anxiety disorder. Biol Psychiatry 2009, 66:1091-1099.
• [4]Gross JJ: Handbook of emotion regulation. New York, NY: Guilford Press; 2007.
• [5]Goldin PR, Manber T, Hakimi S, Canli T, Gross JJ: Neural bases of social anxiety disorder: emotional reactivity and cognitive regulation during social and physical threat. Arch Gen Psychiatry 2009, 66:170-180.
• [6]Lorberbaum JP, Kose S, Johnson MR, Arana GW, Sullivan LK, Hamner MB, Ballenger JC, Lydiard RB, Brodrick PS, Bohning DE, George MS: Neural correlates of speech anticipatory anxiety in generalized social phobia. Neuroreport 2004, 15:2701-2705.
• [7]Blair K, Geraci M, Devido J, McCaffrey D, Chen G, Vythilingam M, Ng P, Hollon N, Jones M, Blair RJ, Pine DS: Neural response to self- and other referential praise and criticism in generalized social phobia. Arch Gen Psychiatry 2008, 65:1176-1184.
• [8]Guyer AE, Lau JY, McClure-Tone EB, Parrish J, Shiffrin ND, Reynolds RC, Chen G, Blair RJ, Leibenluft E, Fox NA, et al.: Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Arch Gen Psychiatry 2008, 65:1303-1312.
• [9]Sripada CS, Angstadt M, Banks S, Nathan PJ, Liberzon I, Phan KL: Functional neuroimaging of mentalizing during the trust game in social anxiety disorder. Neuroreport 2009, 20:984-989.
• [10]Ziv M, Goldin PR, Jazaieri H, Hahn KS, Gross JJ: Is there less to social anxiety than meets the eye? Behavioral and neural responses to three socio-emotional tasks. Biol Mood Anxiety Disord 2013, 3:5. BioMed Central Full Text
• [11]Bruhl AB, Herwig U, Delsignore A, Jancke L, Rufer M: General emotion processing in social anxiety disorder: neural issues of cognitive control. Psychiatry Res 2013, 212:108-115.
• [12]Freitas-Ferrari MC, Hallak JE, Trzesniak C, Filho AS, Machado-de-Sousa JP, Chagas MH, Nardi AE, Crippa JA: Neuroimaging in social anxiety disorder: a systematic review of the literature. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:565-580.
• [13]Goldin PR, Gross JJ: Effects of mindfulness-based stress reduction (MBSR) on emotion regulation in social anxiety disorder. Emotion 2010, 10:83-91.
• [14]Goldin P, Ziv M, Jazaieri H, Gross JJ: Randomized controlled trial of mindfulness-based stress reduction versus aerobic exercise: effects on the self-referential brain network in social anxiety disorder. Front Hum Neurosci 2012, 6:295.
• [15]Campbell DW, Sareen J, Paulus MP, Goldin PR, Stein MB, Reiss JP: Time-varying amygdala response to emotional faces in generalized social phobia. Biol Psychiatry 2007, 62:455-463.
• [16]DSM-IV-TR: Diagnostic and statistical manual of mental disorders. 4th edition. Washington, DC: American Psychiatric Association; 1994:2000.
• [17]DiNardo PA, Brown TA, Barlow DH: Anxiety disorders interview schedule for DSM-IV: lifetime version (ADIS-IV-L). Albany, NY: Graywind Publications, Inc; 1994.
• [18]Oldfield RC: The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
• [19]Liebowitz MR: Social phobia. Mod Probl Pharmacopsychiatry 1987, 22:141-173.
• [20]Fresco DM, Coles ME, Heimberg RG, Liebowitz MR, Hami S, Stein MB, Goetz D: The Liebowitz social anxiety scale: a comparison of the psychometric properties of self-report and clinician-administered formats. Psychol Med 2001, 31:1025-1035.
• [21]Ochsner KN, Ray RD, Cooper JC, Robertson ER, Chopra S, Gabrieli JD, Gross JJ: For better or for worse: neural systems supporting the cognitive down-and up-regulation of negative emotion. Neuroimage 2004, 23:483-499.
• [22]Ekman P, Friesen W: Facial action coding system: a technique for the measurment of facial movement. Palo Alto, CA: Consulting Psychologists Press; 1978.
• [23]Glover GH, Law CS: Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn Reson Med 2001, 46:515-522.
• [24]Cox RW: AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 1996, 29:162-173.
• [25]Cohen MS: Parametric analysis of fMRI data using linear systems methods. Neuroimage 1997, 6:93-103.
• [26]Talairach J, Tournoux P: Co-planar stereotaxic atlas of the human brain. New York, NY: Thieme; 1988.
• [27]Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC: Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 1995, 33:636-647.
• [28]Mcclure EB, Pine DS: Social anxiety and emotion regulation: A model for developmental psychopathology perspectives on anxiety disorders. In Developmental Psychopathology, Risk, Disorder, and Adaptation. 2nd edition. Edited by Cicchetti D, Cohen DJ. Hoboken, New Jersey: John Wiley & Sons; 2006:470-50.
• [29]Ochsner KN, Silvers JA, Buhle JT: Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Ann N Y Acad Sci 2012, 1251:E1-E24.
• [30]Stein MB, Goldin PR, Sareen J, Zorrilla LT, Brown GG: Increased amygdala activation to angry and contemptuous faces in generalized social phobia. Arch Gen Psychiatry 2002, 59:1027-1034.
• [31]Schultz LT, Heimberg RG: Attentional focus in social anxiety disorder: potential for interactive processes. Clin Psychol Rev 2008, 28:1206-1221.
• [32]Lundh LG, Ost LG: Recognition bias for critical faces in social phobics. Behav Res Ther 1996, 34:787-794.
• [33]Horley K, Williams LM, Gonsalvez C, Gordon E: Face to face: visual scanpath evidence for abnormal processing of facial expressions in social phobia. Psychiatry Res 2004, 127:43-53.
• [34]O’Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ: Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 2004, 304:452-454.
• [35]Vrticka P, Simioni S, Fornari E, Schluep M, Vuilleumier P, Sander D: Neural substrates of social emotion regulation: a FMRI study on imitation and expressive suppression to dynamic facial signals. Front Psychol 2013, 4:95.
• [36]Mueller EM, Hofmann SG, Santesso DL, Meuret AE, Bitran S, Pizzagalli DA: Electrophysiological evidence of attentional biases in social anxiety disorder. Psychol Med 2009, 39:1141-1152.
• [37]McRae K, Gross JJ, Weber J, Robertson ER, Sokol-Hessner P, Ray RD, Gabrieli JD, Ochsner KN: The development of emotion regulation: an fMRI study of cognitive reappraisal in children, adolescents and young adults. Soc Cogn Affect Neurosci 2012, 7:11-22.
• [38]Van der Meer L, Costafreda S, Aleman A, David AS: Self-reflection and the brain: a theoretical review and meta-analysis of neuroimaging studies with implications for schizophrenia. Neurosci Biobehav Rev 2010, 34:935-946.
• [39]Northoff G, Bermpohl F: Cortical midline structures and the self. Trends Cogn Sci 2004, 8:102-107.
• [40]Lemogne C, Delaveau P, Freton M, Guionnet S, Fossati P: Medial prefrontal cortex and the self in major depression. J Affect Disord 2012, 136:e1-e11.
• [41]Goldin PR, McRae K, Ramel W, Gross JJ: The neural bases of emotion regulation: reappraisal and suppression of negative emotion. Biol Psychiatry 2008, 63:577-586.