Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-28T20:59:07.581Z Has data issue: false hasContentIssue false
  • English
  • Français

Altered cortical-amygdala coupling in social anxiety disorder during the anticipation of giving a public speech

Published online by Cambridge University Press:  26 November 2014

H. R. Cremers ,
I. M. Veer ,
P. Spinhoven ,
S. A. R. B. Rombouts ,
T. Yarkoni ,
T. D. Wager  and
K. Roelofs
H. R. Cremers*
Affiliation:
Behavioral Science Institute (BSI), Radboud University, Nijmegen, The Netherlands Biological Science Division, Department of Psychiatry, University of Chicago, USA Leiden Institute for Brain and Cognition (LIBC), Leiden, The Netherlands
I. M. Veer
Affiliation:
Leiden Institute for Brain and Cognition (LIBC), Leiden, The Netherlands Division of Mind and Brain Research, Department of Psychiatry and Psychotherapy, Charité Universitätsmedizin, Berlin, Germany
P. Spinhoven
Affiliation:
Leiden Institute for Brain and Cognition (LIBC), Leiden, The Netherlands Institute of Psychology, Leiden University, The Netherlands
S. A. R. B. Rombouts
Affiliation:
Leiden Institute for Brain and Cognition (LIBC), Leiden, The Netherlands Institute of Psychology, Leiden University, The Netherlands Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands
T. Yarkoni
Affiliation:
Department of Psychology, University of Texas, Austin, USA
T. D. Wager
Affiliation:
Department of Psychology and Neuroscience, University of Colorado, Boulder, USA
K. Roelofs
Affiliation:
Behavioral Science Institute (BSI), Radboud University, Nijmegen, The Netherlands Donders Institute for Brain, Cognition and Behavior, Nijmegen, The Netherlands
*
*Address for correspondence: Dr H. R. Cremers, Department of Psychiatry MC 3077, The University of Chicago, 5841 South Maryland Avenue, L-460, Chicago, IL 60637, USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Severe stress in social situations is a core symptom of social anxiety disorder (SAD). Connectivity between the amygdala and cortical regions is thought to be important for emotion regulation, a function that is compromised in SAD. However, it has never been tested if and how this connectivity pattern changes under conditions of stress-inducing social evaluative threat. Here we investigate changes in cortical-amygdala coupling in SAD during the anticipation of giving a public speech.

Method

Twenty individuals with SAD and age-, gender- and education-matched controls (n = 20) participated in this study. During the functional magnetic resonance imaging (fMRI) session, participants underwent three ‘resting-state’ fMRI scans: one before, one during, and one after the anticipation of giving a public speech. Functional connectivity between cortical emotion regulation regions and the amygdala was investigated.

Results

Compared to controls, SAD participants showed reduced functional integration between cortical emotion regulation regions and the amygdala during the public speech anticipation. Moreover, in SAD participants cortical-amygdala connectivity changes correlated with social anxiety symptom severity.

Conclusions

The distinctive pattern of cortical-amygdala connectivity suggests less effective cortical-subcortical communication during social stress-provoking situations in SAD.

Keywords

Amygdalacortexemotion regulationfMRIsocial anxietyspeech anticipation
Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 7 , May 2015 , pp. 1521 - 1529
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amstadter, A (2008). Emotion regulation and anxiety disorders. Journal of Anxiety Disorders 22, 211–221.CrossRefGoogle ScholarPubMed
American Psychiatric Association (1994). Diagnostic and Statistical Manual of Mental Disorders (DSM), 4th edn. American Psychiatric Press: Washington.Google Scholar
Arnsten, AFT (2009). Stress signalling pathways that impair prefrontal cortex structure and function. Nature Reviews Neuroscience 10, 410–422.CrossRefGoogle ScholarPubMed
Beck, AT, Steer, RA, Carbin, MG (1988). Psychometric properties of the Beck Depression Inventory: twenty-five years of evaluation. Clinical Psychology Review 8, 77–100.CrossRefGoogle Scholar
Blöte, AW, Kint, MJW, Miers, AC, Westenberg, PM (2009). The relation between public speaking anxiety and social anxiety: a review. Journal of Anxiety Disorders 23, 305–313.CrossRefGoogle ScholarPubMed
Bressler, SL, Menon, V (2010). Large-scale brain networks in cognition: emerging methods and principles. Elsevier Ltd Trends in Cognitive Sciences 14, 277–290.CrossRefGoogle ScholarPubMed
Buhle, JT, Silvers, JA, Wager, TD, Lopez, R, Onyemekwu, C, Kober, H, Weber, J, Ochsner, KN (2014). Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cerebral Cortex 24, 2981–2990.CrossRefGoogle ScholarPubMed
Button, KS, Ioannidis, JPA, Mokrysz, C, Nosek, BA, Flint, J, Robinson, ESJ, Munafò, MR (2013). Power failure: why small sample size undermines the reliability of neuroscience. Nature Reviews Neuroscience 14, 365–376.CrossRefGoogle ScholarPubMed
Carver, C, White, T (1994). Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales. Journal of Personality and Social Psychology 67, 319–333.CrossRefGoogle Scholar
Choi, JM, Padmala, S, Pessoa, L (2012). Impact of state anxiety on the interaction between threat monitoring and cognition. NeuroImage 59, 1912–1923.CrossRefGoogle ScholarPubMed
Cole, DM, Smith, SM, Beckmann, CF (2010). Advances and pitfalls in the analysis and interpretation of resting-state FMRI data. Frontiers in Systems Neuroscience 4, 8.Google ScholarPubMed
Costa, PT, McCrea, RR (1992). Revised Neo Personality Inventory (Neo PI-R) and Neo Five-Factor Inventory (NEO-FFI). Psychological Assessment Resources: Odessa, FL.Google Scholar
Davidson, RJ, Marshall, JR, Tomarken, AJ, Henriques, JB (2000). While a phobic waits: regional brain electrical and autonomic activity in social phobics during anticipation of public speaking. Biological Psychiatry 47, 85–95.CrossRefGoogle ScholarPubMed
Diekhof, EK, Geier, K, Falkai, P, Gruber, O (2011). Fear is only as deep as the mind allows: a coordinate-based meta-analysis of neuroimaging studies on the regulation of negative affect. NeuroImage 58, 275–285.CrossRefGoogle ScholarPubMed
Etkin, A, Wager, T (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in ptsd, social anxiety disorder, and specific phobia. American Journal of Psychiatry 167, 1–13.Google Scholar
Faria, V, Appel, L, Åhs, F, Linnman, C, Pissiota, A, Frans, O, Bani, M, Bettica, P, Pich, EM, Jacobsson, E, Wahlstedt, K, Fredrikson, M, Furmark, T (2012). Amygdala subregions tied to SSRI and placebo response in patients with social anxiety disorder. Neuropsychopharmacology 37, 2222–2223.CrossRefGoogle ScholarPubMed
Feder, A, Nestler, EJ, Charney, DS (2009). Psychobiology and molecular genetics of resilience. Nature Reviews Neuroscience 10, 446–457.CrossRefGoogle ScholarPubMed
Freese, JL, Amaral, DG (2009). Anatomy of the primate amygdala. In The Human Amygdala (ed. Whalen, P. J. & Phelps, E. A.), pp. 3–42. Guilford: New York.Google Scholar
Fresco, DM, Coles, ME, Heimberg, RG, Liebowitz, MR, Hami, S, Stein, MB, Goetz, D (2001). The Liebowitz Social Anxiety Scale: a comparison of the psychometric properties of self-report and clinician-administered formats. Psychological Medicine 31, 1025–1035.CrossRefGoogle Scholar
Furmark, T, Appel, L, Michelgård, Å, Wahlstedt, K, Åhs, F, Zancan, S, Jacobsson, E, Flyckt, K, Grohp, M, Bergström, M, Pich, EM, Nilsson, L-G, Bani, M, Långström, B, Fredrikson, M (2005). Cerebral blood flow changes after treatment of social phobia with the neurokinin-1 antagonist GR205171, citalopram, or placebo. Biological Psychiatry 58, 132–142.CrossRefGoogle ScholarPubMed
Giménez, M, Ortiz, H, Soriano-Mas, C, López-Solà, M, Farré, M, Deus, J, Martín-Santos, R, Fernandes, S, Fina, P, Bani, M, Zancan, S, Pujol, J, Merlo-Pich, E (2014). Functional effects of chronic paroxetine versus placebo on the fear, stress and anxiety brain circuit in Social Anxiety Disorder: initial validation of an imaging protocol for drug discovery. European Neuropsychopharmacology 24, 105–116.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, 170–180.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, 1091–1099.CrossRefGoogle ScholarPubMed
Goldin, PR, Ziv, M, Jazaieri, H, Hahn, K, Heimberg, R, Gross, JJ (2013). Impact of cognitive behavioral therapy for social anxiety disorder on the neural dynamics of cognitive reappraisal of negative self-beliefs: randomized clinical trial. JAMA Psychiatry 70, 1048–1056.CrossRefGoogle ScholarPubMed
Gramer, M, Saria, K (2007). Effects of social anxiety and evaluative threat on cardiovascular responses to active performance situations. Biological Psychology 74, 67–74.CrossRefGoogle ScholarPubMed
Gross, JJ (2010). The future's so bright, I Gotta wear shades. Emotion Review 2, 212–216.CrossRefGoogle Scholar
Henckens, MJAG, van Wingen, GA, Joëls, M, Fernández, G (2011). Corticosteroid induced decoupling of the amygdala in men. Cerebral Cortex 22, 2336–2345.CrossRefGoogle ScholarPubMed
Joëls, M, Baram, TZ (2009). The neuro-symphony of stress. Nature Publishing Group Nature Reviews Neuroscience 10, 459–466.CrossRefGoogle ScholarPubMed
Lee, H, Heller, AS, van Reekum, CM, Nelson, B, Davidson, RJ (2012). Amygdala-prefrontal coupling underlies individual differences in emotion regulation. NeuroImage 62, 1575–1581.CrossRefGoogle ScholarPubMed
Loftus, GR, Masson, MEJ (1994). Using confidence intervals in within-subject designs. Springer Psychonomic Bulletin & Review 1, 476–490.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 15, 2701–2705.Google ScholarPubMed
Margulies, DS, Böttger, J, Long, X, Lv, Y, Kelly, C, Schäfer, A, Goldhahn, D, Abbushi, A, Milham, MP, Lohmann, G, Villringer, A (2010). Resting developments: a review of fMRI post-processing methodologies for spontaneous brain activity. Magnetic Resonance Materials in Physics, Biology and Medicine 23, 289–307.CrossRefGoogle ScholarPubMed
Moscovitch, DA, Chiupka, CA, Gavric, DL (2013). Within the mind's eye: negative mental imagery activates different emotion regulation strategies in high versus low socially anxious individuals. Journal of Behavior Therapy and Experimental Psychiatry 44, 426–432.CrossRefGoogle ScholarPubMed
Phan, KL, Coccaro, EF, Angstadt, M, Kreger, KJ, Mayberg, HS, Liberzon, I, Stein, MB (2013). Corticolimbic brain reactivity to social signals of threat before and after sertraline treatment in generalized social phobia. Biological Psychiatry 73, 329–336.CrossRefGoogle ScholarPubMed
Pruessner, JC, Dedovic, K, Khalili-Mahani, N, Engert, V, Pruessner, M, Buss, C, Renwick, R, Dagher, A, Meaney, MJ, Lupien, S (2008). Deactivation of the limbic system during acute psychosocial stress: evidence from positron emission tomography and functional magnetic resonance imaging studies. Biological Psychiatry 63, 234–240.CrossRefGoogle ScholarPubMed
Rodrigues, SM, LeDoux, JE, Sapolsky, RM (2009). The influence of stress hormones on fear circuitry. Annual Review of Neuroscience 32, 289–313.CrossRefGoogle ScholarPubMed
Roelofs, K, van Peer, J, Berretty, E, Jong, P, Spinhoven, P, Elzinga, BM (2009). Hypothalamus–pituitary–adrenal axis hyperresponsiveness is associated with increased social avoidance behavior in social phobia. Society of Biological Psychiatry Biological Psychiatry 65, 336–343.CrossRefGoogle ScholarPubMed
Shackman, AJ, Fox, AS, Oler, JA, Shelton, SE, Davidson, RJ, Kalin, NH (2013). Neural mechanisms underlying heterogeneity in the presentation of anxious temperament. Proceedings of the National Academy of Sciences USA 110, 6145–6150.CrossRefGoogle ScholarPubMed
Sheehan, D, Lecrubier, Y, Harnett Sheehan, K, Janavs, J, Weiller, E, Keskiner, A, Schinka, J, Knapp, E, Sheehan, M, Dunbar, G (1997). The validity of the Mini International Neuropsychiatric Interview (MINI) according to the SCID-P and its reliability. European Psychiatry 12, 232–241.CrossRefGoogle Scholar
Smith, SM, Jenkinson, M, Woolrich, MW, Beckmann, CF, Behrens, TEJ, Johansen-Berg, H, Bannister, PR, De Luca, M, Drobnjak, I, Flitney, DE, Niazy, RK, Saunders, J, Vickers, J, Zhang, Y, De Stefano, N, Brady, JM, Matthews, PM (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23, S208–S219.CrossRefGoogle ScholarPubMed
Spreckelmeyer, KN, Krach, S, Kohls, G, Rademacher, L, Irmak, A, Konrad, K, Kircher, T, Gründer, G (2009). Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. Social Cognitive and Affective Neuroscience 4, 158–165.CrossRefGoogle ScholarPubMed
Tillfors, M, Furmark, T, Marteinsdottir, I, Fredrikson, M (2002). Cerebral blood flow during anticipation of public speaking in social phobia: a PET study. Biological Psychiatry 52, 1113–1119.CrossRefGoogle ScholarPubMed
Turner, SM, Beidel, DC, Dancu, CV, Stanley, MA (1989). An empirically derived inventory to measure social fears and anxiety: The Social Phobia and Anxiety Inventory. Psychological Assessment 1, 35–40.CrossRefGoogle Scholar
Ulrich-Lai, YM, Herman, JP (2009). Neural regulation of endocrine and autonomic stress responses. Nature Reviews Neuroscience 10, 397–409.CrossRefGoogle ScholarPubMed
Urry, HL, van Reekum, CM, Johnstone, T, Kalin, NH, Thurow, ME, Schaefer, HS, Jackson, CA, Frye, CJ, Greischar, LL, Alexander, AL, Davidson, RJ (2006). Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. Journal of Neuroscience 26, 4415–4425.CrossRefGoogle ScholarPubMed
van Marle, HJF, Hermans, EJ, Qin, S, Fernández, G (2010). Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress. NeuroImage 53, 348–354.CrossRefGoogle ScholarPubMed
Veer, IM, Oei, NYL, Spinhoven, P, van Buchem, MA, Elzinga, BM, Rombouts, SARB (2011). Beyond acute social stress: increased functional connectivity between amygdala and cortical midline structures. NeuroImage 57, 1534–1541.CrossRefGoogle ScholarPubMed
Veer, IM, Oei, NYL, Spinhoven, P, van Buchem, MA, Elzinga, BM, Rombouts, SARB (2012). Endogenous cortisol is associated with functional connectivity between the amygdala and medial prefrontal cortex. Psychoneuroendocrinology 37, 1039–1047.CrossRefGoogle ScholarPubMed
Wager, TD, Davidson, ML, Hughes, BL, Lindquist, MA, Ochsner, KN (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 59, 1037–1050.CrossRefGoogle ScholarPubMed
Wager, TD, van Ast, VA, Hughes, BL, Davidson, ML, Lindquist, MA, Ochsner, KN (2009 a). Brain mediators of cardiovascular responses to social threat, part II: prefrontal-subcortical pathways and relationship with anxiety. NeuroImage 47, 836–851.CrossRefGoogle ScholarPubMed
Wager, TD, Waugh, CE, Lindquist, M, Noll, DC, Fredrickson, BL, Taylor, SF (2009 b). Brain mediators of cardiovascular responses to social threat: part I: reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. NeuroImage 47, 821–835.CrossRefGoogle ScholarPubMed
Weeks, JW, Heimberg, RG, Fresco, DM, Hart, TA, Turk, CL, Schneier, FR, Liebowitz, MR (2005). Empirical validation and psychometric evaluation of the brief fear of negative evaluation scale in patients with social anxiety disorder. Psychological Assessment 17, 179–190.CrossRefGoogle ScholarPubMed
Yarkoni, T (2009). Big correlations in little studies: inflated fMRI correlations reflect low statistical power-commentary on Vul et al. (2009). Perspectives on Psychological Science 4, 294–298.CrossRefGoogle ScholarPubMed
Yarkoni, T, Poldrack, RA, Nichols, TE, Van Essen, DC, Wager, TD (2011). Large-scale automated synthesis of human functional neuroimaging data. Nature Methods 8, 665–670.CrossRefGoogle ScholarPubMed
Yarkoni, T, Poldrack, RA, Van Essen, DC, Wager, TD (2010). Cognitive neuroscience 2.0: building a cumulative science of human brain function. Trends in Cognitive Sciences 14, 489–496.CrossRefGoogle ScholarPubMed
Supplementary material: File

Cremers Supplementary Material

Supplementary Analyses & Results

Download Cremers Supplementary Material(File)
File 865.3 KB
Supplementary material: File

Cremers Supplementary Material

Table S1

Download Cremers Supplementary Material(File)
File 65.4 KB