Skip to main content
SpringerLink
Log in

Cerebral resting state markers of biased perception in social anxiety

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Social anxiety (SA) comprises a multitude of persistent fears around the central element of dreaded negative evaluation and exclusion. This very common anxiety is spectrally distributed among the general population and associated with social perception biases deemed causal in its maintenance. Here, we investigated cerebral resting state markers linking SA and biased social perception. To this end, resting state functional connectivity (RSFC) was assessed as the neurobiological marker in a study population with greatly varying SA using fMRI in the first step of the experiment. One month later the impact of unattended laughter—exemplifying social threat—on a face rating task was evaluated as a measure of biased social perception. Applying a dimensional approach, SA-related cognitive biases tied to the valence, dominance and arousal of the threat signal and their underlying RSFC patterns among central nodes of the cerebral emotion, voice and face processing networks were identified. In particular, the connectivity patterns between the amygdalae and the right temporal voice area met all criteria for a cerebral mediation of the association between SA and the laughter valence-related interpretation bias. Thus, beyond this identification of non-state-dependent cerebral markers of biased perception in SA, this study highlights both a starting point and targets for future research on the causal relationships between cerebral connectivity patterns, SA and biased perception, potentially via neurofeedback methods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amir N, Taylor CT (2012) Interpretation training in individuals with generalized social anxiety disorder: a randomized controlled trial. J Consult Clin Psychol 80(3):497–511. https://doi.org/10.1037/a0026928

    Article  PubMed  PubMed Central  Google Scholar 

  • Amir N, Beard C, Taylor CT, Klumpp H, Elias J, Burns M, Chen X (2009) Attention training in individuals with generalized social phobia: a randomized controlled trial. J Consult Clin Psychol 77(5):961–973

    Article  PubMed  PubMed Central  Google Scholar 

  • Banos RM, Quero S, Botella C (2008) Detection and distraction effects for threatening information in social phobia and change after treatment. Depress Anxiety 25(1):55–63. https://doi.org/10.1002/da.20269

    Article  CAS  PubMed  Google Scholar 

  • Beard C, Amir N (2008) A multi-session interpretation modification program: changes in interpretation and social anxiety symptoms. Behav Res Ther 46(10):1135–1141. https://doi.org/10.1016/j.brat.2008.05.012

    Article  PubMed  PubMed Central  Google Scholar 

  • Belin P, Zatorre RJ, Lafaille P, Ahad P, Pike B (2000) Voice-selective areas in human auditory cortex. Nature 403(6767):309–312

    Article  CAS  PubMed  Google Scholar 

  • Boehme S, Ritter V, Tefikow S, Stangier U, Strauss B, Miltner WH, Straube T (2015) Neural correlates of emotional interference in social anxiety disorder. PLoS One 10(6):e0128608. https://doi.org/10.1371/journal.pone.0128608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Browning M, Holmes EA, Murphy SE, Goodwin GM, Harmer CJ (2010) Lateral prefrontal cortex mediates the cognitive modification of attentional bias. Biol Psychiatry 67(10):919–925

    Article  PubMed  PubMed Central  Google Scholar 

  • Brück C, Kreifelts B, Wildgruber D (2011) Emotional voices in context: a neurobiological model of multimodal affective information processing. Phys Life Rev 8(4):383–403

    Article  PubMed  Google Scholar 

  • Brühl AB, Delsignore A, Komossa K, Weidt S (2014) Neuroimaging in social anxiety disorder-a meta-analytic review resulting in a new neurofunctional model. Neurosci Biobehav Rev 47:260–280

    Article  PubMed  Google Scholar 

  • Chiao JY, Adams RB, Tse PU, Lowenthal L, Richeson JA, Ambady N (2008) Knowing who’s boss: fMRI and ERP investigations of social dominance perception. Group Process Intergroup Relat GPIR 11(2):201–214. https://doi.org/10.1177/1368430207088038

    Article  PubMed  Google Scholar 

  • Clark DM, McManus F (2002) Information processing in social phobia. Biol Psychiatry 51(1):92–100

    Article  PubMed  Google Scholar 

  • Clark DM, Wells A (1995) A cognitive model of social phobia. In: Heimberg RG, Liebowitz MR, Hope DA, Schneier FR (eds) Social phobia: diagnosis, assessment, and treatment. Guilford Press, New York, pp 69–93

    Google Scholar 

  • Davila Ross M, Owren MJ, Zimmermann E (2009) Reconstructing the evolution of laughter in great apes and humans. Curr Biol 19(13):1106–1111

    Article  CAS  PubMed  Google Scholar 

  • Eibl-Eibesfeldt I (1970) Ethology: the biology of behavior. Holt, Rinehart and Winston, New York

    Google Scholar 

  • Epstein R, Harris A, Stanley D, Kanwisher N (1999) The parahippocampal place area: recognition, navigation, or encoding? Neuron 23(1):115–125

    Article  CAS  PubMed  Google Scholar 

  • Ethofer T, Bretscher J, Wiethoff S, Bisch J, Schlipf S, Wildgruber D, Kreifelts B (2013) Functional responses and structural connections of cortical areas for processing faces and voices in the superior temporal sulcus. NeuroImage 76C:45–56

    Article  Google Scholar 

  • Gilboa-Schechtman E, Foa EB, Amir N (1999) Attentional biases for facial expressions in social phobia: the effects of target and distractor in “face-in-the-crowd” task. Cogn Emot 13:305–318

    Article  Google Scholar 

  • 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(10):1048–1056. https://doi.org/10.1001/jamapsychiatry.2013.234

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldin PR, Ziv M, Jazaieri H, Weeks J, Heimberg RG, Gross JJ (2014) Impact of cognitive-behavioral therapy for social anxiety disorder on the neural bases of emotional reactivity to and regulation of social evaluation. Behav Res Ther 62:97–106. https://doi.org/10.1016/j.brat.2014.08.005

    Article  PubMed  PubMed Central  Google Scholar 

  • Hautzinger M (1991) The Beck Depression Inventory in clinical practice. Der Nervenarzt 62(11):689–696

    CAS  PubMed  Google Scholar 

  • Havranek MM, Volkart F, Bolliger B, Roos S, Buschner M, Mansour R, Chmielewski T, Gaudlitz K, Hattenschwiler J, Seifritz E, Ruch W (2017) The fear of being laughed at as additional diagnostic criterion in social anxiety disorder and avoidant personality disorder? PLoS One 12(11):e0188024. https://doi.org/10.1371/journal.pone.0188024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobi F, Hofler M, Strehle J, Mack S, Gerschler A, Scholl L, Busch MA, Maske U, Hapke U, Gaebel W, Maier W, Wagner M, Zielasek J, Wittchen HU (2014) Mental disorders in the general population: study on the health of adults in Germany and the additional module mental health (DEGS1-MH). Der Nervenarzt 85(1):77–87. https://doi.org/10.1007/s00115-013-3961-y

    Article  CAS  PubMed  Google Scholar 

  • Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17(11):4302–4311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YK, Yoon HK (2018) Common and distinct brain networks underlying panic and social anxiety disorders. Prog Neuro-psychopharmacol Biol Psychiatry 80(Pt B):115–122. https://doi.org/10.1016/j.pnpbp.2017.06.017

    Article  Google Scholar 

  • Kreifelts B, Ethofer T, Grodd W, Erb M, Wildgruber D (2007) Audiovisual integration of emotional signals in voice and face: an event-related fMRI study. NeuroImage 37(4):1445–1456

    Article  PubMed  Google Scholar 

  • Kreifelts B, Ethofer T, Shiozawa T, Grodd W, Wildgruber D (2009) Cerebral representation of non-verbal emotional perception: fMRI reveals audiovisual integration area between voice- and face-sensitive regions in the superior temporal sulcus. Neuropsychologia 47(14):3059–3066

    Article  PubMed  Google Scholar 

  • Kreifelts B, Ethofer T, Huberle E, Grodd W, Wildgruber D (2010) Association of trait emotional intelligence and individual fMRI-activation patterns during the perception of social signals from voice and face. Humn Brain Mapp 31(7):979–991

    Article  Google Scholar 

  • Kreifelts B, Jacob H, Bruck C, Erb M, Ethofer T, Wildgruber D (2013) Non-verbal emotion communication training induces specific changes in brain function and structure. Front Hum Neurosci 7:648

    Article  PubMed  PubMed Central  Google Scholar 

  • Kreifelts B, Brück C, Ritter J, Ethofer T, Domin M, Lotze M, Jacob H, Schlipf S, Wildgruber D (2014) They are laughing at me: cerebral mediation of cognitive biases in social anxiety. PLoS One 9(6):e99815

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kreifelts B, Brück C, Ethofer T, Ritter J, Weigel L, Erb M, Wildgruber D (2017) Prefrontal mediation of emotion regulation in social anxiety disorder during laughter perception. Neuropsychologia 96:175–183. https://doi.org/10.1016/j.neuropsychologia.2017.01.016

    Article  PubMed  Google Scholar 

  • Laux L, Glanzmann P, Schaffner P, Spielberger CD (1981) Das State-Trait-Angstinventar. Beltz, Weinheim

    Google Scholar 

  • Lehrl S (2005) Mehrfachwahl-Wortschatz-Intelligenztest MWT-B, 5th edn. Spitta, Balingen

    Google Scholar 

  • Lipsitz JD, Schneier FR (2000) Social phobia. Epidemiology and cost of illness. Pharmacoeconomics 18(1):23–32

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Zhu C, Wang Y, Guo W, Li M, Wang W, Long Z, Meng Y, Cui Q, Zeng L, Gong Q, Zhang W, Chen H (2015) Disrupted cortical hubs in functional brain networks in social anxiety disorder. Clin Neurophysiol 126(9):1711–1716. https://doi.org/10.1016/j.clinph.2014.11.014

    Article  PubMed  Google Scholar 

  • Machado-de-Sousa JP, Arrais KC, Alves NT, Chagas MH, de Meneses-Gaya C, Crippa JA, Hallak JE (2010) Facial affect processing in social anxiety: tasks and stimuli. J Neurosci Methods 193(1):1–6

    Article  PubMed  Google Scholar 

  • Mendlowicz MV, Stein MB (2000) Quality of life in individuals with anxiety disorders. Am J Psychiatry 157(5):669–682

    Article  CAS  PubMed  Google Scholar 

  • Minkova L, Sladky R, Kranz GS, Woletz M, Geissberger N, Kraus C, Lanzenberger R, Windischberger C (2017) Task-dependent modulation of amygdala connectivity in social anxiety disorder. Psychiatry Res Neuroimaging 262:39–46. https://doi.org/10.1016/j.pscychresns.2016.12.016

    Article  PubMed  Google Scholar 

  • Miskovic V, Schmidt LA (2012) Social fearfulness in the human brain. Neurosci Biobehav Rev 36(1):459–478

    Article  PubMed  Google Scholar 

  • Mogg K, Bradley BP (2002) Selective orienting of attention to masked threat faces in social anxiety. Behav Res Ther 40(12):1403–1414

    Article  PubMed  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(1):440–457. https://doi.org/10.1016/j.neuroimage.2005.12.002

    Article  PubMed  Google Scholar 

  • Öhman A (1986) Face the beast and fear the face: animal and social fears as prototypes for evolutionary analyses of emotion. Psychophysiology 23(2):123–145

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113

    Article  CAS  PubMed  Google Scholar 

  • Pernet CR, McAleer P, Latinus M, Gorgolewski KJ, Charest I, Bestelmeyer PE, Watson RH, Fleming D, Crabbe F, Valdes-Sosa M, Belin P (2015) The human voice areas: spatial organization and inter-individual variability in temporal and extra-temporal cortices. NeuroImage 119:164–174

    Article  PubMed  PubMed Central  Google Scholar 

  • Pourtois G, de Gelder B, Bol A, Crommelinck M (2005) Perception of facial expressions and voices and of their combination in the human brain. Cortex 41(1):49–59

    Article  PubMed  Google Scholar 

  • Preacher KJ, Hayes AF (2008) Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav Res Methods 40(3):879–891

    Article  Google Scholar 

  • Provine RR (2013) Laughing, grooming, and pub science. Trends Cogn Sci 17(1):9–10

    Article  PubMed  Google Scholar 

  • Quadflieg S, Wendt B, Mohr A, Miltner WH, Straube T (2007) Recognition and evaluation of emotional prosody in individuals with generalized social phobia: a pilot study. Behav Res Ther 45(12):3096–3103

    Article  PubMed  Google Scholar 

  • Rapee RM, Heimberg RG (1997) A cognitive-behavioral model of anxiety in social phobia. Behav Res Ther 35(8):741–756

    Article  CAS  PubMed  Google Scholar 

  • Ritter J, Brück C, Jacob H, Wildgruber D, Kreifelts B (2015) Laughter perception in social anxiety. J Psychiatr Res 60C:178–184

    Article  Google Scholar 

  • Robins DL, Hunyadi E, Schultz RT (2009) Superior temporal activation in response to dynamic audio-visual emotional cues. Brain Cogn 69(2):269–278

    Article  PubMed  Google Scholar 

  • Sladky R, Hoflich A, Kublbock M, Kraus C, Baldinger P, Moser E, Lanzenberger R, Windischberger C (2015) Disrupted effective connectivity between the amygdala and orbitofrontal cortex in social anxiety disorder during emotion discrimination revealed by dynamic causal modeling for FMRI. Cereb Cortex 25(4):895–903. https://doi.org/10.1093/cercor/bht279

    Article  PubMed  Google Scholar 

  • Stangier U, Heidenreich T (2003) Die Liebowitz Soziale Angst-Skala (LSAS). Collegium Internationale Psychiatriae Scalarum - Internationale Skalen für Psychiatrie. Hogrefe, Göttingen

    Google Scholar 

  • Staugaard SR (2010) Threatening faces and social anxiety: a literature review. Clin Psychol Rev 30(6):669–690

    Article  PubMed  Google Scholar 

  • Stein DJ, Ruscio AM, Lee S, Petukhova M, Alonso J, Andrade LH, Benjet C, Bromet E, Demyttenaere K, Florescu S, de Girolamo G, de Graaf R, Gureje O, He Y, Hinkov H, Hu C, Iwata N, Karam EG, Lepine JP, Matschinger H, Oakley Browne M, Posada-Villa J, Sagar R, Williams DR, Kessler RC (2010) Subtyping social anxiety disorder in developed and developing countries. Depress Anxiety 27(4):390–403

    Article  PubMed  PubMed Central  Google Scholar 

  • Szameitat DP, Alter K, Szameitat AJ, Darwin CJ, Wildgruber D, Dietrich S, Sterr A (2009) Differentiation of emotions in laughter at the behavioral level. Emotion 9(3):397–405

    Article  PubMed  Google Scholar 

  • Trower P, Gilbert P (1989) New theoretical conceptions of social anxiety and social phobia. Clin Psychol Rev 9(1):19–35. https://doi.org/10.1016/0272-7358(89)90044-5

    Article  Google Scholar 

  • Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Sasaki Y, Shibata K, Kawato M (2017) Advances in fMRI real-time neurofeedback. Trends Cogn Sci 21(12):997–1010. https://doi.org/10.1016/j.tics.2017.09.010

    Article  PubMed  PubMed Central  Google Scholar 

  • Werner S, Noppeney U (2010) Superadditive responses in superior temporal sulcus predict audiovisual benefits in object categorization. Cereb Cortex 20(8):1829–1842

    Article  PubMed  Google Scholar 

  • Whitfield-Gabrieli S, Nieto-Castanon A (2012) Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect 2(3):125–141. https://doi.org/10.1089/brain.2012.0073

    Article  PubMed  Google Scholar 

  • Wittchen HU, Zaudig M, Fydrich T (1997) Strukturiertes Klinisches Interview für DSM-IV. Hogrefe, Göttingen

    Google Scholar 

  • Worsley K, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans A (1996) A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4(1):74–90

    Article  CAS  PubMed  Google Scholar 

  • Wundt W (1905) Grundzüge der physiologischen Psychologie, 5th edn. Engelmann, Leipzig

    Google Scholar 

  • Yuan M, Zhu H, Qiu C, Meng Y, Zhang Y, Shang J, Nie X, Ren Z, Gong Q, Zhang W, Lui S (2016) Group cognitive behavioral therapy modulates the resting-state functional connectivity of amygdala-related network in patients with generalized social anxiety disorder. BMC Psychiatry 16:198. https://doi.org/10.1186/s12888-016-0904-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan M, Zhu H, Qiu C, Meng Y, Zhang Y, Ren Z, Li Y, Yuan C, Gao M, Lui S, Gong Q, Zhang W (2018) Altered regional and integrated resting-state brain activity in general social anxiety disorder patients before and after group cognitive behavior therapy. Psychiatry Res 272:30–37. https://doi.org/10.1016/j.pscychresns.2017.12.004

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by grants of the Fortüne-Program of the University of Tübingen (fortüne 1997-0-0, and fortüne 2140-0-0).

Author information

Authors and Affiliations

  1. Department of Psychiatry and Psychotherapy, Eberhard Karls University of Tübingen, Calwerstr. 14, 72076, Tübingen, Germany

    Benjamin Kreifelts, Lena Weigel, Thomas Ethofer, Carolin Brück & Dirk Wildgruber

  2. Department of Biomedical Magnetic Resonance, Eberhard Karls University of Tübingen, Tübingen, Germany

    Thomas Ethofer & Michael Erb

Authors
  1. Benjamin Kreifelts
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lena Weigel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas Ethofer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carolin Brück
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael Erb
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dirk Wildgruber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benjamin Kreifelts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 33 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kreifelts, B., Weigel, L., Ethofer, T. et al. Cerebral resting state markers of biased perception in social anxiety. Brain Struct Funct 224, 759–777 (2019). https://doi.org/10.1007/s00429-018-1803-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-018-1803-1

Keywords

Search

Navigation