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Brain Imaging and Behavior

, Volume 7, Issue 1, pp 35–48 | Cite as

Self-referential and anxiety-relevant information processing in subclinical social anxiety: an fMRI study

  • Anna Abraham
  • Carolin Kaufmann
  • Ronny Redlich
  • Andrea Hermann
  • Rudolf Stark
  • Stephan Stevens
  • Christiane Hermann
Original Research

Abstract

The fear of negative evaluation is one of the hallmark features of social anxiety. Behavioral evidence thus far largely supports cognitive models which postulate that information processing biases in the face of socially relevant information are a key factor underlying this widespread phobia. So far only one neuroimaging study has explicitly focused on the fear of negative evaluation in social anxiety where the brain responses of social phobics were compared to healthy participants during the processing of self-referential relative to other-referential criticism, praise or neutral information. Only self-referential criticism led to stronger activations in emotion-relevant regions of the brain, such as the amygdala and medial prefrontal cortices (mPFC), in the social phobics. The objective of the current study was to determine whether these findings could be extended to subclinical social anxiety. In doing so, the specificity of this self-referential bias was also examined by including both social and non-social (physical illness-related) threat information as well as a highly health anxious control group in the experimental paradigm. The fMRI findings indicated that the processing of emotional stimuli was accompanied by activations in the amygdala and the ventral mPFC, while self-referential processing was associated with activity in regions such as the mPFC, posterior cingulate and temporal poles. Despite the validation of the paradigm, the results revealed that the previously reported behavioral and brain biases associated with social phobia could not be unequivocally extended to subclinical social anxiety. The divergence between the findings is explored in detail with reference to paradigm differences and conceptual issues.

Keywords

Social anxiety Social cognition Neuroimaging Self-referential processing Emotion processing Fear of negative evaluation 

Notes

Acknowledgements

We thank scientists at the BION, particularly Dr. Bertram Walter, Dr. Ulrich Ott, Dr. Carlo Blecker, and Professor Dieter Vaitl for their support.

Supplementary material

11682_2012_9188_MOESM1_ESM.doc (102 kb)
ESM 1 Supplementary material (DOC 102 kb)

References

  1. Amaro, E., Jr., & Barker, G. J. (2006). Study design in fMRI: basic principles. Brain and Cognition, 60(3), 220–232. doi: 10.1016/j.bandc.2005.11.009.PubMedCrossRefGoogle Scholar
  2. American Psychiatric Association (2000). Diagnostic and statistical manual of mental disorders DSM-IV-TR fourth edition (4th ed.). Arlington, VA: Amer Psychiatric Pub.Google Scholar
  3. Amir, N., Beard, C., & Bower, E. (2005). Interpretation bias and social anxiety. Cognitive Therapy and Research, 29(4), 433–443. doi: 10.1007/s10608-005-2834-5.CrossRefGoogle Scholar
  4. Amir, N., Foa, E. B., & Coles, M. E. (1998). Negative interpretation bias in social phobia. Behaviour Research and Therapy, 36(10), 945–957.CrossRefGoogle Scholar
  5. Amir, N., Weber, G., Beard, C., Bomyea, J., & Taylor, C. T. (2008). The effect of a single-session attention modification program on response to a public-speaking challenge in socially anxious individuals. Journal of Abnormal Psychology, 117(4), 860–868. doi: 10.1037/a0013445.PubMedCrossRefGoogle Scholar
  6. Arja, S. K., Feng, Z., Chen, Z., Caprihan, A., Kiehl, K. A., Adali, T., et al. (2010). Changes in fMRI magnitude data and phase data observed in block-design and event-related tasks. NeuroImage, 49(4), 3149–3160. doi: 10.1016/j.neuroimage.2009.10.087.PubMedCrossRefGoogle Scholar
  7. Bailer, J., & Witthöft, M. (2006). Modifizierte Kurzform des Health Anxiety Inventory (MK-HAI) von Salkovskis, Rimes, Warwick und Clark [Modified Short Version of the Health Anxiety Inventory by Salkovskis, Rimes, Warwick, and Clark]. In A. Glöckner-Rist (Ed.), ZUMA-Informationssystem. Elektronisches Handbuch sozialwissenschaftlicher Erhebungsinstrumente. Version 10.00. Mannheim: Zentrum für Umfragen, Methoden und Analysen.Google Scholar
  8. Bishop, S. J. (2007). Neurocognitive mechanisms of anxiety: an integrative account. Trends in Cognitive Sciences, 11(7), 307–316. doi: 10.1016/j.tics.2007.05.008.PubMedCrossRefGoogle Scholar
  9. Blair, K., Geraci, M., Devido, J., McCaffrey, D., Chen, G., Vythilingam, M., et al. (2008). Neural response to self- and other referential praise and criticism in generalized social phobia. Archives of General Psychiatry, 65(10), 1176–1184. doi: 10.1001/archpsyc.65.10.1176.PubMedCrossRefGoogle Scholar
  10. Bögels, S. M., & Lamers, C. T. J. (2002). The causal role of self-awareness in blushing-anxious, socially-anxious and social phobics individuals. Behaviour Research and Therapy, 40(12), 1367–1384.PubMedCrossRefGoogle Scholar
  11. Bradley, M. M., & Lang, P. J. (1994). Measuring emotion: the self-assessment Manikin and the semantic differential. Journal of Behavior Therapy and Experimental Psychiatry, 25(1), 49–59.PubMedCrossRefGoogle Scholar
  12. Brühl, A. B., Rufer, M., Delsignore, A., Kaffenberger, T., Jäncke, L., & Herwig, U. (2011). Neural correlates of altered general emotion processing in social anxiety disorder. Brain Research, 1378, 72–83. doi: 10.1016/j.brainres.2010.12.084.PubMedCrossRefGoogle Scholar
  13. Canteras, N. S., Resstel, L. B., Bertoglio, L. J., Carobrez, A. P., & Guimarães, F. S. (2010). Neuroanatomy of anxiety. Current Topics in Behavioral Neurosciences, 2, 77–96.PubMedCrossRefGoogle Scholar
  14. Clark, D. M., & Wells, A. (1995). A cognitive model of social phobia. Social phobia: diagnosis, assessment, and treatment (pp. 69–93). New York: The Guilford Press.Google Scholar
  15. Cooney, R. E., Atlas, L. Y., Joormann, J., Eugène, F., & Gotlib, I. H. (2006). Amygdala activation in the processing of neutral faces in social anxiety disorder: is neutral really neutral? Psychiatry Research, 148(1), 55–59. doi: 10.1016/j.pscychresns.2006.05.003.PubMedCrossRefGoogle Scholar
  16. Etkin, A. (2010). Functional neuroanatomy of anxiety: a neural circuit perspective. Current Topics in Behavioral Neurosciences, 2, 251–277.PubMedCrossRefGoogle Scholar
  17. Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. The American Journal of Psychiatry, 164(10), 1476–1488. doi: 10.1176/appi.ajp. 2007.07030504.PubMedCrossRefGoogle Scholar
  18. Evans, K. C., Wright, C. I., Wedig, M. M., Gold, A. L., Pollack, M. H., & Rauch, S. L. (2008). A functional MRI study of amygdala responses to angry schematic faces in social anxiety disorder. Depression and Anxiety, 25(6), 496–505. doi: 10.1002/da.20347.PubMedCrossRefGoogle Scholar
  19. Freitas-Ferrari, M. C., Hallak, J. E. C., Trzesniak, C., Filho, A. S., Machado-de-Sousa, J. P., Chagas, M. H. N., et al. (2010). Neuroimaging in social anxiety disorder: a systematic review of the literature. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 34(4), 565–580. doi: 10.1016/j.pnpbp. 2010.02.028.CrossRefGoogle Scholar
  20. Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J.-P., Frith, C. D., & Frackowiak, R. S. J. (1994). Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping, 2(4), 189–210. doi: 10.1002/hbm.460020402.CrossRefGoogle Scholar
  21. Goldin, P. R., Manber, T., Hakimi, S., Canli, T., & Gross, J. J. (2009). Neural bases of social anxiety disorder: emotional reactivity and cognitive regulation during social and physical threat. Archives of General Psychiatry, 66(2), 170–180. doi: 10.1001/archgenpsychiatry.2008.525.PubMedCrossRefGoogle Scholar
  22. Heimberg, R. G., Horner, K. J., Juster, H. R., Safren, S. A., Brown, E. J., Schneier, F. R., et al. (1999). Psychometric properties of the Liebowitz Social Anxiety Scale. Psychological Medicine, 29(1), 199–212.PubMedCrossRefGoogle Scholar
  23. Heinrichs, N., & Hofmann, S. G. (2001). Information processing in social phobia: a critical review. Clinical Psychology Review, 21(5), 751–770.PubMedCrossRefGoogle Scholar
  24. Hermann, C., Ofer, J., & Flor, H. (2004). Covariation bias for ambiguous social stimuli in generalized social phobia. Journal of Abnormal Psychology, 113(4), 646–653. doi: 10.1037/0021-843X.113.4.646.PubMedCrossRefGoogle Scholar
  25. Lamm, C., & Singer, T. (2010). The role of anterior insular cortex in social emotions. Brain Structure & Function, 214(5–6), 579–591. doi: 10.1007/s00429-010-0251-3.CrossRefGoogle Scholar
  26. Legrand, D., & Ruby, P. (2009). What is self-specific? Theoretical investigation and critical review of neuroimaging results. Psychological Review, 116(1), 252–282. doi: 10.1037/a0014172.PubMedCrossRefGoogle Scholar
  27. Lohmann, G., Müller, K., Bosch, V., Mentzel, H., Hessler, S., Chen, L., et al. (2001). LIPSIA–a new software system for the evaluation of functional magnetic resonance images of the human brain. Computerized Medical Imaging and Graphics: The Official Journal of the Computerized Medical Imaging Society, 25(6), 449–457.CrossRefGoogle Scholar
  28. Lou, H. C., Luber, B., Crupain, M., Keenan, J. P., Nowak, M., Kjaer, T. W., et al. (2004). Parietal cortex and representation of the mental Self. Proceedings of the National Academy of Sciences of the United States of America, 101(17), 6827–6832. doi: 10.1073/pnas.0400049101.PubMedCrossRefGoogle Scholar
  29. Machado-de-Sousa, J. P., Arrais, K. C., Alves, N. T., Chagas, M. H. N., de Meneses-Gaya, C., Crippa, J. A., et al. (2010). Facial affect processing in social anxiety: tasks and stimuli. Journal of Neuroscience Methods, 193(1), 1–6. doi: 10.1016/j.jneumeth.2010.08.013.PubMedCrossRefGoogle Scholar
  30. Marcus, D. K., Gurley, J. R., Marchi, M. M., & Bauer, C. (2007). Cognitive and perceptual variables in hypochondriasis and health anxiety: a systematic review. Clinical Psychology Review, 27(2), 127–139. doi: 10.1016/j.cpr.2006.09.003.PubMedCrossRefGoogle Scholar
  31. Mattick, R. P., & Clarke, J. C. (1998). Development and validation of measures of social phobia scrutiny fear and social interaction anxiety. Behaviour Research and Therapy, 36(4), 455–470.PubMedCrossRefGoogle Scholar
  32. Morrison, S. E., & Salzman, C. D. (2010). Re-valuing the amygdala. Current Opinion in Neurobiology, 20(2), 221–230. doi: 10.1016/j.conb.2010.02.007.PubMedCrossRefGoogle Scholar
  33. Neumann, J., & Lohmann, G. (2003). Bayesian second-level analysis of functional magnetic resonance images. NeuroImage, 20(2), 1346–1355. doi: 10.1016/S1053-8119(03)00443-9.PubMedCrossRefGoogle Scholar
  34. 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. doi: 10.1016/j.neuroimage.2005.12.002.PubMedCrossRefGoogle Scholar
  35. Ochsner, K. N. (2008). The social-emotional processing stream: five core constructs and their translational potential for schizophrenia and beyond. Biological Psychiatry, 64(1), 48–61. doi: 10.1016/j.biopsych.2008.04.024.PubMedCrossRefGoogle Scholar
  36. Pilowsky, I. (1967). Dimensions of hypochondriasis. The British Journal of Psychiatry: The Journal of Mental Science, 113(494), 89–93.CrossRefGoogle Scholar
  37. Rief, W., Hiller, W., Geissner, E., & Fichter, M. M. (1994). Hypochondrie: Erfassung und erste klinische Ergebnisse. [Hypochondriasis: Assessment and initial clinical results.]. Zeitschrift für Klinische Psychologie, 23(1), 34–42.Google Scholar
  38. Salkovskis, P. M., Rimes, K. A., Warwick, H. M. C., & Clark, D. M. (2002). The health anxiety inventory: development and validation of scales for the measurement of health anxiety and hypochondriasis. Psychological Medicine, 32(5), 843–853.PubMedCrossRefGoogle Scholar
  39. Salzman, C. D., & Fusi, S. (2010). Emotion, cognition, and mental state representation in amygdala and prefrontal cortex. Annual Review of Neuroscience, 33, 173–202. doi: 10.1146/annurev.neuro.051508.135256.PubMedCrossRefGoogle Scholar
  40. Schmidt, S., Mohr, A., Miltner, W. H. R., & Straube, T. (2010). Task-dependent neural correlates of the processing of verbal threat-related stimuli in social phobia. Biological Psychology, 84(2), 304–312. doi: 10.1016/j.biopsycho.2010.03.005.PubMedCrossRefGoogle Scholar
  41. Schmitz, T. W., & Johnson, S. C. (2007). Relevance to self: a brief review and framework of neural systems underlying appraisal. Neuroscience and Biobehavioral Reviews, 31(4), 585–596. doi: 10.1016/j.neubiorev.2006.12.003.PubMedCrossRefGoogle Scholar
  42. Shin, L. M., & Liberzon, I. (2010). The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 35(1), 169–191. doi: 10.1038/npp. 2009.83.CrossRefGoogle Scholar
  43. Singer, T., Critchley, H. D., & Preuschoff, K. (2009). A common role of insula in feelings, empathy and uncertainty. Trends in Cognitive Sciences, 13(8), 334–340. doi: 10.1016/j.tics.2009.05.001.PubMedCrossRefGoogle Scholar
  44. Stangier, U., Heidenreich, T., Berardi, A., Golbs, U., & Hoyer, J. (1999). Die Erfassung sozialer Phobie durch die Social Interaction Anxiety Scale (SIAS) und die Social Phobia Scale (SPS). Zeitschrift für Klinische Psychologie und Psychotherapie, 28(1), 28–36. doi: 10.1026//0084-5345.28.1.28.CrossRefGoogle Scholar
  45. Staugaard, S. R. (2010). Threatening faces and social anxiety: a literature review. Clinical Psychology Review, 30(6), 669–690. doi: 10.1016/j.cpr.2010.05.001.PubMedCrossRefGoogle Scholar
  46. Stein, M. B., Simmons, A. N., Feinstein, J. S., & Paulus, M. P. (2007). Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. The American Journal of Psychiatry, 164(2), 318–327.PubMedCrossRefGoogle Scholar
  47. Stevens, S., Gerlach, A. L., Cludius, B., Silkens, A., Craske, M. G., & Hermann, C. (2011). Heartbeat perception in social anxiety before and during speech anticipation. Behaviour Research and Therapy, 49(2), 138–143. doi: 10.1016/j.brat.2010.11.009.PubMedCrossRefGoogle Scholar
  48. Stevens, S., Hofmann, M., Kiko, S., Mall, A. K., Steil, R., Bohus, M., et al. (2010). What determines observer-rated social performance in individuals with social anxiety disorder? Journal of Anxiety Disorders, 24(8), 830–836. doi: 10.1016/j.janxdis.2010.06.005.PubMedCrossRefGoogle Scholar
  49. Stevens, S., Rist, F., & Gerlach, A. L. (2009). Influence of alcohol on the processing of emotional facial expressions in individuals with social phobia. The British Journal of Clinical Psychology/The British Psychological Society, 48(Pt 2), 125–140. doi: 10.1348/014466508X368856.PubMedCrossRefGoogle Scholar
  50. Straube, T., Mentzel, H.-J., & Miltner, W. H. R. (2005). Common and distinct brain activation to threat and safety signals in social phobia. Neuropsychobiology, 52(3), 163–168. doi: 10.1159/000087987.PubMedCrossRefGoogle Scholar
  51. Symons, C. S., & Johnson, B. T. (1997). The self-reference effect in memory: a meta-analysis. Psychological Bulletin, 121(3), 371–394.PubMedCrossRefGoogle Scholar
  52. van den Heuvel, O. A., Veltman, D. J., Groenewegen, H. J., Witter, M. P., Merkelbach, J., Cath, D. C., et al. (2005). Disorder-specific neuroanatomical correlates of attentional bias in obsessive-compulsive disorder, panic disorder, and hypochondriasis. Archives of General Psychiatry, 62(8), 922–933.PubMedCrossRefGoogle Scholar
  53. Vormbrock, F., & Neuser, J. (1983). Konstruktion zweier spezifischer Trait-Fragebogen zur Erfassung von Angst in sozialen Situationen. Diagnostica, 19, 165–182.Google Scholar
  54. Warwick, H. M., & Salkovskis, P. M. (1990). Hypochondriasis. Behaviour Research and Therapy, 28(2), 105–117.PubMedCrossRefGoogle Scholar
  55. Watson, D., & Friend, R. (1969). Measurement of social-evaluative anxiety. Journal of Consulting and Clinical Psychology, 33(4), 448–457. doi: 10.1037/h0027806.PubMedCrossRefGoogle Scholar
  56. Williams, P. G. (2004). The psychopathology of self-assessed health:a cognitive approach to health anxiety and hypochondriasis. Cognitive Therapy and Research, 28(5), 629–644. doi: 10.1023/B:COTR.0000045569.25096.44.CrossRefGoogle Scholar
  57. Worsley, K. J., & Friston, K. J. (1995). Analysis of fMRI time-series revisited–again. NeuroImage, 2(3), 173–181. doi: 10.1006/nimg.1995.1023.PubMedCrossRefGoogle Scholar
  58. Zysset, S., Huber, O., Ferstl, E., & von Cramon, D. Y. (2002). The anterior frontomedian cortex and evaluative judgment: an fMRI study. NeuroImage, 15(4), 983–991. doi: 10.1006/nimg.2001.1008.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Anna Abraham
    • 1
  • Carolin Kaufmann
    • 1
    • 2
  • Ronny Redlich
    • 1
    • 2
  • Andrea Hermann
    • 3
  • Rudolf Stark
    • 3
  • Stephan Stevens
    • 1
  • Christiane Hermann
    • 1
  1. 1.Department of Clinical PsychologyJustus Liebig University of GiessenGiessenGermany
  2. 2.University of MuensterMuensterGermany
  3. 3.Bender Institute of NeuroimagingJustus-Liebig-University of GiessenGiessenGermany

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