Pattern of cortical activation during processing of aversive stimuli in traumatized survivors of war and torture

  • Claudia CataniEmail author
  • Hannah Adenauer
  • Julian Keil
  • Hannah Aichinger
  • Frank Neuner
Original Paper


Posttraumatic stress disorder (PTSD) has been associated with an altered processing of threat-related stimuli. In particular, an attentional bias towards threat cues has been consistently found in behavioral studies. However, it is unclear whether increased attention towards threat cues translates into preferential processing as neurophysiological studies have yielded inconsistent findings. The aim of the present study was to investigate the neocortical activity related to the processing of aversive stimuli in patients with PTSD. 36 survivors of war and torture with PTSD, 21 Trauma Controls and 20 Unexposed Subjects participated in a visual evoked magnetic field study using flickering pictures of varying affective valence as stimulus material. Minimum norm source localization was carried out to estimate the distribution of sources of the evoked neuromagnetic activity in the brain. Statistical permutation analyses revealed reduced steady-state visual evoked field amplitudes over occipital areas in response to aversive pictures for PTSD patients and for Trauma Controls in comparison to unexposed subjects. Furthermore, PTSD patients showed a hyperactivation of the superior parietal cortex selectively in response to aversive stimuli, which was related to dissociative symptoms as well as to torture severity. The results indicate a different pattern of cortical activation driven by aversive stimuli depending on the experience of multiple traumatic events and PTSD. Whereas, a decreased visual processing of aversive stimuli seems to be associated with trauma exposure in general, the superior parietal activity might represent a specific process linked to the diagnosis of PTSD.


Posttraumatic stress disorder (PTSD) Emotional processing Steady-state visual evoked fields (SSVEF) Magnetoencephalography (MEG) 



We are grateful to all subjects who took part in the study. Research was supported by the Deutsche Forschungsgemeinschaft (DFG) and the European Refugee Fund (EFF). The authors would like to thank Heike Riedke for logistical support, the outpatient clinic staff for clinical support, Ursula Lommen for helping with MEG data acquisition, Stephan Moratti and Christian Wienbruch for technical advice, Sonja Haas and Steivan Pinösch for helping with entry and administration of data, and Katy Robjant for editing.

Conflict of interest statement

Authors declare they have no conflict of interest. The corresponding author had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.


  1. 1.
    Attias J, Bleich A, Furman V, Zinger Y (1996) Event-related potentials in post-traumatic stress disorder of combat origin. Biol Psychiatry 40:373–381PubMedCrossRefGoogle Scholar
  2. 2.
    Basoglu M, Jaranson J, Mollica R, Kastrup M (2001) Torture and mental health: a research overview. In: Garrity T, Keane T, Tuma F (eds) The mental health consequences of torture. Plenum, New York, pp 35–62Google Scholar
  3. 3.
    Berg P, Scherg M (1994) A multiple source approach to the correction of eye artifacts. Electroencephalogr Clin Neurophysiol 90:229–241PubMedCrossRefGoogle Scholar
  4. 4.
    Bickford RG, Fleming N, Billinger T (1971) Compression of EEG data. Trans Am Neurol Assoc 96:118–122PubMedGoogle Scholar
  5. 5.
    Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Gusman FD, Charney DS, Keane TM (1995) The development of a Clinician-Administered PTSD Scale. J Trauma Stress 8:75–90PubMedCrossRefGoogle Scholar
  6. 6.
    Bleich AV, Attias J, Furman V (1996) Effect of repeated visual traumatic stimuli on the event related P3 brain potential in post-traumatic stress disorder. Int J Neurosci 85:45–55PubMedCrossRefGoogle Scholar
  7. 7.
    Bradley MM, Lang PJ (1994) Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. J Behav Ther Exp Psychiatry 25:49–59PubMedCrossRefGoogle Scholar
  8. 8.
    Buckley TC, Blanchard EB, Neill WT (2000) Information processing and PTSD: a review of the empirical literature. Clin Psychol Rev 20:1041–1065PubMedCrossRefGoogle Scholar
  9. 9.
    Cabeza R (2008) Role of parietal regions in episodic memory retrieval: the dual attentional processes hypothesis. Neuropsychologia 46:1813–1827PubMedCrossRefGoogle Scholar
  10. 10.
    Campbell TA (2007) Psychological assessment, diagnosis, and treatment of torture survivors: a review. Clin Psychol Rev 27:628–641PubMedCrossRefGoogle Scholar
  11. 11.
    Carlson EB, Rosser-Hogan R (1994) Cross-cultural response to trauma: a study of traumatic experiences and posttraumatic symptoms in Cambodian refugees. J Trauma Stress 7:43–58PubMedCrossRefGoogle Scholar
  12. 12.
    Clark CR, McFarlane AC, Morris P, Weber DL, Sonkkilla C, Shaw M, Marcina J, Tochon-Danguy HJ, Egan GF (2003) Cerebral function in posttraumatic stress disorder during verbal working memory updating: a positron emission tomography study. Biol Psychiatry 53:474–481PubMedCrossRefGoogle Scholar
  13. 13.
    Corbetta M, Shulman GL, Miezin FM, Petersen SE (1995) Superior parietal cortex activation during spatial attention shifts and visual feature conjunction. Science 270:802–805PubMedCrossRefGoogle Scholar
  14. 14.
    Ehlers A, Clark DM (2000) A cognitive model of posttraumatic stress disorder. Behav Res Ther 38:319–345PubMedCrossRefGoogle Scholar
  15. 15.
    Ehlers CL, Hurst S, Phillips E, Gilder DA, Dixon M, Gross A, Lau P, Yehuda R (2006) Electrophysiological responses to affective stimuli in American Indians experiencing trauma with and without PTSD. Ann NY Acad Sci 1071:125–136PubMedCrossRefGoogle Scholar
  16. 16.
    Felmingham KL, Bryant RA, Gordon E (2003) Processing angry and neutral faces in post-traumatic stress disorder: an event-related potentials study. NeuroReport 14:777–780PubMedCrossRefGoogle Scholar
  17. 17.
    Gehricke J, Shapiro D (2000) Reduced facial expression and social context in major depression: discrepancies between facial muscle activity and self-reported emotion. Psychiatry Res 95:157–167PubMedCrossRefGoogle Scholar
  18. 18.
    Hamalainen MS, Ilmoniemi RJ (1994) Interpreting magnetic fields of the brain: minimum norm estimates. Med Biol Eng Comput 32:35–42PubMedCrossRefGoogle Scholar
  19. 19.
    Han S, Jiang Y (2004) The parietal cortex and attentional modulations of activities of the visual cortex. Neuroreport 15:2275–2280PubMedCrossRefGoogle Scholar
  20. 20.
    Hauk O (2004) Keep it simple: a case for using classical minimum norm estimation in the analysis of EEG and MEG data. Neuroimage 21:1612–1621PubMedCrossRefGoogle Scholar
  21. 21.
    Hillyard SA, Anllo-Vento L (1998) Event-related brain potentials in the study of visual selective attention. Proc Natl Acad Sci USA 95:781–787PubMedCrossRefGoogle Scholar
  22. 22.
    Holmes A, Nielsen MK, Green S (2008) Effects of anxiety on the processing of fearful and happy faces: an event-related potential study. Biol Psychol 77:159–173PubMedCrossRefGoogle Scholar
  23. 23.
    Irle E, Lange C, Weniger G, Sachsse U (2007) Size abnormalities of the superior parietal cortices are related to dissociation in borderline personality disorder. Psychiatry Res 156:139–149PubMedCrossRefGoogle Scholar
  24. 24.
    Jensen O, Vanni S (2002) A new method to identify multiple sources of oscillatory activity from magnetoencephalographic data. Neuroimage 15:568–574PubMedCrossRefGoogle Scholar
  25. 25.
    Junghöfer M, Bradley MM, Elbert TR, Lang PJ (2001) Fleeting images: a new look at early emotion discrimination. Psychophysiology 38:175–178PubMedCrossRefGoogle Scholar
  26. 26.
    Junghöfer M, Peyk P (2004) Analyse und Visualisierung von Hirnstrom- und Hirnmagnetfeld-Messungen [analysis of electrical potentials and magnetic fields of the brain]. Matlab Select 2:24–28. EMEGS software is freely available at
  27. 27.
    Junghofer M, Sabatinelli D, Bradley MM, Schupp HT, Elbert TR, Lang PJ (2006) Fleeting images: rapid affect discrimination in the visual cortex. NeuroReport 17:225–229PubMedCrossRefGoogle Scholar
  28. 28.
    Karl A, Malta LS, Maercker A (2006) Meta-analytic review of event-related potential studies in post-traumatic stress disorder. Biol Psychol 71:123–147PubMedCrossRefGoogle Scholar
  29. 29.
    Karniski W, Blair RC, Snider AD (1994) An exact statistical method for comparing topographic maps, with any number of subjects and electrodes. Brain Topogr 6:203–210PubMedCrossRefGoogle Scholar
  30. 30.
    Keil A, Gruber T, Muller MM, Moratti S, Stolarova M, Bradley MM, Lang PJ (2003) Early modulation of visual perception by emotional arousal: evidence from steady-state visual evoked brain potentials. Cogn Affect Behav Neurosci 3:195–206PubMedCrossRefGoogle Scholar
  31. 31.
    Keil A, Stolarova M, Heim S, Gruber T, Müller MM (2003) Temporal stability of high-frequency brain oscillations in the human EEG. Brain Topogr 16:101–110PubMedCrossRefGoogle Scholar
  32. 32.
    Kemp AH, Gray MA, Eide P, Silberstein RB, Nathan PJ (2002) Steady-state visually evoked potential topography during processing of emotional valence in healthy subjects. NeuroImage 17:1684–1692PubMedCrossRefGoogle Scholar
  33. 33.
    Kounios J, Litz B, Kaloupek D, Riggs D, Knight J, Weathers F, Anderson JE, Keane T (1997) Electrophysiology of combat-related PTSD. Ann NY Acad Sci 821:504–507PubMedCrossRefGoogle Scholar
  34. 34.
    Lang PJ, Bradley MM, Cuthbert BN (1998) Emotion, motivation, and anxiety: brain mechanisms and psychophysiology. Biol Psychiatry 44:1248–1263PubMedCrossRefGoogle Scholar
  35. 35.
    Lang PJ, Bradley MM, Cuthbert BN (2005) International Affective Picture System (IAPS): affective ratings of pictures and instruction manual. University of Florida, GainesvilleGoogle Scholar
  36. 36.
    Lang PJ, Bradley MM, Cuthbert BN (1997) Motivated attention: affect, activation and action. In: Lang PJ, Simons RF, Balaban MT (eds) Attention and orienting: sensory and motivational processes. Erlbaum, MahwahGoogle Scholar
  37. 37.
    Lanius RA, Williamson PC, Bluhm RL, Densmore M, Boksman K, Neufeld RW, Gati JS, Menon RS (2005) Functional connectivity of dissociative responses in posttraumatic stress disorder: a functional magnetic resonance imaging investigation. Biol Psychiatry 57:873–884PubMedCrossRefGoogle Scholar
  38. 38.
    Lanius RA, Williamson PC, Boksman K, Densmore M, Gupta M, Neufeld RW, Gati JS, Menon RS (2002) Brain activation during script-driven imagery induced dissociative responses in PTSD: a functional magnetic resonance imaging investigation. Biol Psychiatry 52:305–311PubMedCrossRefGoogle Scholar
  39. 39.
    Ludbrook J, Dudley H (1998) Why permutation tests are superior to t and F tests in biomedical research. The American Statistician 52:127–132CrossRefGoogle Scholar
  40. 40.
    McNally RJ, Clancy SA, Schacter DL, Pitman RK (2000) Cognitive processing of trauma cues in adults reporting repressed, recovered, or continuous memories of childhood sexual abuse. J Abnorm Psychol 109:355–359PubMedCrossRefGoogle Scholar
  41. 41.
    McNally RJ, Kaspi SP, Riemann BC, Zeitlin SB (1990) Selective processing of threat cues in posttraumatic stress disorder. J Abnorm Psychol 99:398–402PubMedCrossRefGoogle Scholar
  42. 42.
    Metzger LJ, Orr SP, Lasko NB, Pitman RK (1997) Auditory event-related potentials to tone stimuli in combat-related posttraumatic stress disorder. Biol Psychiatry 42:1006–1015PubMedCrossRefGoogle Scholar
  43. 43.
    Moratti S, Keil A, Stolarova M (2004) Motivated attention in emotional picture processing is reflected by activity modulation in cortical attention networks. Neuroimage 21:954–964PubMedCrossRefGoogle Scholar
  44. 44.
    Moratti S, Rubio G, Campo P, Keil A, Ortiz T (2008) Hypofunction of right temporoparietal cortex during emotional arousal in depression. Arch Gen Psychiatry 65:532–541PubMedCrossRefGoogle Scholar
  45. 45.
    Ray WJ, Odenwald M, Neuner F, Schauer M, Ruf M, Wienbruch C, Rockstroh B, Elbert T (2006) Decoupling neural networks from reality: dissociative experiences in torture victims are reflected in abnormal brain waves in left frontal cortex. Psychol Sci 17:825–829PubMedCrossRefGoogle Scholar
  46. 46.
    Regan D (1989) Human Brain Electrophysiology: Evoked Potentials and Evoked Magnetic Fields in Science and Medicine. Elsevier, New YorkGoogle Scholar
  47. 47.
    Rief W, Hiller W (2003) A new approach to the assessment of the treatment effects of somatoform disorders. Psychosomatics 44:492–498PubMedCrossRefGoogle Scholar
  48. 48.
    Rossignol M, Philippot P, Douilliez C, Crommelinck M, Campanella S (2005) The perception of fearful and happy facial expression is modulated by anxiety: an event-related potential study. Neurosci Lett 377:115–120PubMedCrossRefGoogle Scholar
  49. 49.
    Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59(Suppl 20):22–33 quiz 34–57PubMedGoogle Scholar
  50. 50.
    Sloan DM, Strauss ME, Quirk SW, Sajatovic M (1997) Subjective and expressive emotional responses in depression. J Affect Disord 46:135–141PubMedCrossRefGoogle Scholar
  51. 51.
    Sloan DM, Strauss ME, Wisner KL (2001) Diminished response to pleasant stimuli by depressed women. J Abnorm Psychol 110:488–493PubMedCrossRefGoogle Scholar
  52. 52.
    vivo (2008)
  53. 53.
    Williams JB (1988) A structured interview guide for the Hamilton Depression Rating Scale. Arch Gen Psychiatry 45:742–747PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Claudia Catani
    • 1
    Email author
  • Hannah Adenauer
    • 2
  • Julian Keil
    • 2
  • Hannah Aichinger
    • 2
  • Frank Neuner
    • 1
  1. 1.Clinical Psychology and Psychotherapy Unit, Department of PsychologyUniversity of BielefeldBielefeldGermany
  2. 2.Department of Psychology, Center for Psychiatry ReichenauUniversity of KonstanzKonstanzGermany

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