Hostname: page-component-745bb68f8f-g4j75 Total loading time: 0 Render date: 2025-01-22T01:05:30.009Z Has data issue: false hasContentIssue false
  • English
  • Français

Dissociative responses to conscious and non-conscious fear impact underlying brain function in post-traumatic stress disorder

Published online by Cambridge University Press:  25 February 2008

K. Felmingham ,
A. H. Kemp ,
L. Williams ,
E. Falconer ,
G. Olivieri ,
A. Peduto  and
R. Bryant
K. Felmingham*
Affiliation:
Brain Dynamics Centre, Westmead Millennium Institute, Westmead Hospital, Australia Division of Psychological Medicine, Western Clinical School, University of Sydney, Australia
A. H. Kemp
Affiliation:
Brain Dynamics Centre, Westmead Millennium Institute, Westmead Hospital, Australia Division of Psychological Medicine, Western Clinical School, University of Sydney, Australia
L. Williams
Affiliation:
Brain Dynamics Centre, Westmead Millennium Institute, Westmead Hospital, Australia Division of Psychological Medicine, Western Clinical School, University of Sydney, Australia
E. Falconer
Affiliation:
Brain Dynamics Centre, Westmead Millennium Institute, Westmead Hospital, Australia School of Psychology, University of New South Wales, Australia
G. Olivieri
Affiliation:
MRI Unit, Department of Radiology, Westmead Hospital, Australia
A. Peduto
Affiliation:
MRI Unit, Department of Radiology, Westmead Hospital, Australia
R. Bryant
Affiliation:
Brain Dynamics Centre, Westmead Millennium Institute, Westmead Hospital, Australia School of Psychology, University of New South Wales, Australia
*
*Address for correspondence: Dr K. Felmingham, Brain Dynamics Centre, Westmead Hospital, Westmead, NSW 2145, Australia. (Email: kim_felmingham@wmi.usyd.edu.au)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Dissociative reactions in post-traumatic stress disorder (PTSD) have been regarded as strategic responses that limit arousal. Neuroimaging studies suggest distinct prefrontal responses in individuals displaying dissociative and hyperarousal responses to threat in PTSD. Increased prefrontal activity may reflect enhanced regulation of limbic arousal networks in dissociation. If dissociation is a higher-order regulatory response to threat, there may be differential responses to conscious and automatic processing of threat stimuli. This study addresses this question by examining the impact of dissociation on fear processing at different levels of awareness.

Method

Functional magnetic resonance imaging (fMRI) with a 1.5-T scanner was used to examine activation to fearful (versus neutral) facial expressions during consciously attended and non-conscious (using backward masking) conditions in 23 individuals with PTSD. Activation in 11 individuals displaying non-dissociative reactions was compared to activation in 12 displaying dissociative reactions to consciously and non-consciously perceived fear stimuli.

Results

Dissociative PTSD was associated with enhanced activation in the ventral prefrontal cortex for conscious fear, and in the bilateral amygdala, insula and left thalamus for non-conscious fear compared to non-dissociative PTSD. Comparatively reduced activation in the dissociative group was apparent in dorsomedial prefrontal regions for conscious fear faces.

Conclusions

These findings confirm our hypotheses of enhanced prefrontal activity to conscious fear and enhanced activity in limbic networks to non-conscious fear in dissociative PTSD. This supports the theory that dissociation is a regulatory strategy invoked to cope with extreme arousal in PTSD, but this strategy appears to function only during conscious processing of threat.

Keywords

DissociationfearfMRInon-consciousPTSD
Type
Original Articles
Information
Psychological Medicine , Volume 38 , Issue 12 , December 2008 , pp. 1771 - 1780
Copyright
Copyright © 2008 Cambridge University Press

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

Blake, DD, Weathers, FW, Nagy, LM, Kaloupek, DG, Klauminzer, G, Charney, DS, Keane, TM (1990). A clinician rating scale for assessing current and lifetime PTSD: The CAPS-1. Behavior Therapist 13, 187–188.Google Scholar
Bremner, JD (1999). Acute and chronic responses to psychological trauma: where do we go from here? American Journal of Psychiatry 156, 349–351.CrossRefGoogle Scholar
Bremner, JD, Krystal, JH, Putnam, F, Southwick, SM, Marmar, C, Charney, DS, Mazure, CM (1998). Measurement of dissociative states with the Clinician Administered Dissociative States Scale (CADDS). Journal of Traumatic Stress 11, 125–136.CrossRefGoogle Scholar
Britton, JC, Phan, KL, Taylor, SF, Fig, LM, Liberzon, I (2005). Corticolimbic blood flow in posttraumatic stress disorder during script-driven imagery. Biological Psychiatry 57, 832–840.CrossRefGoogle ScholarPubMed
Bush, G, Phan, KL, Posner, MI (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 4, 215–222.CrossRefGoogle ScholarPubMed
Clark, CR, McFarlane, AC, Morris, P, Weber, DL, Sonkkilla, C, Shaw, M (2003). Cerebral function in posttraumatic stress disorder during verbal working memory updating: a positron emission tomography study. Biological Psychiatry 53, 474–481.CrossRefGoogle ScholarPubMed
Craig, AD (2004). Human feelings: why are some more aware than others? Trends in Cognitive Sciences 8, 239–241.CrossRefGoogle ScholarPubMed
Critchley, HD, Wiens, S, Rotshtein, P, Ohman, A, Dolan, RJ (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience 7, 189–195.CrossRefGoogle ScholarPubMed
Devinsky, O, Morrell, MJ, Vogt, BA (1995). Contributions of anterior cingulate cortex to behaviour. Brain 118, 279–306.CrossRefGoogle ScholarPubMed
Devinsky, O, Putnam, F, Grafman, J, Bromfeld, E, Theodore, WH (1989). Dissociative states and epilepsy. Neurology 39, 835–840.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1997). Structured clinical interview for DSM-IV axis I disorders – clinician version (SCID-CV). New York State Psychiatric Institute, Biometrics Research: New York.Google Scholar
Griffin, GM, Resick, P, Mechanic, MB (1997). Objective assessment of peritraumatic dissociation: psychophysiological indicators. American Journal of Psychiatry 154, 1081–1088.Google ScholarPubMed
Gur, RC, Sara, R, Hagendoorn, M, Maron, O, Hughgett, P, Turner, TH, Bajcsy, R, Gur, RE (2002). A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. Journal of Neuroscience Methods 115, 137–143.CrossRefGoogle ScholarPubMed
Harvey, AG, Bryant, RA, Rapee, R (1996). Supraliminal and subliminal processing of threat-related material in post-traumatic stress disorder. Cognitive Therapy and Research, 20, 613–623.CrossRefGoogle Scholar
Hollander, E, Carrasco, JL, Mullen, LS, Trungold, S, DeCaria, CM, Towey, J (1992). Left hemispheric activation in depersonalization disorder: a case report. Biological Psychiatry 31, 1157–1162.CrossRefGoogle ScholarPubMed
Lanius, RA, Williamson, PC, Densmore, M, Boksman, K, Gupta, M, Neufeld, RW, Gati, JS, Menon, RS (2001). Neural correlates of traumatic memories in posttraumatic stress disorder: a functional MRI investigation. American Journal of Psychiatry 158, 1920–1922.CrossRefGoogle ScholarPubMed
Lanius, RA, Bluhm, R, Lanius, U, Pain, C (2006). A review of neuroimaging studies in PTSD: heterogeneity of response to symptom provocation. Journal of Psychiatric Research 40, 709–729.CrossRefGoogle ScholarPubMed
Lanius, RA, Williamson, PC, Bluhm, RL, Densmore, M, Boksman, K, Neufeld, RWJ, Gati, JS, Menon, RS (2005). Functional connectivity of dissociative responses in posttraumatic stress disorder: a functional magnetic resonance imaging investigation. Biological Psychiatry 57, 873–884.CrossRefGoogle ScholarPubMed
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. Biological Psychiatry 52, 305–311.CrossRefGoogle ScholarPubMed
Liberzon, I, Taylor, SF, Amdur, R, Jung, TD, Chamberlain, KR, Minoshima, S, Koeppe, RA, Fig, LM (1999). Brain activation in PTSD in response to trauma-related stimuli. Biological Psychiatry 45, 817–826.CrossRefGoogle ScholarPubMed
Liddell, BJ, Brown, KJ, Kemp, AH, Barton, MJ, Das, P, Peduto, A, Gordon, E, Williams, LM (2005). A direct brainstem-amygdala-cortical ‘alarm’ system for subliminal signals of fear. NeuroImage 24, 235–243.CrossRefGoogle ScholarPubMed
Morgan, MA, Romanski, LM, LeDoux, JE (1993). Extinction of emotional learning: contribution of medial prefrontal cortex. Neuroscience Letters 163, 109–113.CrossRefGoogle ScholarPubMed
Nagai, Y, Critchley, JD, Featherstone, E, Trimble, MR, Dolan, RJ (2004). Activity in ventromedial prefrontal cortex covaries with sympathetic skin conductance: a physiological account of a ‘default mode’ of brain function. Neuroimage 22, 243–251.CrossRefGoogle ScholarPubMed
Noyes, R, Kletti, R (1977). Depersonalization in response to life-threatening danger. Comprehensive Psychiatry 18, 374–384.CrossRefGoogle ScholarPubMed
Penny, WD, Ashburner, J, Kiebel, S, Henson, R, Glaser, DE, Phillips, C (2001). Statistical Parametric Mapping: an annotated bibliography (http://www.fil.ion.ucl.ac.uk/spm/course/notes02/misc/bib.pdf).Google Scholar
Phan, KL, Wager, T, Taylor, SF, Liberzon, I (2003). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 16, 331–348.CrossRefGoogle Scholar
Phelps, EA, Delgado, MR, Nearing, KI, LeDoux, JE (2004). Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43, 897–905.CrossRefGoogle ScholarPubMed
Phillips, ML, Medford, N, Senior, C, Bullmore, ET, Suckling, J, Brammer, MJ (2001). Depersonalization disorder: thinking without feeling. Psychiatry Research 108, 145–160.CrossRefGoogle ScholarPubMed
Rauch, SL, Whalen, PJ, Shin, LM, McInerney, SC, Macklin, ML, Lasko, NB (2000). Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biological Psychiatry 47, 769–776.CrossRefGoogle ScholarPubMed
Shin, LM, Orr, SP, Carson, MA, Rauch, SL, Macklin, ML, Lasko, NB (2004). Regional cerebral blood flow in the amygdala and medial prefrontal cortex during traumatic imagery in male and female Vietnam veterans with PTSD. Archives of General Psychiatry 61, 168–176.CrossRefGoogle ScholarPubMed
Shin, LM, Wright, CI, Cannistraro, PA, Wedig, MM, McMullin, K, Martis, B, Macklin, ML, Lasko, M, Cavanagh, SR, Krangek, TS, Orr, SP, Pitman, RK, Whalen, PJ, Rauch, SL (2005). A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Archives of General Psychiatry 62, 273–281.CrossRefGoogle ScholarPubMed
Sierra, M, Berrios, GE (1998). Depersonalization: neurobiological perspectives. Biological Psychiatry 44, 898–908.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273–289.CrossRefGoogle ScholarPubMed
Weathers, FW, Keane, TM, Davidson, JRT (2001). Clinician administered PTSD scale: a review of the first 10 years of research. Depression and Anxiety 13, 132–154.CrossRefGoogle Scholar
Williams, LM, Das, P, Liddell, BJ, Kemp, AH, Rennie, CJ, Gordon, E (2006 a). Mode of functional connectivity in amygdala pathways dissociates level of awareness for signals of fear. Journal of Neuroscience 26, 9246–9271.CrossRefGoogle ScholarPubMed
Williams, LM, Kemp, AH, Felmingham, KL, Barton, M, Olivieri, G, Peduto, AS, Gordon, E, Bryant, RA (2006 b). Trauma modulates amygdala and medial prefrontal responses to consciously attended fear. NeuroImage 29, 347–357.CrossRefGoogle ScholarPubMed
Williams, LM, Liddell, BJ, Rathjen, J, Brown, KJ, Gray, J, Phillips, M, Young, A, Gordon, E (2004). Mapping the timecourse of nonconscious and conscious perception of fear: an integration of central and peripheral measures. Human Brain Mapping 21, 64–74.CrossRefGoogle Scholar