Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-14T07:27:30.324Z Has data issue: false hasContentIssue false

The distinctive neural circuitry of complex posttraumatic stress disorder during threat processing

Published online by Cambridge University Press:  08 January 2020

Richard A. Bryant*
Affiliation:
School of Psychology, University of New South Wales, Sydney, NSW 2052, Australia Brain Dynamics Centre, Westmead Institute of Medical Research, University of Sydney, Westmead, Australia
Kim L. Felmingham
Affiliation:
Department of Psychological Medicine, University of Melbourne, Melbourne, Australia
Gin Malhi
Affiliation:
Department of Psychiatry, University of Sydney, Sydney, Australia
Elpiniki Andrew
Affiliation:
School of Psychology, University of New South Wales, Sydney, NSW 2052, Australia Brain Dynamics Centre, Westmead Institute of Medical Research, University of Sydney, Westmead, Australia
Mayuresh S. Korgaonkar
Affiliation:
Brain Dynamics Centre, Westmead Institute of Medical Research, University of Sydney, Westmead, Australia Department of Psychiatry, University of Sydney, Sydney, Australia
*
Author for correspondence: Richard A. Bryant, E-mail: [email protected]

Abstract

Background

There is controversy over the extent to which the new International Classification of Diseases (ICD-11) diagnosis of complex posttraumatic stress disorder (CPTSD) is distinct from posttraumatic stress disorder (PTSD). This study aimed to conduct the first investigation of distinctive neural processes during threat processing in CPTSD relative to PTSD.

Method

This cross-sectional functional magnetic resonance study included 99 participants who met criteria for PTSD (PTSD = 32, CPTSD = 28) and 39 trauma-exposed controls. PTSD was assessed with the Clinician-Administered PTSD Scale (CAPS). CPTSD was assessed with an adapted version of the International Trauma Questionnaire. Neural responses were measured across the brain while threat or neutral faces were presented at both supraliminal and subliminal levels.

Results

During supraliminal presentations of threat stimuli, there was greater bilateral insula and right amygdala activation in CPTSD participants relative to PTSD. Reduced supraliminal right dorsolateral prefrontal cortex activation and increased subliminal amygdala and insula activation were observed as common dysfunction for both CPTSD and PTSD groups relative to trauma controls. There were no significant differences in terms of subliminal presentations and no differences in functional connectivity. Dissociative responses were positively associated with right insula activation (r = 0.347, p < 0.01).

Conclusions

These results provide the first evidence of distinct neural profiles of CPTSD and PTSD during threat processing. The observation of increased insula and right amygdala activation in CPTSD accords with the proposal that CPTSD is distinguished from PTSD by disturbances in emotion regulation and self-concept.

Type
Original Article
Copyright
Copyright © Cambridge University Press 2020

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

Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Beck depression Inventory (2nd ed.). San Antonio, TX: The Psychological Corporation.Google Scholar
Blake, D. D., Weathers, F., Nagy, L. M., Kaloupek, D. G., Gusman, F. D., Charney, D. S., & Keane, T. M. (1995). The development of a clinician administered PTSD scale. Journal of Traumatic Stress, 8, 7590.CrossRefGoogle ScholarPubMed
Bremner, J. D., Krystal, J. H., Putnam, F. W., Southwick, S. M., Marmar, C., Charney, D. S., & Mazure, C. M. (1998). Measurement of dissociative states with the Clinician-Administered Dissociative States Scale (CADSS). Journal of Traumatic Stress, 11, 125136.CrossRefGoogle ScholarPubMed
Brewin, C. R., Cloitre, M., Hyland, P., Shevlin, M., Maercker, A., Bryant, R. A., … Reed, G. M. (2017). A review of current evidence regarding the ICD-11 proposals for diagnosing PTSD and complex PTSD. Clinical Psychological Review, 58, 115.CrossRefGoogle ScholarPubMed
Bryant, R. A., Kemp, A. H., Felmingham, K. L., Liddell, B., Olivieri, G., Peduto, A., … Williams, L. M. (2008). Enhanced amygdala and medial prefrontal activation during nonconscious processing of fear in posttraumatic stress disorder: An fMRI study. Human Brain Mapping, 29, 517523.CrossRefGoogle ScholarPubMed
Choi, J., Jeong, B., Polcari, A., Rohan, M. L., & Teicher, M. H. (2012). Reduced fractional anisotropy in the visual limbic pathway of young adults witnessing domestic violence in childhood. Neuroimage, 59, 10711079.10.1016/j.neuroimage.2011.09.033CrossRefGoogle ScholarPubMed
Cloitre, M., Garvert, D. W., Weiss, B., Carlson, E. B., & Bryant, R. A. (2014). Distinguishing PTSD, complex PTSD, and borderline personality disorder: A latent class analysis. European Journal of Psychotraumatology, 5, 25097.CrossRefGoogle ScholarPubMed
Cloitre, M., Shevlin, M., Brewin, C. R., Bisson, J. I., Roberts, N. P., Maercker, A., … Hyland, P. (2018). The International Trauma Questionnaire: Development of a self-report measure of ICD-11 PTSD and complex PTSD. Acta Psychiatrica Scandinavia, 138, 536546.CrossRefGoogle ScholarPubMed
Craig, A. D. (2009). How do you feel--now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10, 5970.10.1038/nrn2555CrossRefGoogle Scholar
Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7, 189195.10.1038/nn1176CrossRefGoogle ScholarPubMed
Damasio, A. R., Grabowski, T. J., Bechara, A., Damasio, H., Ponto, L. L., Parvizi, J., & Hichwa, R. D. (2000). Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neuroscience, 3, 10491056.10.1038/79871CrossRefGoogle ScholarPubMed
Dehaene, S., & Changeux, J. P. (2011). Experimental and theoretical approaches to conscious processing. Neuron, 70, 200227.CrossRefGoogle ScholarPubMed
Dehaene, S., Changeux, J. P., Naccache, L., Sackur, J., & Sergent, C. (2006). Conscious, preconscious, and subliminal processing: A testable taxonomy. Trends in Cognitive Science, 10, 204211.CrossRefGoogle ScholarPubMed
Felmingham, K., Kemp, A. H., Williams, L., Falconer, E., Olivieri, G., Peduto, A., & Bryant, R. A. (2008). Dissociative responses to conscious and non-conscious fear impact underlying brain function in post-traumatic stress disorder. Psychological Medicine, 38, 17711780.CrossRefGoogle ScholarPubMed
Fitzgerald, J. M., DiGangi, J. A., & Phan, K. L. (2018). Functional neuroanatomy of emotion and its regulation in PTSD. Harvard Review of Psychiatry, 26, 116128.CrossRefGoogle ScholarPubMed
Fonzo, G. A., Simmons, A. N., Thorp, S. R., Norman, S. B., Paulus, M. P., & Stein, M. B. (2010). Exaggerated and disconnected insular-amygdalar blood oxygenation level-dependent response to threat-related emotional faces in women with intimate-partner violence posttraumatic stress disorder. Biological Psychiatry, 68, 433441.CrossRefGoogle ScholarPubMed
Friedman, M. J., Resick, P. A., Bryant, R. A., & Brewin, C. R. (2011). Considering PTSD for DSM-V. Depression and Anxiety, 28, 750769.10.1002/da.20767CrossRefGoogle Scholar
Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., Allen, P., Surguladze, S., … Politi, P. (2009). Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry and Neuroscience, 34, 418432.Google ScholarPubMed
Hanson, J. L., Nacewicz, B. M., Sutterer, M. J., Cayo, A. A., Schaefer, S. M., Rudolph, K. D., … Davidson, R. J. (2015). Behavioral problems after early life stress: Contributions of the hippocampus and amygdala. Biological Psychiatry, 77, 314323.CrossRefGoogle ScholarPubMed
Jovanovic, T., & Ressler, K. J. (2010). How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. American Journal of Psychiatry, 167, 648662.CrossRefGoogle ScholarPubMed
Karatzias, T., Shevlin, M., Fyvie, C., Hyland, P., Efthymiadou, E., Wilson, D., … Cloitre, M. (2017). Evidence of distinct profiles of Posttraumatic Stress Disorder (PTSD) and Complex Posttraumatic Stress Disorder (CPTSD) based on the new ICD-11 Trauma Questionnaire (ICD-TQ). Journal of Affective Disorders, 207, 181187.10.1016/j.jad.2016.09.032CrossRefGoogle ScholarPubMed
Knefel, M., & Lueger-Schuster, B. (2013). An evaluation of ICD-11 PTSD and complex PTSD criteria in a sample of adult survivors of childhood institutional abuse. European Journal of Psychotraumatology, 4, 22608.CrossRefGoogle Scholar
Korgaonkar, M. S., Grieve, S. M., Etkin, A., Koslow, S. H., & Williams, L. M. (2013). Using standardized fMRI protocols to identify patterns of prefrontal circuit dysregulation that are common and specific to cognitive and emotional tasks in major depressive disorder: First wave results from the iSPOT-D study. Neuropsychopharmacology, 38, 863871.CrossRefGoogle ScholarPubMed
Lanius, R. A., Frewen, P. A., Girotti, M., Neufeld, R. W. J., Stevens, T. K., & Densmore, M. (2007). Neural correlates of trauma script-imagery in posttraumatic stress disorder with and without comorbid major depression: A functional MRI investigation. Psychiatry Research, 155, 4556.10.1016/j.pscychresns.2006.11.006CrossRefGoogle ScholarPubMed
Lanius, R. A., Vermetten, E., Loewenstein, R. J., Brand, B., Schmahl, C., Bremner, J. D., & Spiegel, D. (2010). A dissociative subtype of PTSD: Clinical and neurobiological evidence. American Journal of Psychiatry, 167, 640647.CrossRefGoogle ScholarPubMed
Ludascher, P., Valerius, G., Stiglmayr, C., Mauchnik, J., Lanius, R. A., Bohus, M., & Schmahl, C. (2010). Pain sensitivity and neural processing during dissociative states in patients with borderline personality disorder with and without comorbid posttraumatic stress disorder: A pilot study. Journal of Psychiatry and Neuroscience, 35, 177184.10.1503/jpn.090022CrossRefGoogle ScholarPubMed
McCrory, E. J., De Brito, S. A., Sebastian, C. L., Mechelli, A., Bird, G., Kelly, P. A., & Viding, E. (2011). Heightened neural reactivity to threat in child victims of family violence. Current Biology, 21, R947R948.CrossRefGoogle ScholarPubMed
McLaren, D. G., Ries, z. M. L., Xu, G., & Johnson, S. C. (2012). A generalized form of context dependent psychophysiological interactions (gPPI): A comparison to standard approaches. Neuroimage, 61, 12771286.10.1016/j.neuroimage.2012.03.068CrossRefGoogle ScholarPubMed
Mier, D., Lis, S., Esslinger, C., Sauer, C., Hagenhoff, M., Ulferts, J., … Kirsch, P. (2013). Neuronal correlates of social cognition in borderline personality disorder. Social Cognitive and Affective Neurosciences, 8, 531537.CrossRefGoogle ScholarPubMed
Morey, R. A., Dunsmoor, J. E., Haswell, C. C., Brown, V. M., Vora, A., Weiner, J., … LaBar, K. S. (2015). Fear learning circuitry is biased toward generalization of fear associations in posttraumatic stress disorder. Translational Psychiatry, 5, e700.CrossRefGoogle ScholarPubMed
Phelps, E. A., Delgado, M. R., Nearing, K. I., & LeDoux, J. E. (2004). Extinction learning in humans: Role of the amygdala and vmPFC. Neuron, 43, 897905.CrossRefGoogle ScholarPubMed
Rabinak, C. A., MacNamara, A., Kennedy, A. E., Angstadt, M., Stein, M. B., Liberzon, I., & Phan, K. L. (2014). Focal and aberrant prefrontal engagement during emotion regulation in veterans with posttraumatic stress disorder. Depression and Anxiety, 31, 851861.10.1002/da.22243CrossRefGoogle ScholarPubMed
Resick, P. A., Bovin, M. J., Calloway, A. L., Dick, A. M., King, M. W., Mitchell, K. S., … Wolf, E. J. (2012). A critical evaluation of the complex PTSD literature: Implications for DSM-5. Journal of Traumatic Stress, 25, 241251.CrossRefGoogle ScholarPubMed
Schmahl, C., Herpertz, S. C., Bertsch, K., Ende, G., Flor, H., Kirsch, P., … Bohus, M. (2014). Mechanisms of disturbed emotion processing and social interaction in borderline personality disorder: State of knowledge and research agenda of the German Clinical Research Unit. Borderline Personality Disorder and Emotion Dysregulation, 1, 12.CrossRefGoogle ScholarPubMed
Schulze, L., Domes, G., Kruger, A., Berger, C., Fleischer, M., Prehn, K., … Herpertz, S. C. (2011). Neuronal correlates of cognitive reappraisal in borderline patients with affective instability. Biological Psychiatry, 69, 564573.CrossRefGoogle ScholarPubMed
Schulze, L., Schmahl, C., & Niedtfeld, I. (2016). Neural correlates of disturbed emotion processing in borderline personality disorder: A multimodal meta-analysis. Biological Psychiatry, 79, 97106.CrossRefGoogle ScholarPubMed
Schulze, L., Schulze, A., Renneberg, B., Schmahl, C., & Niedtfeld, I. (2019). Neural correlates of affective disturbances: A comparative meta-analysis of negative affect processing in borderline personality disorder, major depressive disorder, and posttraumatic stress disorder. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4, 220232.Google ScholarPubMed
Shalev, A., Liberzon, I., & Marmar, C. (2017). Post-traumatic stress disorder. New England Journal of Medicine, 376, 24592469.CrossRefGoogle ScholarPubMed
Sheehan, D. V., Lecrubier, Y., Harnett-Sheehan, K., Amorim, P., Janavs, J., Weiller, E., … Dunbar, G. (1998). The Mini International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview. Journal of Clinical Pscyhiatry, 59, 2233.Google ScholarPubMed
Shin, L. M., Wright, C. I., Cannistraro, P. A., Wedig, M. M., McMullin, K., Martis, B., … Rauch, S. L. (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, 273281.CrossRefGoogle ScholarPubMed
Teicher, M. H., Anderson, C. M., Ohashi, K., & Polcari, A. (2014). Childhood maltreatment: Altered network centrality of cingulate, precuneus, temporal pole and insula. Biological Psychiatry, 76, 297305.10.1016/j.biopsych.2013.09.016CrossRefGoogle ScholarPubMed
van Harmelen, A. L., van Tol, M. J., Demenescu, L. R., van der Wee, N. J., Veltman, D. J., Aleman, A., … Elzinga, B. M. (2013). Enhanced amygdala reactivity to emotional faces in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience, 8, 362369.CrossRefGoogle ScholarPubMed
White, S. F., Costanzo, M. E., Blair, J. R., & Roy, M. J. (2015). PTSD Symptom severity is associated with increased recruitment of top-down attentional control in a trauma-exposed sample. Neuroimage Clinical, 7, 1927.CrossRefGoogle Scholar
Williams, L. M., Liddell, B. J., Rathjen, J., Brown, K. J., Gray, J., Phillips, M., … Gordon, E. (2004). Mapping the time course of nonconscious and conscious perception of fear: An integration of central and peripheral measures. Human Brain Mapping, 21, 6474.CrossRefGoogle ScholarPubMed
World Health Organization. (2018). ICD-11: International classification of diseases 11th revision. Geneva: World Health Organization. Available at http://www.who.int/classifications/icd/revision/en/.Google Scholar
Supplementary material: File

Bryant et al. supplementary material

Bryant et al. supplementary material

Download Bryant et al. supplementary material(File)
File 32.7 KB