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Reappraisal-related neural predictors of treatment response to cognitive behavior therapy for post-traumatic stress disorder

Published online by Cambridge University Press:  05 May 2020

Richard A. Bryant Open the ORCID record for Richard A. Bryant [Opens in a new window] ,
May Erlinger ,
Kim Felmingham ,
Aleksandra Klimova ,
Leanne M. Williams ,
Gin Malhi ,
David Forbes  and
Mayuresh S. Korgaonkar
Richard A. Bryant*
Affiliation:
University of New South Wales, School, Sydney, Australia Brain Dynamics Centre, Westmead Institute for Medical Research, University of Sydney, Westmead, Australia
May Erlinger
Affiliation:
Brain Dynamics Centre, Westmead Institute for Medical Research, University of Sydney, Westmead, Australia
Kim Felmingham
Affiliation:
Department of Psychological Medicine, University of Melbourne, Melbourne, Australia
Aleksandra Klimova
Affiliation:
Brain Dynamics Centre, Westmead Institute for Medical Research, University of Sydney, Westmead, Australia
Leanne M. Williams
Affiliation:
Department of Psychiatry and Behavioral Sciences, Stanford University, San Francisco, USA Sierra-Pacific Mental Illness Research, Education, and Clinical Center (MIRECC) VA Palo Alto Health Care System, San Francisco, USA
Gin Malhi
Affiliation:
Department of Psychiatry, University of Sydney, Sydney, Australia
David Forbes
Affiliation:
Phoenix Australia, University of Melbourne, Melbourne, Australia
Mayuresh S. Korgaonkar
Affiliation:
Brain Dynamics Centre, Westmead Institute for Medical Research, University of Sydney, Westmead, Australia Department of Psychiatry, University of Sydney, Sydney, Australia
*
Author for correspondence: Richard A. Bryant, E-mail: r.bryant@unsw.edu.au
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Abstract

Background

Although trauma-focused cognitive behavior therapy (TF-CBT) is the frontline treatment for post-traumatic stress disorder (PTSD), one-third of patients are treatment non-responders. To identify neural markers of treatment response to TF-CBT when participants are reappraising aversive material.

Methods

This study assessed PTSD patients (n = 37) prior to TF-CBT during functional magnetic brain resonance imaging (fMRI) when they reappraised or watched traumatic images. Patients then underwent nine sessions of TF-CBT, and were then assessed for symptom severity on the Clinician-Administered PTSD Scale. FMRI responses for cognitive reappraisal and emotional reactivity contrasts of traumatic images were correlated with the reduction of PTSD severity from pretreatment to post-treatment.

Results

Symptom improvement was associated with decreased activation of the left amygdala during reappraisal, but increased activation of bilateral amygdala and hippocampus during emotional reactivity prior to treatment. Lower connectivity of the left amygdala to the subgenual anterior cingulate cortex, pregenual anterior cingulate cortex, and right insula, and that between the left hippocampus and right amygdala were also associated with symptom improvement.

Conclusions

These findings provide evidence that optimal treatment response to TF-CBT involves the capacity to engage emotional networks during emotional processing, and also to reduce the engagement of these networks when down-regulating emotions.

Keywords

Functional magnetic resonance imagingpost-traumatic stress disorderpredictionreappraisaltrauma-focused cognitive behavior therapy
Type
Original Article
Information
Psychological Medicine , Volume 51 , Issue 14 , October 2021 , pp. 2454 - 2464
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Aupperle, R. L., Allard, C. B., Simmons, A. N., Flagan, T., Thorp, S. R., Norman, S. B., … Stein, M. B. (2013). Neural responses during emotional processing before and after cognitive trauma therapy for battered women. Psychiatry Research, 214, 48–55.CrossRefGoogle ScholarPubMed
Ball, T. M., Stein, M. B., Ramsawh, H. J., Campbell-Sills, L., & Paulus, M. P. (2014). Single-subject anxiety treatment outcome prediction using functional neuroimaging. Neuropsychopharmacology, 39, 1254–1261.CrossRefGoogle ScholarPubMed
Banks, S. J., Eddy, K. T., Angstadt, M., Nathan, P. J., & Phan, K. L. (2007). Amygdala-frontal connectivity during emotion regulation. Social, Cognitive, and Affective Neuroscience, 2, 303–312.CrossRefGoogle ScholarPubMed
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, 75–90.CrossRefGoogle ScholarPubMed
Blanchard, E. B., Hickling, E. J., Malta, L. S., Jaccard, J., Devineni, T., Veazey, C. H., & Galovski, T. E. (2003). Prediction of response to psychological treatment among motor vehicle accident survivors with PTSD. Behavior Therapy, 34, 351–363.CrossRefGoogle Scholar
Bradley, R., Greene, J., Russ, E., Dutra, L., & Westen, D. (2005). A multidimensional meta-analysis of psychotherapy for PTSD. American Journal of Psychiatry, 162, 214–227.CrossRefGoogle ScholarPubMed
Bryant, R. A., Felmingham, K., Kemp, A., Das, P., Hughes, G., Peduto, A., & Williams, L. (2008). Amygdala and ventral anterior cingulate activation predicts treatment response to cognitive behaviour therapy for post-traumatic stress disorder. Psychological Medicine, 38, 555–561.CrossRefGoogle ScholarPubMed
Bryant, R. A., Mastrodomenico, J., Hopwood, S., Kenny, L., Cahill, C., Kandris, K., & Taylor, K. (2013). Augmenting cognitive behavior therapy for PTSD with emotion tolerance training: A randomized controlled trial. Psychological Medicine, 43, 2153–2160.CrossRefGoogle ScholarPubMed
Buhle, J. T., Silvers, J. A., Wager, T. D., Lopez, R., Onyemekwu, C., Kober, H., … Ochsner, K. N. (2014). Cognitive reappraisal of emotion: A meta-analysis of human neuroimaging studies. Cerebral Cortex, 24, 2981–2990.CrossRefGoogle ScholarPubMed
Cisler, J. M., Sigel, B. A., Steele, J. S., Smitherman, S., Vanderzee, K., Pemberton, J., … Kilts, C. D. (2016). Changes in functional connectivity of the amygdala during cognitive reappraisal predict symptom reduction during trauma-focused cognitive-behavioral therapy among adolescent girls with post-traumatic stress disorder. Psychological Medicine, 46, 3013–3023.CrossRefGoogle ScholarPubMed
Cisler, J. M., Steele, J. S., Lenow, J. K., Smitherman, S., Everett, B., Messias, E., & Kilts, C. D. (2014). Functional reorganization of neural networks during repeated exposure to the traumatic memory in posttraumatic stress disorder: An exploratory fMRI study. Journal of Psychiatric Research, 48, 47–55.CrossRefGoogle ScholarPubMed
Craske, M. G., Kircanski, K., Zelikowsky, M., Mystkowski, J., Chowdhury, N., & Baker, A. (2008). Optimizing inhibitory learning during exposure therapy. Behaviour Research and Therapy, 46, 5–27.CrossRefGoogle ScholarPubMed
Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry, 164, 1476–1488.CrossRefGoogle ScholarPubMed
Falconer, E., Allen, A., Felmingham, K. L., Williams, L. M., & Bryant, R. A. (2013). Inhibitory neural activity predicts response to cognitive-behavioral therapy for posttraumatic stress disorder. Journal of Clinical Psychiatry, 74, 895–901.CrossRefGoogle ScholarPubMed
Foa, E. B. (2006). Psychosocial therapy for posttraumatic stress disorder. Journal of Clinical Psychiatry, 67, 40–45.Google ScholarPubMed
Fonzo, G. A., Goodkind, M. S., Oathes, D. J., Zaiko, Y. V., Harvey, M., Peng, K. K., … Etkin, A. (2017). PTSD psychotherapy outcome predicted by brain activation during emotional reactivity and regulation. American Journal of Psychiatry, 174, 1163–1174.CrossRefGoogle ScholarPubMed
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, 170–180.CrossRefGoogle ScholarPubMed
Goldin, P. R., McRae, K., Ramel, W., & Gross, J. J. (2008). The neural bases of emotion regulation: Reappraisal and suppression of negative emotion. Biological Psychiatry, 63, 577–586.CrossRefGoogle ScholarPubMed
Goldin, P. R., Ziv, M., Jazaieri, H., Hahn, K., Heimberg, R., & Gross, J. J. (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, 1048–1056.CrossRefGoogle ScholarPubMed
Greco, J. A., & Liberzon, I. (2016). Neuroimaging of fear-associated learning. Neuropsychopharmacology, 41, 320–334.CrossRefGoogle ScholarPubMed
Gross, J. J. (1998). Antecedent- and response-focused emotion regulation: Divergent consequences for experience, expression, and physiology. Journal of Personality and Social Psychology, 74, 224–237.CrossRefGoogle ScholarPubMed
Institute of Medicine. (2008). Treatment of posttraumatic stress disorder: An assessment of the evidence. Washington, DC: Institute of Medicine.Google Scholar
Klumpp, H., Fitzgerald, D. A., & Phan, K. L. (2013). Neural predictors and mechanisms of cognitive behavioral therapy on threat processing in social anxiety disorder. Progress in Neuropsychopharmacology and Biological Psychiatry, 45, 83–91.CrossRefGoogle ScholarPubMed
Kober, H., Barrett, L. F., Joseph, J., Bliss-Moreau, E., Lindquist, K., & Wager, T. D. (2008). Functional grouping and cortical-subcortical interactions in emotion: A meta-analysis of neuroimaging studies. Neuroimage, 42, 998–1031.CrossRefGoogle ScholarPubMed
Kozel, F.A., Motes, M.A., Didehbani, N., DeLaRosa, B., Bass, C., Schraufnagel, C.D., … Hart, J. Jr. (2018). Repetitive TMS to augment cognitive processing therapy in combat veterans of recent conflicts with PTSD: A randomized clinical trial. Journal of Affective Disorders, 229, 506–514.CrossRefGoogle ScholarPubMed
Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2005). International affective picture system (IAPS): Affective ratings of pictures and instruction manual. Gainesville, FL: University of Florida.Google Scholar
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, 640–647.CrossRefGoogle ScholarPubMed
McLaren, D. G., Ries, M. L., Xu, G., & Johnson, S. C. (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches. Neuroimage, 61, 1277–1286.CrossRefGoogle ScholarPubMed
McLean, C.P., Asnaani, A., & Foa, E.B. (2015). Prolonged exposure therapy. In Schnyder, U. & Cloitre, M. (Eds.), Evidence based treatments for trauma-related psychological disorders (pp. 143–159). Heidelberg: Springer.Google Scholar
National Institute of Clinical Excellence. (2005). The management of PTSD in adults and children in primary and secondary care. Wiltshire: National Institute of Clinical Excellence.Google Scholar
New, A. S., Fan, J., Murrough, J. W., Liu, X., Liebman, R. E., Guise, K. G., … Charney, D. S. (2009). A functional magnetic resonance imaging study of deliberate emotion regulation in resilience and posttraumatic stress disorder. Biological Psychiatry, 66, 656–664.CrossRefGoogle ScholarPubMed
Nitschke, J. B., Sarinopoulos, I., Oathes, D. J., Johnstone, T., Whalen, P. J., Davidson, R. J., & Kalin, N. H. (2009). Anticipatory activation in the amygdala and anterior cingulate in generalized anxiety disorder and prediction of treatment response. American Journal of Psychiatry, 166, 302–310.CrossRefGoogle Scholar
Ochsner, K. N., Bunge, S. A., Gross, J. J., & Gabrieli, J. D. (2002). Rethinking feelings: An FMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience, 14, 1215–1229.CrossRefGoogle ScholarPubMed
Ochsner, K. N., Silvers, J. A., & Buhle, J. T. (2012). Functional imaging studies of emotion regulation: A synthetic review and evolving model of the cognitive control of emotion. Annals of the New York Academy of Sciences, 1251, E1–24.CrossRefGoogle ScholarPubMed
Paquette, V., Levesque, J., Mensour, B., Leroux, J. M., Beaudoin, G., Bourgouin, P., & Beauregard, M. (2003). ‘Change the mind and you change the brain’: Effects of cognitive-behavioral therapy on the neural correlates of spider phobia. Neuroimage, 18, 401–409.CrossRefGoogle Scholar
Parsons, R. G., & Ressler, K. J. (2013). Implications of memory modulation for post-traumatic stress and fear disorders. Nature Neuroscience, 16, 146–153.CrossRefGoogle ScholarPubMed
Paschke, L. M., Dorfel, D., Steimke, R., Trempler, I., Magrabi, A., Ludwig, V. U., … Walter, H. (2016). Individual differences in self-reported self-control predict successful emotion regulation. Social, Cognitive, and Affective Neuroscience, 11, 1193–1204.CrossRefGoogle ScholarPubMed
Pico-Perez, M., Alonso, P., Contreras-Rodriguez, O., Martinez-Zalacain, I., Lopez-Sola, C., Jiminez-Murcia, S., … Soriano-Mas, C. (2018). Dispositional use of emotion regulation strategies and resting-state cortico-limbic functional connectivity. Brain Imaging and Behavior, 12, 1022–1031.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, 851–861.CrossRefGoogle ScholarPubMed
Reinecke, A., Thilo, K., Filippini, N., Croft, A., & Harmer, C. J. (2014). Predicting rapid response to cognitive-behavioural treatment for panic disorder: The role of hippocampus, insula, and dorsolateral prefrontal cortex. Behaviour Research and Therapy, 62, 120–128.CrossRefGoogle ScholarPubMed
Reinhardt, I., Jansen, A., Kellerman, T., Schuppen, A., Kohn, N., Gerlach, A. L., & Kircher, T. (2010). Neural correlates of aversive conditioning: Development of a functional imaging paradigm for the investigation of anxiety disorders. European Archives of Psychiatry and Clinical Neuroscience, 260, 443–453.CrossRefGoogle ScholarPubMed
Seligowski, A. V., Lee, D. J., Bardeen, J. R., & Orcutt, H. K. (2015). Emotion regulation and posttraumatic stress symptoms: A meta-analysis. Cognitive Behavior Therapy, 44, 87–102.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 Psychiatry, 59(Suppl 20), 22–33.Google ScholarPubMed
Shiba, Y., Oikonomidis, L., Sawiak, S., Fryer, T. D., Hong, Y. T., Cockcroft, G., … Roberts, A. C. (2017). Converging prefronto-insula-amygdala pathways in negative emotion regulation in marmoset monkeys. Biological Psychiatry, 82, 895–903.CrossRefGoogle ScholarPubMed
Siegle, G. J., Carter, C. S., & Thase, M. E. (2006). Use of FMRI to predict recovery from unipolar depression with cognitive behavior therapy. American Journal of Psychiatry, 163, 735–738.CrossRefGoogle ScholarPubMed
Straube, T., Glauer, M., Dilger, S., Mentzel, H. J., & Miltner, W. H. (2006). Effects of cognitive behavioral therapy on brain activation in specific phobia. Neuroimage, 29, 125–135.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., … Joliot, M. (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
Uchida, M., Biederman, J., Gabrieli, J. D., Micco, J., de Los Angeles, C., Brown, A., … Whitfield-Gabrieli, S. (2015). Emotion regulation ability varies in relation to intrinsic functional brain architecture. Social, Cognitive, and Affective Neuroscience, 10, 1738–1748.CrossRefGoogle ScholarPubMed
Urry, H. L., van Reekum, C. M., Johnstone, T., Kalin, N. H., Thurow, M. E., Schaefer, H. S., … Davidson, R. J. (2006). Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. Journal of Neuroscience, 26, 4415–4425.CrossRefGoogle ScholarPubMed
Whalen, P. J., Johnstone, T., Somerville, L. H., Nitschke, J. B., Polis, S., Alexander, A. L., … Kalin, N. H. (2008). A functional magnetic resonance imaging predictor of treatment response to venlafaxine in generalized anxiety disorder. Biological Psychiatry, 63, 858–863.CrossRefGoogle ScholarPubMed
Williams, L. M. (2016). Precision psychiatry: A neural circuit taxonomy for depression and anxiety. The Lancet. Psychiatry, 3, 472–480.CrossRefGoogle ScholarPubMed
Wolf, E. J., Lunny, C. A., & Schnurr, P. P. (2016). The influence of the dissociative subtype of posttraumatic stress disorder on treatment efficacy in female veterans and active duty service members. Journal of Consulting and Clinical Psychology, 84, 95–100.CrossRefGoogle ScholarPubMed
Zilverstand, A., Parvaz, M. A., & Goldstein, R. Z. (2017). Neuroimaging cognitive reappraisal in clinical populations to define neural targets for enhancing emotion regulation. A systematic review. Neuroimage, 151, 105–116.CrossRefGoogle ScholarPubMed
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