The neurobiology of emotion regulation in posttraumatic stress disorder: Amygdala downregulation via real‐time fMRI neurofeedback

Andrew A. Nicholson; Daniela Rabellino; Maria Densmore; Paul A. Frewen; Christian Paret; Rosemarie Kluetsch; Christian Schmahl; Jean Théberge; Richard W.J. Neufeld; Margaret C. McKinnon; Jeffrey P. Reiss; Rakesh Jetly; Ruth A. Lanius

doi:10.1002/hbm.23402

journal article Sep 20, 2016

The neurobiology of emotion regulation in posttraumatic stress disorder: Amygdala downregulation via real‐time fMRI neurofeedback

Andrew A. Nicholson Daniela Rabellino Maria Densmore Paul A. Frewen Christian Paret Rosemarie Kluetsch Christian Schmahl Jean Théberge Richard W.J. Neufeld Margaret C. McKinnon

Jeffrey P. Reiss Rakesh Jetly Ruth A. Lanius

Human Brain Mapping Vol. 38 No. 1 pp. 541-560 · Wiley

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Abstract

AbstractAmygdala dysregulation has been shown to be central to the pathophysiology of posttraumatic stress disorder (PTSD) representing a critical treatment target. Here, amygdala downregulation was targeted using real‐time fMRI neurofeedback (rt‐fMRI‐nf) in patients with PTSD, allowing us to examine further the regulation of emotional states during symptom provocation. Patients (n = 10) completed three sessions of rt‐fMRI‐nf with the instruction to downregulate activation in the amygdala, while viewing personalized trauma words. Amygdala downregulation was assessed by contrasting (a) regulate trials, with (b) viewing trauma words and not attempting to regulate. Training was followed by one transfer run not involving neurofeedback. Generalized psychophysiological interaction (gPPI) and dynamic causal modeling (DCM) analyses were also computed to explore task‐based functional connectivity and causal structure, respectively. It was found that PTSD patients were able to successfully downregulate both right and left amygdala activation, showing sustained effects within the transfer run. Increased activation in the dorsolateral and ventrolateral prefrontal cortex (PFC), regions related to emotion regulation, was observed during regulate as compared with view conditions. Importantly, activation in the PFC, rostral anterior cingulate cortex, and the insula, were negatively correlated to PTSD dissociative symptoms in the transfer run. Increased functional connectivity between the amygdala‐ and both the dorsolateral and dorsomedial PFC was found during regulate, as compared with view conditions during neurofeedback training. Finally, our DCM analysis exploring directional structure suggested that amygdala downregulation involves both top‐down and bottom‐up information flow with regard to observed PFC‐amygdala connectivity. This is the first demonstration of successful downregulation of the amygdala using rt‐fMRI‐nf in PTSD, which was critically sustained in a subsequent transfer run without neurofeedback, and corresponded to increased connectivity with prefrontal regions involved in emotion regulation during the intervention. Hum Brain Mapp 38:541–560, 2017. © 2016 Wiley Periodicals, Inc.

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References

Details

Published: Sep 20, 2016
Vol/Issue: 38(1)
Pages: 541-560
License: View

Authors

A

Andrew A. Nicholson

Department of Neuroscience Western University London Ontario Canada; Department of Psychiatry Western University London Ontario Canada; Department of Imaging Lawson Health Research Institute London Ontario Canada

D

Daniela Rabellino

Department of Psychiatry Western University London Ontario Canada; Department of Imaging Lawson Health Research Institute London Ontario Canada

M

Maria Densmore

Department of Imaging Lawson Health Research Institute London Ontario Canada

P

Paul A. Frewen

Department of Neuroscience Western University London Ontario Canada; Department of Psychology Western University London Ontario Canada

C

Christian Paret

Department of Neuroimaging Central Institute of Mental Health Mannheim, Medical, Faculty Mannheim/Heidelberg University Heidelberg Germany; Department of Psychosomatic Medicine and Psychotherapy Central Institute of Mental Health Mannheim, Medical Faculty Mannheim/Heidelberg University Heidelberg Germany

R

Rosemarie Kluetsch

Department of Psychosomatic Medicine and Psychotherapy Central Institute of Mental Health Mannheim, Medical Faculty Mannheim/Heidelberg University Heidelberg Germany

C

Christian Schmahl

Department of Psychosomatic Medicine and Psychotherapy Central Institute of Mental Health Mannheim, Medical Faculty Mannheim/Heidelberg University Heidelberg Germany

J

Jean Théberge

Department of Psychiatry Western University London Ontario Canada; Department of Imaging Lawson Health Research Institute London Ontario Canada; Department of Medical Imaging Western University London Ontario Canada; Department of Medial Biophysics, Western University London Ontario Canada; Department of Diagnostic Imaging St. Joseph's Healthcare London Ontario Canada

R

Richard W.J. Neufeld

Department of Neuroscience Western University London Ontario Canada; Department of Psychiatry Western University London Ontario Canada; Department of Psychology Western University London Ontario Canada

M

Margaret C. McKinnon

Mood Disorders Program and Clinical Neuropsychology Service St. Joseph's Healthcare Hamilton Ontario Canada; Department of Psychiatry and Behavioural Neuroscience McMaster University Hamilton Ontario Canada

J

Jeffrey P. Reiss

Department of Psychiatry Western University London Ontario Canada

R

Rakesh Jetly

Canadian Forces, Health Services Ottawa Ontario Canada

R

Ruth A. Lanius

Department of Neuroscience Western University London Ontario Canada; Department of Psychiatry Western University London Ontario Canada; Department of Imaging Lawson Health Research Institute London Ontario Canada

Funding

Canadian Institutes of Health Research

Cite This Article

Andrew A. Nicholson, Daniela Rabellino, Maria Densmore, et al. (2016). The neurobiology of emotion regulation in posttraumatic stress disorder: Amygdala downregulation via real‐time fMRI neurofeedback. Human Brain Mapping, 38(1), 541-560. https://doi.org/10.1002/hbm.23402

The neurobiology of emotion regulation in posttraumatic stress disorder: Amygdala downregulation via real‐time fMRI neurofeedback

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