The neural networks of inhibitory control in posttraumatic stress disorder

The neural networks of inhibitory control in posttraumatic stress disorder

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J Psychiatry Neurosci 2008;33(5):413–22

Erin Falconer, MSc; Richard Bryant, PhD; Kim L. Felmingham, PhD; Andrew H. Kemp, PhD; Evian Gordon, PhD; Anthony Peduto, MD; Gloria Olivieri, AssDip (MedRad); Leanne M. Williams, PhD

Falconer, Bryant, Felmingham, Kemp, Peduto, Olivieri, Williams — Brain Dynamics Centre, Westmead Millenium Institute, Westmead Hospital, Westmead; Falconer, Bryant, Kemp — School of Psychology, University of New South Wales; Felmingham, Williams — School of Psychology, University of Sydney, Sydney; Gordon — The Brain Resource International Database, Brain Resource Company, Ultimo; Peduto, Olivieri — Department of Radiology, Westmead Hospital, Sydney; Williams — Psychological Medicine, Western Clinical School, University of Sydney, Sydney, Australia

Abstract

Objective: Posttraumatic stress disorder (PTSD) involves deficits in information processing that may reflect hypervigilence and deficient inhibitory control. To date, however, no PTSD neuroimaging study has directly examined PTSD-related changes in executive inhibition. Our objective was to investigate the hypothesis that executive inhibitory control networks are compromised in PTSD.

Methods: Functional magnetic resonance imaging (fMRI) was used during a Go/No-Go inhibition task completed by a sample of patients with PTSD (n = 23), a matched sample of healthy (i.e. without trauma exposure) control participants (n = 23) and a sample of control participants with trauma exposure who did not meet criteria for PTSD (n = 17).

Results: Participants with PTSD showed more inhibition-related errors than did individuals without trauma exposure. During inhibition, control participants activated a right-lateralized cortical inhibitory network, whereas patients with PTSD activated only the left lateral frontal cortex. PTSD was associated with a reduction in right cortical activation and increased activation of striatal and somatosensory regions.

Conclusion: The increased inhibitory error and reduced right frontal cortical activation are consistent with compromised inhibitory control in PTSD, while the increased activation of brain regions associated with sensory processing and a greater demand on inhibitory control may reflect enhanced stimulus processing in PTSD, which may undermine cortical control mechanisms.

Résumé

Objectif : Le syndrome de stress post-traumatique (SSPT) met en cause des déficits du traitement de l’information qui peuvent traduire une hypervigilance et un déficit du contrôle inhibiteur. Jusqu’à maintenant, toutefois, aucune étude de neuro-imagerie portant sur le SSPT n’a examiné directement les changements de l’inhibition de l’exécution reliés au SSPT. Notre objectif consistait à étudier l’hypothèse selon laquelle les réseaux de contrôle inhibiteur de l’exécution sont affaiblis dans les cas de SSPT.

Méthodes : On a utilisé l’imagerie par résonance magnétique fonctionnelle (IMRf) au cours d’une tâche d’inhibition oui/non exécutée par un échantillon de patients atteints de SSPT (n = 23), un échantillon jumelé de participants témoins (n = 23) en bonne santé (c.-à-d. sans exposition à un traumatisme) et un échantillon de participants témoins exposés à un traumatisme mais ne satisfaisant aux critères du SSPT (n = 17).

Résultats : Les participants atteints de SSPT ont commis plus d’erreurs reliées à l’inhibition que les individus sans exposition à un traumatisme. Au cours de l’inhibition, les participants témoins ont activé un réseau inhibiteur cortical latéralisé à droite tandis que les patients atteints de SSPT ont activé seulement le cortex frontal latéral gauche. Le SSPT était associé à une réduction de l’activation du cortex droit et une augmentation de l’activation des aires striées et somatosensorielles.

Conclusion : L’erreur accrue de l’inhibition et la réduction de l’activité du cortex frontal droit concordent avec le contrôle affaibli de l’inhibition dans les cas de SSPT, tandis que l’activation accrue des aires cérébrales associées au traitement sensoriel et une plus grande demande imposée au contrôle inhibiteur peuvent refléter le traitement accru des stimulis dans les cas de SSPT, ce qui peut miner les mécanismes de contrôle cortical.


Medical subject headings: inhibition; stress disorders, posttraumatic; motor activity; neurophysiology.

Competing interests: None declared for Drs. Bryant, Felmingham, Peduto and Ms. Olivieri. Ms. Falconer has been employed part-time by the Brain Resource Company Ltd. to conduct work unrelated to the study. Dr. Kemp is currently employed by the Brain Resource Company Ltd. in work unrelated to this study. Dr. Gordon is CEO of the Brain Resource Company Ltd. Dr. Williams owns stock in the Brain Resource Company Ltd. and has received paid contract work from them unrelated to the study.

Submitted Apr. 12, 2007; Revised Sep. 22, Nov. 15, 2007; Accepted Nov. 15, 2007

Contributors: Ms. Falconer and Drs. Bryant, Gordon and Williams designed the study. Ms. Olivieri and Dr. Perduto acquired the data, which Ms. Falconer and Drs. Bryant, Felmingham, Kemp and Williams analyzed. Ms. Falconer and Drs. Williams, Bryant and Felmingham wrote the article, which Mses. Falconer and Olivieri and Drs. Bryant, Felmingham, Kemp, Gordon, Peduto and Williams reviewed. All authors gave final approval for publication.

Acknowledgements: This study was funded by an Australian Research Council Linkage Grant (LP0212045) and a National Health and Medical Research Council (NHMRC) program grant (300304). We would like to acknowledge the contribution of the Brain Resource International Database (BRID). L.M.W. is a small equity holder and E.G. holds significant equity and stock options in the Brain Resource Company Ltd. We acknowledge the support of the Brain Resource International Database (under the auspices of the Brain Resource Company) in data acquisition and methodology.

Correspondence to: Ms. E. Falconer, Brain Dynamics Centre, Westmead Hospital, Westmead, NSW 2145, Australia; fax 61-2-96357734; efalconer@psy.unsw.edu.au