Error Processing and Inhibitory Control in Obsessive-Compulsive Disorder: A Meta-analysis Using Statistical Parametric Maps

Luke J Norman; Stephan F Taylor; Yanni Liu; Joaquim Radua; Yann Chye; Stella J De Wit; Chaim Huyser; F Isik Karahanoglu; Tracy Luks; Dara Manoach; Carol Mathews; Katya Rubia; Chao Suo; Odile A van den Heuvel; Murat Yücel; Kate Fitzgerald

doi:10.1016/j.biopsych.2018.11.010

Error Processing and Inhibitory Control in Obsessive-Compulsive Disorder: A Meta-analysis Using Statistical Parametric Maps

Biol Psychiatry. 2019 May 1;85(9):713-725. doi: 10.1016/j.biopsych.2018.11.010. Epub 2018 Nov 29.

Authors

Luke J Norman¹, Stephan F Taylor², Yanni Liu², Joaquim Radua³, Yann Chye⁴, Stella J De Wit⁵, Chaim Huyser⁶, F Isik Karahanoglu⁷, Tracy Luks⁸, Dara Manoach⁹, Carol Mathews¹⁰, Katya Rubia¹¹, Chao Suo⁴, Odile A van den Heuvel¹², Murat Yücel¹³, Kate Fitzgerald²

Affiliations

¹ Department of Psychiatry, Michigan Medicine, University of Michigan, Ann Arbor, Michigan; Department of Child and Adolescent Psychiatry, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK. Electronic address: [email protected].
² Department of Psychiatry, Michigan Medicine, University of Michigan, Ann Arbor, Michigan.
³ Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK; Institut d'Investigacions Biomèdiques August Pi i Sunyer, Mental Health Research Networking Center, Barcelona, Spain; Centre for Psychiatric Research and Education, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.
⁴ Brain and Mental Health Research Hub, Monash Institute of Cognitive and Clinical Neurosciences, School of Psychological Sciences, Monash University, Melbourne, Australia.
⁵ Amsterdam Neuroscience, Amsterdam University Medical Centers, Department of Psychiatry, Amsterdam, The Netherlands; Department of Anatomy & Neurosciences, Vrije Universiteit, GGZ inGeest Specialized Mental Health Care, Amsterdam, The Netherlands.
⁶ Bascule, Academic Centre for Children and Adolescent Psychiatry, Amsterdam, The Netherlands.
⁷ Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.
⁸ Department of Radiology and Biomedical Imaging, University of California, San Francisco, San Francisco, California.
⁹ Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts; Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, Massachusetts.
¹⁰ Department of Psychiatry and Center for OCD, Anxiety and Related Disorders, University of Florida, Gainesville, Florida.
¹¹ Department of Child and Adolescent Psychiatry, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹² Amsterdam Neuroscience, Amsterdam University Medical Centers, Department of Psychiatry, Amsterdam, The Netherlands; OCD Team, Haukeland University Hospital, Bergen, Norway.
¹³ Brain and Mental Health Research Hub, Monash Institute of Cognitive and Clinical Neurosciences, School of Psychological Sciences, Monash University, Melbourne, Australia; Melbourne Neuropsychiatry Centre, Department of Psychiatry, University of Melbourne, Melbourne, Australia.

Abstract

Background: Error processing and inhibitory control enable the adjustment of behaviors to meet task demands. Functional magnetic resonance imaging studies report brain activation abnormalities in patients with obsessive-compulsive disorder (OCD) during both processes. However, conclusions are limited by inconsistencies in the literature and small sample sizes. Therefore, the aim here was to perform a meta-analysis of the existing literature using unthresholded statistical maps from previous studies.

Methods: A voxelwise seed-based d mapping meta-analysis was performed using t-maps from studies comparing patients with OCD and healthy control subjects (HCs) during error processing and inhibitory control. For the error processing analysis, 239 patients with OCD (120 male; 79 medicated) and 229 HCs (129 male) were included, while the inhibitory control analysis included 245 patients with OCD (120 male; 91 medicated) and 239 HCs (135 male).

Results: Patients with OCD, relative to HCs, showed longer inhibitory control reaction time (standardized mean difference = 0.20, p = .03, 95% confidence interval = 0.016, 0.393) and more inhibitory control errors (standardized mean difference = 0.22, p = .02, 95% confidence interval = 0.039, 0.399). In the brain, patients showed hyperactivation in the bilateral dorsal anterior cingulate cortex, supplementary motor area, and pre-supplementary motor area as well as right anterior insula/frontal operculum and anterior lateral prefrontal cortex during error processing but showed hypoactivation during inhibitory control in the rostral and ventral anterior cingulate cortices and bilateral thalamus/caudate, as well as the right anterior insula/frontal operculum, supramarginal gyrus, and medial orbitofrontal cortex (all seed-based d mapping z value >2, p < .001).

Conclusions: A hyperactive error processing mechanism in conjunction with impairments in implementing inhibitory control may underlie deficits in stopping unwanted compulsive behaviors in the disorder.

Keywords: Error processing; Inhibitory control; Meta-analysis; OCD; Performance monitoring; fMRI.

Publication types

Meta-Analysis
Research Support, N.I.H., Extramural

MeSH terms

Adolescent
Adult
Brain / physiopathology*
Brain Mapping
Female
Humans
Inhibition, Psychological*
Magnetic Resonance Imaging
Male
Neural Pathways / physiopathology
Obsessive-Compulsive Disorder / physiopathology*
Obsessive-Compulsive Disorder / psychology*
Young Adult

Grants and funding

R01 MH102242/MH/NIMH NIH HHS/United States