Impaired inhibition of prepotent motor actions in patients with Tourette syndrome

Impaired inhibition of prepotent motor actions in patients with Tourette syndrome

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J Psychiatry Neurosci 2013; 38(5): 349-356

Scott A. Wylie, PhD; Daniel O. Claassen, MD; Kristen E. Kanoff, BA; K. Richard Ridderinkhof, PhD; Wery P.M. van den Wildenberg, PhD

Wylie, Claassen, Kanoff — Department of Neurology, Vanderbilt University, Nashville, Tenn., USA; Ridderinkhof, van den Wildenberg — Psychology Department, University of Amsterdam, Amsterdam, the Netherlands

Abstract

Background: Evidence that tic behaviour in individuals with Tourette syndrome reflects difficulties inhibiting prepotent motor actions is mixed. Response conflict tasks produce sensitive measures of response interference from prepotent motor impulses and the proficiency of inhibiting these impulses as an act of cognitive control. We tested the hypothesis that individuals with Tourette syndrome show a deficit in inhibiting prepotent motor actions.

Methods: Healthy controls and older adolescents/adults with persistent Tourette syndrome without a history of obsessive–compulsive disorder or attention-deficit/hyperactivity disorder and presenting with stable mood functioning (i.e., no history of well-treated anxiety or depression) participated in this study. They performed a Simon task that induced conflict between prepotent actions and goal-directed actions. A novel theoretical framework distinguished group differences in acting impulsively (i.e., fast motor errors) from the proficiency of inhibiting interference by prepotent actions (i.e., slope of interference reduction).

Results: We included 27 controls and 28 individuals with Tourette syndrome in our study. Both groups showed similar susceptibility to making fast, impulsive motor errors (Tourette syndrome 26% v. control 23%; p = 0.10). The slope (m) reduction of the interference effect was significantly less pronounced among participants with Tourette syndrome than controls (Tourette syndrome: m = –0.07 v. control: m = –0.23; p = 0.022), consistent with deficient inhibitory control over prepotent actions in Tourette syndrome.

Limitations: This study does not address directly the role of psychiatric comorbidities and medication effects on inhibitory control over impulsive actions in individuals with Tourette syndrome.

Conclusion: The results offer empirical evidence for deficient inhibitory control over prepotent motor actions in individuals with persistent Tourette syndrome with minimal to absent psychiatric comorbidities. These findings also suggest that the frontal–basal ganglia circuits involved in suppressing unwanted motor actions may underlie deficient inhibitory control abilities in individuals with Tourette syndrome.


Submitted July 20, 2012; Revised Dec. 18, 2012, Mar. 5, 2013; Accepted Mar. 9, 2013.

Acknowledgements: This work was supported by a Tourette Syndrome Association (TSA) grant awarded to S.A. Wylie, W. van den Wildenberg and D.O. Claassen. We thank Bert van Beek for programming the computer task. We thank Laura Wegner for study coordination and Dr. Fred Wooten for assistance in participant recruitment.

Competing interests: None declared for K.E. Kanoff and K.R. Ridderinkhof. As above for S.A. Wylie, W.P.M. van den Wildenberg and D.O. Classen. S.A. Wylie also declares institutional grant support from the National Institute on Aging (National Institutes of Health). D.O. Classen also declares a speaker honorarium from Teva Pharmaceutical Industries.

Contributors: S.A. Wylie, D.O. Claassen, K.R. Ridderinkhof and W.P.M. van den Wildenberg designed the study and wrote the article. S.A. Wylie, D.O. Claassen and K.E. Kanoff acquired the data. All authors analyzed the data and approved the article’s publication. S.A. Wylie, K.E. Kanoff, K.R. Ridderinkhof and W.P.M. van den Wildenberg reviewed the article.

DOI: 10.1503/jpn.120138

Correspondence to: S.A. Wylie, Department of Neurology, Vanderbilt University Medical Center, 1161 21st Ave. S, A-0118 Medical Center North, Nashville TN 37232; scott.a.wylie@vanderbilt.edu