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Costs of control: decreased motor cortex engagement during a Go/NoGo task in Tourette’s syndrome

Götz Thomalla, Melanie Jonas, Tobias Bäumer, Hartwig R. Siebner, Katja Biermann-Ruben, Christos Ganos, Michael Orth, Friedhelm C. Hummel, Christian Gerloff, Kirsten Müller-Vahl, Alfons Schnitzler, Alexander Münchau
DOI: http://dx.doi.org/10.1093/brain/awt288 122-136 First published online: 31 October 2013

Summary

Gilles de la Tourette syndrome is a neuropsychiatric disorder characterized by an impaired ability to inhibit unwanted behaviour. Although the presence of chronic motor and vocal tics defines Tourette’s syndrome, other distinctive behavioural features like echo- and coprophenomena, and non-obscene socially inappropriate behaviour are also core features. We investigated neuronal activation during stimulus-driven execution and inhibition of prepared movements in Tourette’s syndrome. To this end, we performed event-related functional magnetic resonance imaging and structural diffusion tensor imaging in 15 moderately affected uncomplicated patients with ‘pure’ Tourette’s syndrome and 15 healthy control participants matched for age and gender. Subjects underwent functional magnetic resonance imaging during a Go/NoGo reaction time task. They had to withhold a prepared finger movement for a variable time until a stimulus instructed them to either execute (Go) or inhibit it (NoGo). Tics were monitored throughout the experiments, combining surface electromyogram, video recording, and clinical assessment in the scanner. Patients with Tourette’s syndrome had longer reaction times than healthy controls in Go trials and made more errors in total. Their functional brain activation was decreased in left primary motor cortex and secondary motor areas during movement execution (Go trials) but not during response inhibition (NoGo trials) compared with healthy control subjects. Volume of interest analysis demonstrated less task-related activation in patients with Tourette’s syndrome in primary and secondary motor cortex bilaterally, but not in the basal ganglia and cortical non-motor areas. They showed reduced co-activation between the left primary sensory-motor hand area and a network of contralateral sensory-motor areas and ipsilateral cerebellar regions. There were no between-group differences in structural connectivity of the left primary sensory-motor cortex as measured by diffusion tensor imaging-based probabilistic tractography. Our results link reduced sensory-motor cortical activation during movement execution to a decreased co-activation between the sensory-motor cortex and other brain areas involved in motor processing. These functional changes in patients with Tourette’s syndrome might result from adaptive reorganization in fronto-parietal brain networks engaged in motor and behavioural control, possibly triggered by abnormal processing and presumably overactivity in cortico-striato-cortical circuits. This might enable patients with Tourette’s syndrome to better suppress unwanted movements but comes at a price of behavioural deficits in other domains.

  • Gilles de la Tourette’s syndrome
  • tics
  • functional magnetic resonance imaging
  • Go/NoGo
  • Abbreviations
    BOLD
    blood oxygen level-dependent
    M1
    primary motor cortex
    SMA
    supplementary motor area
    YGTSS
    Yale Global Tic Severity Scale
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