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

Abstract

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.

Functional neuroimaging in Tourette syndrome: recent perspectives

“…Results are contradictory. Thomalla et al 22 found decreased activity in left primary motor cortex and secondary motor areas during go trials. Another study showed a reduced activation in the dorsal premotor cortex for the StopSuccess trial.…”

“…Another study showed a reduced activation in the dorsal premotor cortex for the StopSuccess trial. 21 The conflicting results might be caused by a difference in study design: in Ganos et al's study, 21 the procedure was adapted to ensure a fifty-fifty successful performance in the no-go trials in both patients and controls, whereas in Thomalla et al's study, 22 there were behavioral differences between patients and controls. The patients with TS were slower and and made more mistakes in no-go trials than the healthy controls.…”

“…21,22 Go/ no-go test is a test of behavioral control in which an appropriate reaction must be performed and an inappropriate reaction must be inhibited. Results are contradictory.…”

“…With regard to the fMRI studies, for example, one study has used resting state networks, 12 while another has used regional homogeneity. 19 The fMRI tasks themselves can have had different paradigms, 21,22 but also the same tasks can have been performed in different ways -eg, finger tapping with preferred or nonpreferred hand or imaginary finger …”

Without Blinking an Eye: Proactive Motor Control Enhancement

“…The majority of studies investigating impulsivity and selfcontrol in normal and clinical populations utilized the reactive inhibition paradigm's tasks and based on the results formulated conclusions as to the general inhibitory mechanisms (Barkley 1997;Corbetta and Shulman 2002;Lipszyc and Schachar 2010;Monsell 1996;Thomalla et al 2013). …”