Inhibitory control in children with tic disorder: aberrant fronto-parietal network activity and connectivity

Abstract

Chronic tic disorders, including Tourette syndrome, are typically thought to have deficits in cognitive inhibition and top down cognitive control due to the frequent and repetitive occurrence of tics, yet studies reporting task performance results have been equivocal. Despite similar behavioural performance, individuals with chronic tic disorder have exhibited aberrant patterns of neural activation in multiple frontal and parietal regions relative to healthy controls during inhibitory control paradigms. In addition to these top down attentional control regions, widespread alterations in brain activity across multiple neural networks have been reported. There is a dearth, however, of studies examining event-related connectivity during cognitive inhibitory paradigms among affected individuals. The goal of this study was to characterize neural oscillatory activity and effective connectivity, using a case–control design, among children with and without chronic tic disorder during performance of a cognitive inhibition task. Electroencephalogram data were recorded in a cohort of children aged 8–12 years old (60 with chronic tic disorder, 35 typically developing controls) while they performed a flanker task. While task accuracy did not differ by diagnosis, children with chronic tic disorder displayed significant cortical source-level, event-related spectral power differences during incongruent flanker trials, which required inhibitory control. Specifically, attenuated broad band oscillatory power modulation within the anterior cingulate cortex was observed relative to controls. Whole brain effective connectivity analyses indicated that children with chronic tic disorder exhibit greater information flow between the anterior cingulate and other fronto-parietal network hubs (midcingulate cortex and precuneus) relative to controls, who instead showed stronger connectivity between central and posterior nodes. Spectral power within the anterior cingulate was not significantly correlated with any connectivity edges, suggesting lower power and higher connectivity are independent (versus resultant) neural mechanisms. Significant correlations between clinical features, task performance and anterior cingulate spectral power and connectivity suggest this region is associated with tic impairment (r = −0.31, P = 0.03) and flanker task incongruent trial accuracy (r’s = −0.27 to −0.42, P’s = 0.0008–0.04). Attenuated activation of the anterior cingulate along with dysregulated information flow between and among nodes within the fronto-parietal attention network may be neural adaptations that result from frequent engagement of neural pathways needed for inhibitory control in chronic tic disorder.