Increased perception-action binding in Tourette syndrome

Abstract

Gilles de la Tourette syndrome is a multifaceted neurodevelopmental disorder characterized by multiple motor and vocal tics. Research in Tourette syndrome has traditionally focused on the motor system. However, there is increasing evidence that perceptual and cognitive processes play a crucial role as well. Against this background it has been reasoned that processes linking perception and action might be particularly affected in these patients with the strength of perception-action binding being increased. However, this has not yet been studied experimentally. Here, we investigated adult Tourette patients within the framework of the ‘Theory of Event Coding’ using an experimental approach allowing us to directly test the strength of perception-action binding. We included 24 adult patients with Tourette syndrome and n = 24 healthy control subjects using a previously established visual-motor event file task with four levels of feature overlap requiring repeating or alternating responses. Concomitant to behavioural testing, EEG was recorded and analysed using temporal signal decomposition and source localization methods. On a behavioural level, perception-action binding was increased in Tourette patients. Tic frequency correlated with performance in conditions where unbinding processes of previously established perception-action bindings were required with higher tic frequency being associated with stronger perception-action binding. This suggests that perception-action binding is intimately related to the occurrence of tics. Analysis of EEG data showed that behavioural changes cannot be explained based on simple perceptual or motor processes. Instead, cognitive processes linking perception to action in inferior parietal cortices are crucial. Our findings suggest that motor or sensory processes alone are less relevant for the understanding of Tourette syndrome than cognitive processes engaged in linking and restructuring of perception-action association. A broader cognitive framework encompassing perception and action appears well suited to opening new routes for the understanding of Tourette syndrome.

Non-invasive Brain Stimulation for the Treatment of Gilles de la Tourette Syndrome

“…This study yielded robust evidence for stronger perception-action bindings in these patients (13). Brain electromagnetic topography showed these effects to originate from BA 40 (13). In line with this, Petruo et al (12) carried out an unimodal vs. bimodal visual/acoustic Go/NoGo paradigm in adolescents with GTS.…”

“…In this study, a previously established visuomotor task was used (155), allowing to test the strength of perception-action bindings directly. This study yielded robust evidence for stronger perception-action bindings in these patients (13). Brain electromagnetic topography showed these effects to originate from BA 40 (13).…”

“…The pathophysiology of GTS, particularly the nature of tics, is still incompletely understood and a matter of debate ( 11 – 13 ). However, there is increasing evidence that structural and functional abnormalities in the basal ganglia, e.g., a volume reduction of the striatum ( 14 , 15 ), in cortico-striato-thalamo-cortical circuits ( 16 , 17 ), and in some cortical areas including medial frontal regions and the prefrontal cortex ( 15 , 18 ) as well as hyperactivity of the dopamine system ( 19 – 21 ) are key findings.…”

“…Recent findings derived from behavioral experiments comprising visuomotor stimulus-response tasks confirmed alterations of central processing of perceptions and actions in GTS. Against the background of clinical findings suggesting a strong interaction between motor (i.e., tics) and perceptional (e.g., premonitory urges) processes ( 88 ), Kleimaker et al ( 13 ) examined perception-action processes in the context of the Theory of Event Coding (TEC) ( 154 ). Presenting a general framework for the cognitive basis of perception and action paying particular attention to their dependency, TEC considers sensory stimuli and motor actions to be bound and stored together in so-called “event files” ( 154 ).…”

Electro-Myo-Stimulation Induced Tic Exacerbation – Increased Tendencies for the Formation of Perception-Action Links in Tourette Syndrome

“…If behaviorally irrelevant stimuli (low current) readily trigger or exacerbate tics, then this also implies that in GTS, there is high readiness of the motor system to respond to any sensory stimulus. That perception-action binding might indeed be stronger in GTS has been proposed [5] and also shown experimentally [8]. This case suggests that in addition to tighter binding between previously established perception-action links, there is also a higher likelihood of the formation of automatic perception-action links, the neural basis of which warrants further neurophysiological studies.…”