Increased perception-action binding in Tourette syndrome

• Published in: Brain (London, England : 1878) Vol. 143; no. 6; pp. 1934 - 1945
• Main Authors: Kleimaker, Maximilian, Takacs, Adam, Conte, Giulia, Onken, Rebecca, Verrel, Julius, Bäumer, Tobias, Münchau, Alexander, Beste, Christian
• Format: Journal Article
• Language: English
• Published: England 01.06.2020
• Subjects: Adult; Benzofurans; Electroencephalography - methods; Fatty Acids, Unsaturated; Female; Humans; Image Processing, Computer-Assisted; Male; Middle Aged; Motor Activity - physiology; Perception - physiology; Photic Stimulation - methods; Tics - physiopathology; Tourette Syndrome - metabolism; Tourette Syndrome - physiopathology; Visual Perception - physiology; Gilles de la Tourette syndrome; event-related potentials; Theory of Event Coding; perception-action binding; EEG
• ISSN: 0006-8950; 1460-2156; 1460-2156
• DOI: 10.1093/brain/awaa111

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.