Theta Activity Dynamics during Embedded Response Plan Processing in Tourette Syndrome

Abstract

Gilles de la Tourette syndrome (GTS) is a neuropsychiatric disorder. Because motor signs are the defining feature of GTS, addressing the neurophysiology of motor processes is central to understanding GTS. The integration of voluntary motor processes is subject to so-called “binding problems”, i.e., how different aspects of an action are integrated. This was conceptualized in the theory of event coding, in which ‘action files’ accomplish the integration of motor features. We examined the functional neuroanatomical architecture of EEG theta band activity related to action file processing in GTS patients and healthy controls. Whereas, in keeping with previous data, behavioral performance during action file processing did not differ between GTS and controls, underlying patterns of neural activity were profoundly different. Superior parietal regions (BA7) were predominantly engaged in healthy controls, but superior frontal regions (BA9, BA10) in GTS indicated that the processing of different motor feature codes was central for action file processing in healthy controls, whereas episodic processing was more relevant in GTS. The data suggests a cascade of cognitive branching in fronto-polar areas followed by episodic processing in superior frontal regions in GTS. Patients with GTS accomplish the integration of motor plans via qualitatively different neurophysiological processes.

Cognitive and Neural Mechanisms of Behavior Therapy for Tics: A Perception–Action Integration Approach

“…A few studies have already investigated the neurophysiological processes which change due to cognitive-behavioral therapy [ 49 , 53 ]. However, it has proven useful to consider GTS as a disorder of perception–action integration since there is ample evidence confirming the suitability of TEC and BRAC as a conceptual framework for GTS [ 19 , 54 , 55 , 57 ], resulting in new perspectives on the analysis of underlying mechanisms [ 4 ]. However, further investigations are needed to enhance the understanding of neurophysiological processes to enable the individualization of therapeutic approaches, i.e., the assignment of therapies according to predicted efficacy.…”

“…In light of recent findings, the Theory of Event Coding (TEC) and its derivative BRAC (Binding and Retrieval in Action Control) seem to be suitable for the investigation of neural and cognitive processes, especially in the context of tic disorders. Conceptualizing GTS and chronic tic disorders as disorders of perception–action integration opens up new possibilities for investigating and understanding the underlying neurophysiological processes [ 4 , 54 , 55 , 56 , 57 ].…”

Resting network architecture of theta oscillations reflects hyper-learning of sensorimotor information in Gilles de la Tourette syndrome

“…These include (i) behavioural evidence of enhanced learning of probabilistic stimulus–response information in GTS 8 , 13 , 14 , (ii) a biophysical perspective of why theta band activity should be considered in learning 19 , 35 , (iii) a clinical perspective of why theta band activity should be relevant in GTS 36 and (iv) specific results on theta activity’s role in statistical learning 21 , 37 , 38 and stimulus–response binding. 39 , 40 Importantly, it was assumed that superior learning performance is associated with a more optimal network architecture, 32 , 33 which resulted in the use of the small-world coefficient. Network architecture was assessed before, during and after the learning task (see the orange rectangles in the middle).…”

“…Regarding network dynamics, we focused on theta band activity for various reasons: First, high-amplitude, low-frequency oscillations, such as those in the theta band, are particularly suitable for large-scale information integration, 19 , 35 including establishing perception–action associations in HC 39 and GTS. 40 Second, connectivity changes in the theta band have been linked to statistical learning. 37 Third, theta band activity plays a crucial role in the pathophysiology of fronto-striatal networks in GTS, 36 also known to underlie statistical learning.…”

Unsigned surprise but not reward magnitude modulates the integration of motor elements during actions

“…Therefore, an overlap between a to-be-performed and a planned response impairs performance, which is reflected by increased reaction times (RTs) and higher error rates 1 , 2 , 7 , 8 , 20 . The degree of performance impairment depends on the strength of binding 2 , 20 – 22 . The employed experimental approach therefore uses an “ABBA design”, which requires that a planned response (A) is executed only after another response (B) is planned and performed immediately.…”