Resting network architecture of theta oscillations reflects hyper-learning of sensorimotor information in Gilles de la Tourette syndrome
Adam Takacs,
Eszter Toth-Faber,
Lina Schubert
et al.
Abstract:Gilles de la Tourette syndrome (GTS) is a neurodevelopmental disorder characterized by motor and vocal tics. GTS is associated with enhanced processing of stimulus-response (S-R) associations, including a higher propensity to learn probabilistic S-R contingencies (i.e., statistical learning), the nature of which is still elusive. In this study, we investigated the hypothesis that resting-state theta network organization is key for the understanding of superior statistical learning in these patients. We investi… Show more
“…Alternatively, clinical groups who show superior implicit learning (e.g. Takacs et al. 2024 ) may evidence lower levels of theta and/or alpha/beta synchronization compared to controls.…”
Implicit visuomotor sequence learning is crucial for acquiring skills that result in automated behaviors. The oscillatory dynamics underpinning this learning process are not well understood. To address this gap, the current study employed electroencephalography with a medium-density array (64 electrodes) to investigate oscillatory activity associated with implicit visuomotor sequence learning in the Serial Reaction Time task. In the task, participants unknowingly learn a series of finger movements. Eighty-five healthy adults participated in the study. Analyses revealed that theta activity at the vertex and alpha/beta activity over the motor areas decreased over the course of learning. No associations between alpha/beta and theta power were observed. These findings are interpreted within a dual-process framework: midline theta activity is posited to regulate top-down attentional processes, whereas beta activity from motor areas underlies the bottom-up encoding of sensory information from movement. From this model, we suggest that during implicit visuomotor sequence learning, top-down processes become disengaged (indicated by a reduction in theta activity), and modality specific bottom-up processes encode the motor sequence (indicated by a reduction in alpha/beta activity).
“…Alternatively, clinical groups who show superior implicit learning (e.g. Takacs et al. 2024 ) may evidence lower levels of theta and/or alpha/beta synchronization compared to controls.…”
Implicit visuomotor sequence learning is crucial for acquiring skills that result in automated behaviors. The oscillatory dynamics underpinning this learning process are not well understood. To address this gap, the current study employed electroencephalography with a medium-density array (64 electrodes) to investigate oscillatory activity associated with implicit visuomotor sequence learning in the Serial Reaction Time task. In the task, participants unknowingly learn a series of finger movements. Eighty-five healthy adults participated in the study. Analyses revealed that theta activity at the vertex and alpha/beta activity over the motor areas decreased over the course of learning. No associations between alpha/beta and theta power were observed. These findings are interpreted within a dual-process framework: midline theta activity is posited to regulate top-down attentional processes, whereas beta activity from motor areas underlies the bottom-up encoding of sensory information from movement. From this model, we suggest that during implicit visuomotor sequence learning, top-down processes become disengaged (indicated by a reduction in theta activity), and modality specific bottom-up processes encode the motor sequence (indicated by a reduction in alpha/beta activity).
Gilles de la Tourette syndrome (GTS) is a disorder characterised by motor and vocal tics, which may represent habitual actions as a result of enhanced learning of associations between stimuli and responses (S‐R). In this study, we investigated how adults with GTS and healthy controls (HC) learn two types of regularities in a sequence: statistics (non‐adjacent probabilities) and rules (predefined order). Participants completed a visuomotor sequence learning task while EEG was recorded. To understand the neurophysiological underpinnings of these regularities in GTS, multivariate pattern analyses on the temporally decomposed EEG signal as well as sLORETA source localisation method were conducted. We found that people with GTS showed superior statistical learning but comparable rule‐based learning compared to HC participants. Adults with GTS had different neural representations for both statistics and rules than HC adults; specifically, adults with GTS maintained the regularity representations longer and had more overlap between them than HCs. Moreover, over different time scales, distinct fronto‐parietal structures contribute to statistical learning in the GTS and HC groups. We propose that hyper‐learning in GTS is a consequence of the altered sensitivity to encode complex statistics, which might lead to habitual actions.
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