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; Zsanett Tárnok; Foroogh Ghorbani; Madita Trelenberg; Dezso Nemeth; Alexander Münchau; Christian Beste

doi:10.1093/braincomms/fcae092

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

Brain Commun. 2024 Mar 14;6(2):fcae092. doi: 10.1093/braincomms/fcae092. eCollection 2024.

Authors

Adam Takacs^{1

2}, Eszter Toth-Faber^{3

4}, Lina Schubert⁵, Zsanett Tárnok⁶, Foroogh Ghorbani^{1

2}, Madita Trelenberg¹, Dezso Nemeth^{7

8

9}, Alexander Münchau⁵, Christian Beste^{1

2}

Affiliations

¹ Cognitive Neurophysiology, Department of Child and Adolescent Psychiatry, Faculty of Medicine, TU Dresden, Dresden 01069, Germany.
² Faculty of Medicine, University Neuropsychology Center, TU Dresden, Dresden 01069, Germany.
³ Institute of Psychology, ELTE Eötvös Loránd University, Budapest 1064, Hungary.
⁴ Brain, Memory and Language Research Group, Institute of Cognitive Neuroscience and Psychology, HUN-REN Research Centre for Natural Sciences, Budapest 1117, Hungary.
⁵ Institute of Systems Motor Science, University of Lübeck, Lübeck 23562, Germany.
⁶ Vadaskert Child and Adolescent Psychiatry Hospital and Outpatient Clinic, Budapest 1021, Hungary.
⁷ INSERM, Université Claude Bernard Lyon 1, CNRS, Centre de Recherche en Neurosciences de Lyon CRNL U1028 UMR5292, Bron 69500, France.
⁸ NAP Research Group, Institute of Psychology, Eötvös Loránd University & Institute of Cognitive Neuroscience and Psychology, HUN-REN Research Centre for Natural Sciences, Budapest 1071, Hungary.
⁹ Department of Education and Psychology, Faculty of Social Sciences, University of Atlántico Medio, Las Palmas de Gran Canaria 35017, Spain.

Abstract

Gilles de la Tourette syndrome is a neurodevelopmental disorder characterized by motor and vocal tics. It is associated with enhanced processing of stimulus-response associations, including a higher propensity to learn probabilistic stimulus-response 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 a key for the understanding of superior statistical learning in these patients. We investigated the graph-theoretical network architecture of theta oscillations in adult patients with Gilles de la Tourette syndrome and healthy controls during a statistical learning task and in resting states both before and after learning. We found that patients with Gilles de la Tourette syndrome showed a higher statistical learning score than healthy controls, as well as a more optimal (small-world-like) theta network before the task. Thus, patients with Gilles de la Tourette syndrome had a superior facility to integrate and evaluate novel information as a trait-like characteristic. Additionally, the theta network architecture in Gilles de la Tourette syndrome adapted more to the statistical information during the task than in HC. We suggest that hyper-learning in patients with Gilles de la Tourette syndrome is likely a consequence of increased sensitivity to perceive and integrate sensorimotor information leveraged through theta oscillation-based resting-state dynamics. The study delineates the neural basis of a higher propensity in patients with Gilles de la Tourette syndrome to pick up statistical contingencies in their environment. Moreover, the study emphasizes pathophysiologically endowed abilities in patients with Gilles de la Tourette syndrome, which are often not taken into account in the perception of this common disorder but could play an important role in destigmatization.

Keywords: Gilles de la Tourette syndrome; connectivity; resting state; statistical learning; theta.