Stroke Recovery–Related Changes in Cortical Reactivity Based on Modulation of Intracortical Inhibition-Reference-Cited by-同舟云学术

Stroke Recovery–Related Changes in Cortical Reactivity Based on Modulation of Intracortical Inhibition

Published:2024-06 Issue:6 Volume:55 Page:1629-1640
ISSN:0039-2499
Container-title:Stroke
language:en
Short-container-title:Stroke

Author:

Harquel Sylvain¹²^ORCID,Cadic-Melchior Andéol¹²^ORCID,Morishita Takuya¹²^ORCID,Fleury Lisa¹²^ORCID,Witon Adrien¹²³,Ceroni Martino¹²^ORCID,Brügger Julia¹²^ORCID,Meyer Nathalie H.⁴^ORCID,Evangelista Giorgia G.¹²^ORCID,Egger Philip¹²^ORCID,Beanato Elena¹²^ORCID,Menoud Pauline¹²,Van de Ville Dimitri⁵⁶^ORCID,Micera Silvestro⁷⁸^ORCID,Blanke Olaf⁴⁹,Léger Bertrand¹⁰^ORCID,Adolphsen Jan¹¹^ORCID,Jagella Caroline¹²,Constantin Christophe¹³^ORCID,Alvarez Vincent¹³^ORCID,Vuadens Philippes¹⁰,Turlan Jean-Luc¹⁰^ORCID,Mühl Andreas¹⁰,Bonvin Christophe¹³^ORCID,Koch Philipp J.¹²¹⁴^ORCID,Wessel Maximilian J.¹²¹⁵,Hummel Friedhelm C.¹²¹⁶^ORCID

Affiliation:

1. Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École Polytechnique Fédérale de Lausanne (EPFL), Geneva, Switzerland (S.H., A.C.-M., T.M., L.F., A.W., M.C., J.B., G.G.E., P.E., E.B., P.M., P.J.K., M.J.W., F.C.H.).

2. Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Sion, Switzerland (S.H., A.C.-M., T.M., L.F., A.W., M.C., J.B., G.G.E., P.E., E.B., P.M., P.J.K., M.J.W., F.C.H.).

3. Health-IT, Centre de Service, Hôpital du Valais, Switzerland (A.W.).

4. Laboratory of Cognitive Neuroscience, INX and BMI, EPFL, Geneva, Switzerland (N.H.M., O.B.).

5. Medical Image Processing Laboratory, INX, EPFL, Geneva, Switzerland (D.V.V.).

6. Department of Radiology and Medical Informatics, University of Geneva (UNIGE), Switzerland (D.V.d.V.).

7. The Biorobotics Institute and Department of Excellence in Robotics and AI, Scuola Superiore Sant’Anna, Pisa, Italy (S.M.).

8. Bertarelli Foundation Chair in Translational Neuroengineering, INX and Institute of Bioengineering, School of Engineering, Ecole Polytechnique Fédérale de Lausanne (S.M.).

9. Department of Neurology, Geneva University Hospital (HUG), Switzerland (O.B.).

10. Clinique Romande de Réadaptation, Sion, Switzerland (B.L., P.V., J.-L.T., A.M.).

11. Mediclin Reha-Zentrum Plau am See, Germany (J.A.).

12. Berner Klinik Montana, Switzerland (C.J.).

13. Department of Neurology, Hôpital du Valais, Sion, Switzerland (C.C., V.A., C.B.).

14. Department of Neurology, University of Lübeck, Germany (P.J.K.).

15. Department of Neurology, Julius-Maximilians-University Würzburg, Germany (M.J.W.).

16. Clinical Neuroscience, Geneva University Hospital, Switzerland (F.C.H.).

Abstract

BACKGROUND: Cortical excitation/inhibition dynamics have been suggested as a key mechanism occurring after stroke. Their supportive or maladaptive role in the course of recovery is still not completely understood. Here, we used transcranial magnetic stimulation (TMS)-electroencephalography coupling to study cortical reactivity and intracortical GABAergic inhibition, as well as their relationship to residual motor function and recovery longitudinally in patients with stroke. METHODS: Electroencephalography responses evoked by TMS applied to the ipsilesional motor cortex were acquired in patients with stroke with upper limb motor deficit in the acute (1 week), early (3 weeks), and late subacute (3 months) stages. Readouts of cortical reactivity, intracortical inhibition, and complexity of the evoked dynamics were drawn from TMS-evoked potentials induced by single-pulse and paired-pulse TMS (short-interval intracortical inhibition). Residual motor function was quantified through a detailed motor evaluation. RESULTS: From 76 patients enrolled, 66 were included (68.2±13.2 years old, 18 females), with a Fugl-Meyer score of the upper extremity of 46.8±19. The comparison with TMS-evoked potentials of healthy older revealed that most affected patients exhibited larger and simpler brain reactivity patterns ( P cluster <0.05). Bayesian ANCOVA statistical evidence for a link between abnormally high motor cortical excitability and impairment level. A decrease in excitability in the following months was significantly correlated with better motor recovery in the whole cohort and the subgroup of recovering patients. Investigation of the intracortical GABAergic inhibitory system revealed the presence of beneficial disinhibition in the acute stage, followed by a normalization of inhibitory activity. This was supported by significant correlations between motor scores and the contrast of local mean field power and readouts of signal dynamics. CONCLUSIONS: The present results revealed an abnormal motor cortical reactivity in patients with stroke, which was driven by perturbations and longitudinal changes within the intracortical inhibition system. They support the view that disinhibition in the ipsilesional motor cortex during the first-week poststroke is beneficial and promotes neuronal plasticity and recovery.

Publisher

Ovid Technologies (Wolters Kluwer Health)

Reference50 articles.

1. Brain Excitability in Stroke

2. Excitotoxicity and stroke: Identifying novel targets for neuroprotection

3. Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke

4. Restoring brain function after stroke — bridging the gap between animals and humans

5. Encouraging an excitable brain state: mechanisms of brain repair in stroke