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

Article Article scientifique Article Stroke Recovery–Related Changes in Cortical Reactivity Based on Modulation of Intracortical Inhibition eng 2024-04-19 2024-06 author Harquel Sylvain 0000-0001-8756-2230 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.).,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.). author Cadic-Melchior Andéol 0000-0001-9899-299X 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.).,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.). author Morishita Takuya 0000-0003-0039-1825 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.).,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.). author Fleury Lisa 0000-0002-1277-7197 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.).,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.). author Witon Adrien 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.).,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.).,Health-IT, Centre de Service, Hôpital du Valais, Switzerland (A.W.). author Ceroni Martino 0000-0002-9470-1849 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.).,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.). 754893 author Bruegger Julia 0000-0002-4675-2502 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.).,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.). 841684 author Meyer Nathalie H 0000-0001-8969-7761 Laboratory of Cognitive Neuroscience, INX and BMI, EPFL, Geneva, Switzerland (N.H.M., O.B.). author Evangelista Giorgia G 0000-0002-8317-393X 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.).,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.). author Egger Philip 0000-0003-0823-3266 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.).,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.). author Beanato Elena 0000-0002-4451-1684 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.).,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.). author Menoud Pauline 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.).,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.). author Van De Ville Dimitri 0000-0002-2879-3861 Medical Image Processing Laboratory, INX, EPFL, Geneva, Switzerland (D.V.V.).,Department of Radiology and Medical Informatics, University of Geneva (UNIGE), Switzerland (D.V.d.V.). 638484 Département de radiologie et informatique médicale (RADIO) author Micera Silvestro 0000-0003-4396-8217 The Biorobotics Institute and Department of Excellence in Robotics and AI, Scuola Superiore Sant'Anna, Pisa, Italy (S.M.).,Bertarelli Foundation Chair in Translational Neuroengineering, INX and Institute of Bioengineering, School of Engineering, Ecole Polytechnique Fédérale de Lausanne (S.M.). author Blanke Olaf Laboratory of Cognitive Neuroscience, INX and BMI, EPFL, Geneva, Switzerland (N.H.M., O.B.).,Department of Neurology, Geneva University Hospital (HUG), Switzerland (O.B.). 107390 Département des neurosciences cliniques (OTONO) author Léger Bertrand 0000-0003-2782-1442 Clinique Romande de Réadaptation, Sion, Switzerland (B.L., P.V., J.-L.T., A.M.). author Adolphsen Jan 0000-0001-5702-1708 Mediclin Reha-Zentrum Plau am See, Germany (J.A.). author Jagella Caroline Berner Klinik Montana, Switzerland (C.J.). author Constantin Christophe 0000-0003-1849-2659 Department of Neurology, Hôpital du Valais, Sion, Switzerland (C.C., V.A., C.B.). author Alvarez Vincent 0000-0002-2489-4577 Department of Neurology, Hôpital du Valais, Sion, Switzerland (C.C., V.A., C.B.). author Vuadens Philippes Clinique Romande de Réadaptation, Sion, Switzerland (B.L., P.V., J.-L.T., A.M.). author Turlan Jean-Luc 0000-0003-0654-620X Clinique Romande de Réadaptation, Sion, Switzerland (B.L., P.V., J.-L.T., A.M.). author Mühl Andreas Clinique Romande de Réadaptation, Sion, Switzerland (B.L., P.V., J.-L.T., A.M.). author Bonvin Christophe 0000-0002-9058-8105 Department of Neurology, Hôpital du Valais, Sion, Switzerland (C.C., V.A., C.B.). author Koch Philipp J 0000-0002-8795-758X 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.).,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.).,Department of Neurology, University of Lübeck, Germany (P.J.K.). author Wessel Maximilian J 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.).,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.).,Department of Neurology, Julius-Maximilians-University Würzburg, Germany (M.J.W.). author Hummel Friedhelm 0000-0002-4746-4633 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.).,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.).,Clinical Neuroscience, Geneva University Hospital, Switzerland (F.C.H.). 868060 Département des neurosciences cliniques (OTONO) 1629-1640 10.1161/STROKEAHA.123.045174 38639087 0039-2499 https://www.ahajournals.org/doi/10.1161/STROKEAHA.123.045174 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. Cortical excitability Electroencephalography Evoked potential Motor cortex Transcranial magnetic stimulation Upper extremity Aged Aged, 80 and over Evoked Potentials, Motor / physiology Female Humans Male Middle Aged Motor Cortex / physiopathology Neural Inhibition / physiology Recovery of Function / physiology Stroke / physiopathology Transcranial Magnetic Stimulation / methods Dewey 616.8 Dewey 616.0757 Swiss National Science Foundation Novel, individualized Brain Stimulation, network-based approaches to improve Cognition in healthy seniors and patients with MCI (NiBS-iCog) 197899 CH Projects 62 Département de radiologie et informatique médicale 227 61 Département des neurosciences cliniques 226 false 552 Traitement d'images médicales 893 Stroke 55 6 4ffb8a30-4c62-4118-80bf-171570739c74 Article (Published version) Restricted harquel-et-al-2024-stroke-recovery-.pdf 6931526 application/pdf 6d43b4af072414c00b958eda7aeab936aa879c9e8f2cbaab8497e50b9a4ab6fa 1b9140d4-9914-4c33-8572-e895f52296b1 Appendix Public strokeaha.123.045174.fig06.jpg 179713 image/jpeg Graphical abstract 8d3a6032845f1df3d8657e2fc567d976d13126089c04d61f2f42f150f5233d98 6a1fcd51-6e20-4295-9783-02df19f4dc00 Appendix Restricted str_stroke-2023-045174_supp1.pdf 649129 application/pdf Supplementary material 1 55aa759f882060915bff506284b620d4b5f1c4451072cfe1bb5798dca3ced946 5522bff8-dbaa-4ce1-ac68-66de2e8eaee8 Appendix Restricted str_stroke-2023-045174_supp2.pdf 122168 application/pdf Supplementary material 2 45ce314968e95071049398fc747e965ec9cf0e10e3c5cc13f44bc2b3b28246cd Vignette Public strokeaha.123.045174.fig06.jpg 93243 image/png restrictedAccess Faculté de médecine / Section de médecine clinique / Département de radiologie et informatique médicale Faculté de médecine / Section de médecine clinique / Département des neurosciences cliniques

Title	Published in	Year	Views	Downloads

Stroke Recovery–Related Changes in Cortical Reactivity Based on Modulation of Intracortical Inhibition	Stroke	2024	70	0
Toward individualized medicine in stroke — The TiMeS project: Protocol of longitudinal, multi-modal, multi-domain study in stroke	Frontiers in neurology	2022	101	247

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