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

• DOI: 10.1161/strokeaha.123.045174
• Publication Date: 2024-04-19T09:00:26Z
• Authors: Sylvain Harquel; Andéol Cadic-Melc...; Takuya Morishita; Lisa Fleury; Adrien Witon; Martino Ceroni; Julia Brügger; Nathalie H. Meyer; Giorgia G. Evange...; Philip Egger; Elena Beanato; Pauline Menoud; Dimitri Van de Ville; Silvestro Micera; Olaf Blanke; Bertrand Léger; Jan Adolphsen; Caroline Jagella; Christophe Consta...; Vincent Alvarez; Philippes Vuadens; Jean-Luc Turlan; Andreas Mühl; Christophe Bonvin; Philipp J. Koch; Maximilian J. Wessel; Friedhelm C. Hummel
• Keywords: Male; 0301 basic medicine; Upper extremity; Evoked potential; 610; Stroke / physiopathology; info:eu-repo/classification/ddc/616.0757; 03 medical and health sciences; Motor Cortex / physiopathology; transcranial magnetic stimulation; 616; Humans; Aged; Aged, 80 and over; [SCCO.NEUR]Cognitive science/Neuroscience; Cortical excitability; Electroencephalography; info:eu-repo/classification/ddc/616.8; Middle Aged; stroke; Neural Inhibition / physiology; Transcranial Magnetic Stimulation / methods; Electroencephalography EEG; Evoked Potentials, Motor / physiology; Motor cortex; Female; neurophysiology; Transcranial magnetic stimulation; Recovery of Function / physiology

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.