Local Neuronal Sleep after Stroke: The role of cortical bistability in brain reorganization.

TMS-EEG neuromodulation neurorehabilitation plasticity sleep-like off-period slow waves stroke lesion

Journal

Brain stimulation
ISSN: 1876-4754
Titre abrégé: Brain Stimul
Pays: United States
ID NLM: 101465726

Informations de publication

Date de publication:
15 Jul 2024
Historique:
received: 07 10 2023
revised: 30 06 2024
accepted: 12 07 2024
medline: 18 7 2024
pubmed: 18 7 2024
entrez: 17 7 2024
Statut: aheadofprint

Résumé

Acute cerebral ischemia triggers a number of cellular mechanisms not only leading to excitotoxic cell death but also to enhanced neuroplasticity, facilitating neuronal reorganization and functional recovery. Transferring these cellular mechanisms to neurophysiological correlates adaptable to patients is crucial to promote recovery post-stroke. The combination of TMS and EEG constitutes a promising readout of neuronal network activity in stroke patients. We used the combination of TMS and EEG to investigate the development of local signal processing and global network alterations in 40 stroke patients with motor deficits alongside neural reorganization from the acute to the chronic phase. We show that the TMS-EEG response reflects information about reorganization and signal alterations associated with persistent motor deficits throughout the entire post-stroke period. In the early post-stroke phase and in a subgroup of patients with severe motor deficits, TMS applied to the lesioned motor cortex evoked a sleep-like slow wave response associated with a cortical off-period, a manifestation of cortical bistability, as well as a rapid disruption of the TMS-induced formation of causal network effects. Mechanistically, these phenomena were linked to lesions affecting ascending activating brainstem fibers. Of note, slow waves invariably vanished in the chronic phase, but were highly indicative of a poor functional outcome. In summary, we found evidence that transient effects of sleep-like slow waves and cortical bistability within ipsilesional M1 resulting in excessive inhibition may interfere with functional reorganization, leading to a less favorable functional outcome post-stroke, pointing to a new therapeutic target to improve recovery of function.

Sections du résumé

BACKGROUND BACKGROUND
Acute cerebral ischemia triggers a number of cellular mechanisms not only leading to excitotoxic cell death but also to enhanced neuroplasticity, facilitating neuronal reorganization and functional recovery.
OBJECTIVE OBJECTIVE
Transferring these cellular mechanisms to neurophysiological correlates adaptable to patients is crucial to promote recovery post-stroke. The combination of TMS and EEG constitutes a promising readout of neuronal network activity in stroke patients.
METHODS METHODS
We used the combination of TMS and EEG to investigate the development of local signal processing and global network alterations in 40 stroke patients with motor deficits alongside neural reorganization from the acute to the chronic phase.
RESULTS RESULTS
We show that the TMS-EEG response reflects information about reorganization and signal alterations associated with persistent motor deficits throughout the entire post-stroke period. In the early post-stroke phase and in a subgroup of patients with severe motor deficits, TMS applied to the lesioned motor cortex evoked a sleep-like slow wave response associated with a cortical off-period, a manifestation of cortical bistability, as well as a rapid disruption of the TMS-induced formation of causal network effects. Mechanistically, these phenomena were linked to lesions affecting ascending activating brainstem fibers. Of note, slow waves invariably vanished in the chronic phase, but were highly indicative of a poor functional outcome.
CONCLUSION CONCLUSIONS
In summary, we found evidence that transient effects of sleep-like slow waves and cortical bistability within ipsilesional M1 resulting in excessive inhibition may interfere with functional reorganization, leading to a less favorable functional outcome post-stroke, pointing to a new therapeutic target to improve recovery of function.

Identifiants

DOI: 10.1016/j.brs.2024.07.008 PMID: 39019396
pubmed: 39019396
pii: S1935-861X(24)00123-2
doi: 10.1016/j.brs.2024.07.008
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024. Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of Competing Interest ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

Auteurs

Caroline Tscherpel (C)

Department of Neurology, University Hospital Frankfurt, Goethe University, Frankfurt am Main, Germany; Medical Faculty, University of Cologne, and Department of Neurology, University Hospital Cologne, Cologne, Germany; Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Research Centre Jülich, jülich, Germany.

Maike Mustin (M)

Medical Faculty, University of Cologne, and Department of Neurology, University Hospital Cologne, Cologne, Germany.

Marcello Massimini (M)

Department of Biomedical and Clinical Science 'L. Sacco', University Milan, Milan, Italy; IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, Italy.

Theresa Paul (T)

Medical Faculty, University of Cologne, and Department of Neurology, University Hospital Cologne, Cologne, Germany.

Ulf Ziemann (U)

Department of Neurology & Stroke and Hertie Institute for Clinical Brain Research, Eberhard-Karls-University Tübingen, Tübingen, Germany.

Gereon R Fink (GR)

Medical Faculty, University of Cologne, and Department of Neurology, University Hospital Cologne, Cologne, Germany; Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Research Centre Jülich, jülich, Germany.

Christian Grefkes (C)

Department of Neurology, University Hospital Frankfurt, Goethe University, Frankfurt am Main, Germany; Medical Faculty, University of Cologne, and Department of Neurology, University Hospital Cologne, Cologne, Germany; Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Research Centre Jülich, jülich, Germany. Electronic address: christian.grefkes-hermann@kgu.de.

Classifications MeSH