Differential Impact of Brain Network Efficiency on Poststroke Motor and Attentional Deficits.

Humans Brain / diagnostic imaging Diffusion Magnetic Resonance Imaging / methods Stroke / complications Cognitive Dysfunction / pathology Cognition Connectome / methods Magnetic Resonance Imaging
attention connectivity motor stroke structural MRI

Journal

Stroke
ISSN: 1524-4628
Titre abrégé: Stroke
Pays: United States
ID NLM: 0235266

Informations de publication

Date de publication:
04 2023
Historique:
medline: 29 3 2023
pubmed: 28 2 2023
entrez: 27 2 2023
Statut: ppublish

Résumé

Most studies on stroke have been designed to examine one deficit in isolation; yet, survivors often have multiple deficits in different domains. While the mechanisms underlying multiple-domain deficits remain poorly understood, network-theoretical methods may open new avenues of understanding. Fifty subacute stroke patients (7±3days poststroke) underwent diffusion-weighted magnetic resonance imaging and a battery of clinical tests of motor and cognitive functions. We defined indices of impairment in strength, dexterity, and attention. We also computed imaging-based probabilistic tractography and whole-brain connectomes. To efficiently integrate inputs from different sources, brain networks rely on a rich-club of a few hub nodes. Lesions harm efficiency, particularly when they target the rich-club. Overlaying individual lesion masks onto the tractograms enabled us to split the connectomes into their affected and unaffected parts and associate them to impairment. We computed efficiency of the unaffected connectome and found it was more strongly correlated to impairment in strength, dexterity, and attention than efficiency of the total connectome. The magnitude of the correlation between efficiency and impairment followed the order attention>dexterity ≈ strength (strength: | Attentional impairment is more sensitive to disruption of coordinated networks between brain regions than motor impairment, which is sensitive to disruption of localized networks. Providing more accurate reflections of actually functioning parts of the network enables the incorporation of information about the impact of brain lesions on connectomics contributing to a better understanding of underlying stroke mechanisms.

Sections du résumé

BACKGROUND
Most studies on stroke have been designed to examine one deficit in isolation; yet, survivors often have multiple deficits in different domains. While the mechanisms underlying multiple-domain deficits remain poorly understood, network-theoretical methods may open new avenues of understanding.
METHODS
Fifty subacute stroke patients (7±3days poststroke) underwent diffusion-weighted magnetic resonance imaging and a battery of clinical tests of motor and cognitive functions. We defined indices of impairment in strength, dexterity, and attention. We also computed imaging-based probabilistic tractography and whole-brain connectomes. To efficiently integrate inputs from different sources, brain networks rely on a rich-club of a few hub nodes. Lesions harm efficiency, particularly when they target the rich-club. Overlaying individual lesion masks onto the tractograms enabled us to split the connectomes into their affected and unaffected parts and associate them to impairment.
RESULTS
We computed efficiency of the unaffected connectome and found it was more strongly correlated to impairment in strength, dexterity, and attention than efficiency of the total connectome. The magnitude of the correlation between efficiency and impairment followed the order attention>dexterity ≈ strength (strength: |
CONCLUSIONS
Attentional impairment is more sensitive to disruption of coordinated networks between brain regions than motor impairment, which is sensitive to disruption of localized networks. Providing more accurate reflections of actually functioning parts of the network enables the incorporation of information about the impact of brain lesions on connectomics contributing to a better understanding of underlying stroke mechanisms.

Identifiants

DOI: 10.1161/STROKEAHA.122.040001 PMID: 36846963 PMC: PMC10662579
pubmed: 36846963
doi: 10.1161/STROKEAHA.122.040001
pmc: PMC10662579
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

955-963

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Auteurs

Giorgia G Evangelista (GG)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
ORCID: 0000-0002-8317-393X

Philip Egger (P)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
ORCID: 0000-0003-0823-3266

Julia Brügger (J)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
ORCID: 0000-0002-4675-2502

Elena Beanato (E)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
ORCID: 0000-0002-4451-1684

Philipp J Koch (PJ)

Department of Neurology, University of Lübeck, Germany (P.J.K.).
Center of Brain, Behavior and Metabolism, University of Lübeck, Germany (P.J.K.).

Martino Ceroni (M)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
ORCID: 0000-0002-9470-1849

Lisa Fleury (L)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
ORCID: 0000-0002-1277-7197

Andéol Cadic-Melchior (A)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
ORCID: 0000-0001-9899-299X

Nathalie H Meyer (NH)

Laboratory of Cognitive Neuroscience, CNP and BMI, EPFL, Switzerland (N.H.M., D.d.L.R.).
ORCID: 0000-0001-8969-7761

Diego de León Rodríguez (DL)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
Laboratory of Cognitive Neuroscience, CNP and BMI, EPFL, Switzerland (N.H.M., D.d.L.R.).
Department of Neurology, Hôpital du Valais, Switzerland (C.C., V.A., D.d.L.R., D.S.M., C.B.).
ORCID: 0000-0003-3649-4420

Gabriel Girard (G)

Signal Processing Laboratory (LTS5), School of Engineering, EPFL, Switzerland (G.G.).
Center for Biomedical Imaging (CIBM), Switzerland (G.G.).
Department of Radiology, CHUV, Switzerland (G.G.).
ORCID: 0000-0002-5781-3104

Bertrand Léger (B)

Clinique Romande de Réadaptation, Switzerland (B.L., A.M., P.V., J.-L.T.).
ORCID: 0000-0003-2782-1442

Jean-Luc Turlan (JL)

Clinique Romande de Réadaptation, Switzerland (B.L., A.M., P.V., J.-L.T.).
ORCID: 0000-0003-0654-620X

Andreas Mühl (A)

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

Philippe Vuadens (P)

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

Jan Adolphsen (J)

Mediclin Reha-Zentrum, Germany (J.A.).

Caroline E Jagella (CE)

Migräne- und Kopfschmerzklinik Königstein, Germany (C.E.J.).

Christophe Constantin (C)

Department of Neurology, Hôpital du Valais, Switzerland (C.C., V.A., D.d.L.R., D.S.M., C.B.).
ORCID: 0000-0003-1849-2659

Vincent Alvarez (V)

Department of Neurology, Hôpital du Valais, Switzerland (C.C., V.A., D.d.L.R., D.S.M., C.B.).

Diego San Millán (D)

Department of Neurology, Hôpital du Valais, Switzerland (C.C., V.A., D.d.L.R., D.S.M., C.B.).
ORCID: 0000-0003-4945-812X

Christophe Bonvin (C)

Department of Neurology, Hôpital du Valais, Switzerland (C.C., V.A., D.d.L.R., D.S.M., C.B.).
ORCID: 0000-0002-9058-8105

Takuya Morishita (T)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
ORCID: 0000-0003-0039-1825

Maximilian J Wessel (MJ)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
Department of Neurology, University Hospital Würzburg, Germany (M.J.W.).

Dimitri Van De Ville (D)

Medical Image Processing Laboratory, Institute of Bioengineering, EPFL, Switzerland (D.V.D.V.).
Department of Radiology and Medical Informatics, University of Geneva (UNIGE), Switzerland (D.V.D.V.).
ORCID: 0000-0002-2879-3861

Friedhelm C Hummel (FC)

Defitech Chair of Clinical Neuroengineering, Neuro-X Institute (INX), École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., D.d.L.R., T.M., M.J.W., F.C.H.).
Defitech Chair of Clinical Neuroengineering, INX, EPFL Valais, Clinique Romande de Réadaptation, Switzerland (G.G.E., P.E., J.B., E.B., M.C., L.F., A.C.-M., T.M., D.d.L.R., M.J.W., F.C.H.).
Clinical Neuroscience, Geneva University Hospital (HUG), Switzerland (F.C.H.).
ORCID: 0000-0002-4746-4633

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Differential Impact of Brain Network...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Differential Impact of Brain Network...
questionsmedicales.fr › Diagnostic › Techniques et procédures diagnostiques › Imagerie diagnostique › Tomographie › Imagerie par résonance magnétique › Imagerie par résonance magnétique de diffusion › Differential Impact of Brain Network...
questionsmedicales.fr › Maladies cardiovasculaires › Maladies vasculaires › Angiopathies intracrâniennes › Accident vasculaire cérébral › Differential Impact of Brain Network...
questionsmedicales.fr › Troubles mentaux › Troubles neurocognitifs › Troubles de la cognition › Dysfonctionnement cognitif › Differential Impact of Brain Network...
questionsmedicales.fr › Phénomènes psychologiques › Processus mentaux › Cognition › Differential Impact of Brain Network...
questionsmedicales.fr › Techniques d'investigation › Neuroimagerie › Neuroimagerie fonctionnelle › Cartographie cérébrale › Connectome › Differential Impact of Brain Network...
questionsmedicales.fr › Diagnostic › Techniques et procédures diagnostiques › Imagerie diagnostique › Tomographie › Imagerie par résonance magnétique › Differential Impact of Brain Network...