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

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 understa...

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Autores principales: Evangelista, Giorgia G., Egger, Philip, Brügger, Julia, Beanato, Elena, Koch, Philipp J., Ceroni, Martino, Fleury, Lisa, Cadic-Melchior, Andéol, Meyer, Nathalie H., Rodríguez, Diego de León, Girard, Gabriel, Léger, Bertrand, Turlan, Jean-Luc, Mühl, Andreas, Vuadens, Philippe, Adolphsen, Jan, Jagella, Caroline E., Constantin, Christophe, Alvarez, Vincent, San Millán, Diego, Bonvin, Christophe, Morishita, Takuya, Wessel, Maximilian J., Van De Ville, Dimitri, Hummel, Friedhelm C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Lippincott Williams & Wilkins 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10662579/
https://www.ncbi.nlm.nih.gov/pubmed/36846963
http://dx.doi.org/10.1161/STROKEAHA.122.040001
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author Evangelista, Giorgia G.
Egger, Philip
Brügger, Julia
Beanato, Elena
Koch, Philipp J.
Ceroni, Martino
Fleury, Lisa
Cadic-Melchior, Andéol
Meyer, Nathalie H.
Rodríguez, Diego de León
Girard, Gabriel
Léger, Bertrand
Turlan, Jean-Luc
Mühl, Andreas
Vuadens, Philippe
Adolphsen, Jan
Jagella, Caroline E.
Constantin, Christophe
Alvarez, Vincent
San Millán, Diego
Bonvin, Christophe
Morishita, Takuya
Wessel, Maximilian J.
Van De Ville, Dimitri
Hummel, Friedhelm C.
author_facet Evangelista, Giorgia G.
Egger, Philip
Brügger, Julia
Beanato, Elena
Koch, Philipp J.
Ceroni, Martino
Fleury, Lisa
Cadic-Melchior, Andéol
Meyer, Nathalie H.
Rodríguez, Diego de León
Girard, Gabriel
Léger, Bertrand
Turlan, Jean-Luc
Mühl, Andreas
Vuadens, Philippe
Adolphsen, Jan
Jagella, Caroline E.
Constantin, Christophe
Alvarez, Vincent
San Millán, Diego
Bonvin, Christophe
Morishita, Takuya
Wessel, Maximilian J.
Van De Ville, Dimitri
Hummel, Friedhelm C.
author_sort Evangelista, Giorgia G.
collection PubMed
description 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: |r|=.03, P=0.02, dexterity: |r|=.30, P=0.05, attention: |r|=.55, P<0.001). Network weights associated with the rich-club were more strongly correlated to efficiency than non-rich-club weights. 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.
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spelling pubmed-106625792023-11-21 Differential Impact of Brain Network Efficiency on Poststroke Motor and Attentional Deficits Evangelista, Giorgia G. Egger, Philip Brügger, Julia Beanato, Elena Koch, Philipp J. Ceroni, Martino Fleury, Lisa Cadic-Melchior, Andéol Meyer, Nathalie H. Rodríguez, Diego de León Girard, Gabriel Léger, Bertrand Turlan, Jean-Luc Mühl, Andreas Vuadens, Philippe Adolphsen, Jan Jagella, Caroline E. Constantin, Christophe Alvarez, Vincent San Millán, Diego Bonvin, Christophe Morishita, Takuya Wessel, Maximilian J. Van De Ville, Dimitri Hummel, Friedhelm C. Stroke Original Contributions 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: |r|=.03, P=0.02, dexterity: |r|=.30, P=0.05, attention: |r|=.55, P<0.001). Network weights associated with the rich-club were more strongly correlated to efficiency than non-rich-club weights. 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. Lippincott Williams & Wilkins 2023-02-27 2023-04 /pmc/articles/PMC10662579/ /pubmed/36846963 http://dx.doi.org/10.1161/STROKEAHA.122.040001 Text en © 2023 The Authors. https://creativecommons.org/licenses/by-nc-nd/4.0/Stroke is published on behalf of the American Heart Association, Inc., by Wolters Kluwer Health, Inc. This is an open access article under the terms of the Creative Commons Attribution Non-Commercial-NoDerivs (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use, distribution, and reproduction in any medium, provided that the original work is properly cited, the use is noncommercial, and no modifications or adaptations are made.
spellingShingle Original Contributions
Evangelista, Giorgia G.
Egger, Philip
Brügger, Julia
Beanato, Elena
Koch, Philipp J.
Ceroni, Martino
Fleury, Lisa
Cadic-Melchior, Andéol
Meyer, Nathalie H.
Rodríguez, Diego de León
Girard, Gabriel
Léger, Bertrand
Turlan, Jean-Luc
Mühl, Andreas
Vuadens, Philippe
Adolphsen, Jan
Jagella, Caroline E.
Constantin, Christophe
Alvarez, Vincent
San Millán, Diego
Bonvin, Christophe
Morishita, Takuya
Wessel, Maximilian J.
Van De Ville, Dimitri
Hummel, Friedhelm C.
Differential Impact of Brain Network Efficiency on Poststroke Motor and Attentional Deficits
title Differential Impact of Brain Network Efficiency on Poststroke Motor and Attentional Deficits
title_full Differential Impact of Brain Network Efficiency on Poststroke Motor and Attentional Deficits
title_fullStr Differential Impact of Brain Network Efficiency on Poststroke Motor and Attentional Deficits
title_full_unstemmed Differential Impact of Brain Network Efficiency on Poststroke Motor and Attentional Deficits
title_short Differential Impact of Brain Network Efficiency on Poststroke Motor and Attentional Deficits
title_sort differential impact of brain network efficiency on poststroke motor and attentional deficits
topic Original Contributions
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10662579/
https://www.ncbi.nlm.nih.gov/pubmed/36846963
http://dx.doi.org/10.1161/STROKEAHA.122.040001
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