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Altered topology of large-scale structural brain networks in chronic stroke

Beyond disruption of neuronal pathways, focal stroke lesions induce structural disintegration of distant, yet connected brain regions via retrograde neuronal degeneration. Stroke lesions alter functional brain connectivity and topology in large-scale brain networks. These changes are associated with...

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Autores principales: Cheng, Bastian, Schlemm, Eckhard, Schulz, Robert, Boenstrup, Marlene, Messé, Arnaud, Hilgetag, Claus, Gerloff, Christian, Thomalla, Götz
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7425306/
https://www.ncbi.nlm.nih.gov/pubmed/32954263
http://dx.doi.org/10.1093/braincomms/fcz020
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author Cheng, Bastian
Schlemm, Eckhard
Schulz, Robert
Boenstrup, Marlene
Messé, Arnaud
Hilgetag, Claus
Gerloff, Christian
Thomalla, Götz
author_facet Cheng, Bastian
Schlemm, Eckhard
Schulz, Robert
Boenstrup, Marlene
Messé, Arnaud
Hilgetag, Claus
Gerloff, Christian
Thomalla, Götz
author_sort Cheng, Bastian
collection PubMed
description Beyond disruption of neuronal pathways, focal stroke lesions induce structural disintegration of distant, yet connected brain regions via retrograde neuronal degeneration. Stroke lesions alter functional brain connectivity and topology in large-scale brain networks. These changes are associated with the degree of clinical impairment and recovery. In contrast, changes of large scale, structural brain networks after stroke are less well reported. We therefore aimed to analyse the impact of focal lesions on the structural connectome after stroke based on data from diffusion-weighted imaging and probabilistic fibre tracking. In total, 17 patients (mean age 64.5 ± 8.4 years) with upper limb motor deficits in the chronic stage after stroke and 21 healthy participants (mean age 64.9 ± 10.3 years) were included. Clinical deficits were evaluated by grip strength and the upper extremity Fugl-Meyer assessment. We calculated global and local graph theoretical measures to characterize topological changes in the structural connectome. Results from our analysis demonstrated significant alterations of network topology in both ipsi- and contralesional, primarily unaffected, hemispheres after stroke. Global efficiency was significantly lower in stroke connectomes as an indicator of overall reduced capacity for information transfer between distant brain areas. Furthermore, topology of structural connectomes was shifted toward a higher degree of segregation as indicated by significantly higher values of global clustering and modularity. On a level of local network parameters, these effects were most pronounced in a subnetwork of cortico-subcortical brain regions involved in motor control. Structural changes were not significantly associated with clinical measures. We propose that the observed network changes in our patients are best explained by the disruption of inter- and intrahemispheric, long white matter fibre tracts connecting distant brain regions. Our results add novel insights on topological changes of structural large-scale brain networks in the ipsi- and contralesional hemisphere after stroke.
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spelling pubmed-74253062020-09-17 Altered topology of large-scale structural brain networks in chronic stroke Cheng, Bastian Schlemm, Eckhard Schulz, Robert Boenstrup, Marlene Messé, Arnaud Hilgetag, Claus Gerloff, Christian Thomalla, Götz Brain Commun Original Article Beyond disruption of neuronal pathways, focal stroke lesions induce structural disintegration of distant, yet connected brain regions via retrograde neuronal degeneration. Stroke lesions alter functional brain connectivity and topology in large-scale brain networks. These changes are associated with the degree of clinical impairment and recovery. In contrast, changes of large scale, structural brain networks after stroke are less well reported. We therefore aimed to analyse the impact of focal lesions on the structural connectome after stroke based on data from diffusion-weighted imaging and probabilistic fibre tracking. In total, 17 patients (mean age 64.5 ± 8.4 years) with upper limb motor deficits in the chronic stage after stroke and 21 healthy participants (mean age 64.9 ± 10.3 years) were included. Clinical deficits were evaluated by grip strength and the upper extremity Fugl-Meyer assessment. We calculated global and local graph theoretical measures to characterize topological changes in the structural connectome. Results from our analysis demonstrated significant alterations of network topology in both ipsi- and contralesional, primarily unaffected, hemispheres after stroke. Global efficiency was significantly lower in stroke connectomes as an indicator of overall reduced capacity for information transfer between distant brain areas. Furthermore, topology of structural connectomes was shifted toward a higher degree of segregation as indicated by significantly higher values of global clustering and modularity. On a level of local network parameters, these effects were most pronounced in a subnetwork of cortico-subcortical brain regions involved in motor control. Structural changes were not significantly associated with clinical measures. We propose that the observed network changes in our patients are best explained by the disruption of inter- and intrahemispheric, long white matter fibre tracts connecting distant brain regions. Our results add novel insights on topological changes of structural large-scale brain networks in the ipsi- and contralesional hemisphere after stroke. Oxford University Press 2019-10-04 /pmc/articles/PMC7425306/ /pubmed/32954263 http://dx.doi.org/10.1093/braincomms/fcz020 Text en © The Author(s) (2019). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Cheng, Bastian
Schlemm, Eckhard
Schulz, Robert
Boenstrup, Marlene
Messé, Arnaud
Hilgetag, Claus
Gerloff, Christian
Thomalla, Götz
Altered topology of large-scale structural brain networks in chronic stroke
title Altered topology of large-scale structural brain networks in chronic stroke
title_full Altered topology of large-scale structural brain networks in chronic stroke
title_fullStr Altered topology of large-scale structural brain networks in chronic stroke
title_full_unstemmed Altered topology of large-scale structural brain networks in chronic stroke
title_short Altered topology of large-scale structural brain networks in chronic stroke
title_sort altered topology of large-scale structural brain networks in chronic stroke
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7425306/
https://www.ncbi.nlm.nih.gov/pubmed/32954263
http://dx.doi.org/10.1093/braincomms/fcz020
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