Cargando…
The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking
BACKGROUND: Mass flexion-extension co-excitation patterns during walking are often seen as a consequence of stroke, but there is limited understanding of the specific contributions of different descending motor pathways toward their control. The corticospinal tract is a major descending motor pathwa...
Autores principales: | , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9650203/ https://www.ncbi.nlm.nih.gov/pubmed/36388195 http://dx.doi.org/10.3389/fneur.2022.968385 |
_version_ | 1784827959499030528 |
---|---|
author | Srivastava, Shraddha Seamon, Bryant A. Marebwa, Barbara K. Wilmskoetter, Janina Bowden, Mark G. Gregory, Chris M. Seo, Na Jin Hanlon, Colleen A. Bonilha, Leonardo Brown, Truman R. Neptune, Richard R. Kautz, Steven A. |
author_facet | Srivastava, Shraddha Seamon, Bryant A. Marebwa, Barbara K. Wilmskoetter, Janina Bowden, Mark G. Gregory, Chris M. Seo, Na Jin Hanlon, Colleen A. Bonilha, Leonardo Brown, Truman R. Neptune, Richard R. Kautz, Steven A. |
author_sort | Srivastava, Shraddha |
collection | PubMed |
description | BACKGROUND: Mass flexion-extension co-excitation patterns during walking are often seen as a consequence of stroke, but there is limited understanding of the specific contributions of different descending motor pathways toward their control. The corticospinal tract is a major descending motor pathway influencing the production of normal sequential muscle coactivation patterns for skilled movements. However, control of walking is also influenced by non-corticospinal pathways such as the corticoreticulospinal pathway that possibly contribute toward mass flexion-extension co-excitation patterns during walking. The current study sought to investigate the associations between damage to corticospinal (CST) and corticoreticular (CRP) motor pathways following stroke and the presence of mass flexion-extension patterns during walking as evaluated using module analysis. METHODS: Seventeen healthy controls and 44 stroke survivors were included in the study. We used non-negative matrix factorization for module analysis of paretic leg electromyographic activity. We typically have observed four modules during walking in healthy individuals. Stroke survivors often have less independently timed modules, for example two-modules presented as mass flexion-extension pattern. We used diffusion tensor imaging-based analysis where streamlines connecting regions of interest between the cortex and brainstem were computed to evaluate CST and CRP integrity. We also used a coarse classification tree analysis to evaluate the relative CST and CRP contribution toward module control. RESULTS: Interhemispheric CST asymmetry was associated with worse lower extremity Fugl-Meyer score (p = 0.023), propulsion symmetry (p = 0.016), and fewer modules (p = 0.028). Interhemispheric CRP asymmetry was associated with worse lower extremity Fugl-Meyer score (p = 0.009), Dynamic gait index (p = 0.035), Six-minute walk test (p = 0.020), Berg balance scale (p = 0.048), self-selected walking speed (p = 0.041), and propulsion symmetry (p = 0.001). The classification tree model reveled that substantial ipsilesional CRP or CST damage leads to a two-module pattern and poor walking ability with a trend toward increased compensatory contralesional CRP based control. CONCLUSION: Both CST and CRP are involved with control of modules during walking and damage to both may lead to greater reliance on the contralesional CRP, which may contribute to a two-module pattern and be associated with worse walking performance. |
format | Online Article Text |
id | pubmed-9650203 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-96502032022-11-15 The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking Srivastava, Shraddha Seamon, Bryant A. Marebwa, Barbara K. Wilmskoetter, Janina Bowden, Mark G. Gregory, Chris M. Seo, Na Jin Hanlon, Colleen A. Bonilha, Leonardo Brown, Truman R. Neptune, Richard R. Kautz, Steven A. Front Neurol Neurology BACKGROUND: Mass flexion-extension co-excitation patterns during walking are often seen as a consequence of stroke, but there is limited understanding of the specific contributions of different descending motor pathways toward their control. The corticospinal tract is a major descending motor pathway influencing the production of normal sequential muscle coactivation patterns for skilled movements. However, control of walking is also influenced by non-corticospinal pathways such as the corticoreticulospinal pathway that possibly contribute toward mass flexion-extension co-excitation patterns during walking. The current study sought to investigate the associations between damage to corticospinal (CST) and corticoreticular (CRP) motor pathways following stroke and the presence of mass flexion-extension patterns during walking as evaluated using module analysis. METHODS: Seventeen healthy controls and 44 stroke survivors were included in the study. We used non-negative matrix factorization for module analysis of paretic leg electromyographic activity. We typically have observed four modules during walking in healthy individuals. Stroke survivors often have less independently timed modules, for example two-modules presented as mass flexion-extension pattern. We used diffusion tensor imaging-based analysis where streamlines connecting regions of interest between the cortex and brainstem were computed to evaluate CST and CRP integrity. We also used a coarse classification tree analysis to evaluate the relative CST and CRP contribution toward module control. RESULTS: Interhemispheric CST asymmetry was associated with worse lower extremity Fugl-Meyer score (p = 0.023), propulsion symmetry (p = 0.016), and fewer modules (p = 0.028). Interhemispheric CRP asymmetry was associated with worse lower extremity Fugl-Meyer score (p = 0.009), Dynamic gait index (p = 0.035), Six-minute walk test (p = 0.020), Berg balance scale (p = 0.048), self-selected walking speed (p = 0.041), and propulsion symmetry (p = 0.001). The classification tree model reveled that substantial ipsilesional CRP or CST damage leads to a two-module pattern and poor walking ability with a trend toward increased compensatory contralesional CRP based control. CONCLUSION: Both CST and CRP are involved with control of modules during walking and damage to both may lead to greater reliance on the contralesional CRP, which may contribute to a two-module pattern and be associated with worse walking performance. Frontiers Media S.A. 2022-10-28 /pmc/articles/PMC9650203/ /pubmed/36388195 http://dx.doi.org/10.3389/fneur.2022.968385 Text en Copyright © 2022 Srivastava, Seamon, Marebwa, Wilmskoetter, Bowden, Gregory, Seo, Hanlon, Bonilha, Brown, Neptune and Kautz. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Neurology Srivastava, Shraddha Seamon, Bryant A. Marebwa, Barbara K. Wilmskoetter, Janina Bowden, Mark G. Gregory, Chris M. Seo, Na Jin Hanlon, Colleen A. Bonilha, Leonardo Brown, Truman R. Neptune, Richard R. Kautz, Steven A. The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking |
title | The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking |
title_full | The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking |
title_fullStr | The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking |
title_full_unstemmed | The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking |
title_short | The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking |
title_sort | relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking |
topic | Neurology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9650203/ https://www.ncbi.nlm.nih.gov/pubmed/36388195 http://dx.doi.org/10.3389/fneur.2022.968385 |
work_keys_str_mv | AT srivastavashraddha therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT seamonbryanta therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT marebwabarbarak therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT wilmskoetterjanina therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT bowdenmarkg therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT gregorychrism therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT seonajin therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT hanloncolleena therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT bonilhaleonardo therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT browntrumanr therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT neptunerichardr therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT kautzstevena therelationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT srivastavashraddha relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT seamonbryanta relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT marebwabarbarak relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT wilmskoetterjanina relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT bowdenmarkg relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT gregorychrism relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT seonajin relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT hanloncolleena relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT bonilhaleonardo relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT browntrumanr relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT neptunerichardr relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking AT kautzstevena relationshipbetweenmotorpathwaydamageandflexionextensionpatternsofmusclecoexcitationduringwalking |