The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking
BackgroundMass 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...
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Frontiers Media S.A.
2022-10-01
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| Series: | Frontiers in Neurology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fneur.2022.968385/full |
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| author | Shraddha Srivastava Shraddha Srivastava Bryant A. Seamon Bryant A. Seamon Bryant A. Seamon Barbara K. Marebwa Janina Wilmskoetter Mark G. Bowden Mark G. Bowden Mark G. Bowden Chris M. Gregory Chris M. Gregory Chris M. Gregory Na Jin Seo Na Jin Seo Na Jin Seo Colleen A. Hanlon Leonardo Bonilha Truman R. Brown Richard R. Neptune Steven A. Kautz Steven A. Kautz Steven A. Kautz |
| author_facet | Shraddha Srivastava Shraddha Srivastava Bryant A. Seamon Bryant A. Seamon Bryant A. Seamon Barbara K. Marebwa Janina Wilmskoetter Mark G. Bowden Mark G. Bowden Mark G. Bowden Chris M. Gregory Chris M. Gregory Chris M. Gregory Na Jin Seo Na Jin Seo Na Jin Seo Colleen A. Hanlon Leonardo Bonilha Truman R. Brown Richard R. Neptune Steven A. Kautz Steven A. Kautz Steven A. Kautz |
| author_sort | Shraddha Srivastava |
| collection | DOAJ |
| description | BackgroundMass 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.MethodsSeventeen 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.ResultsInterhemispheric 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.ConclusionBoth 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. |
| first_indexed | 2024-04-11T08:27:18Z |
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| last_indexed | 2024-04-11T08:27:18Z |
| publishDate | 2022-10-01 |
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| series | Frontiers in Neurology |
| spelling | doaj.art-dc3aeda7ed004d03986421509433f1062022-12-22T04:34:41ZengFrontiers Media S.A.Frontiers in Neurology1664-22952022-10-011310.3389/fneur.2022.968385968385The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walkingShraddha Srivastava0Shraddha Srivastava1Bryant A. Seamon2Bryant A. Seamon3Bryant A. Seamon4Barbara K. Marebwa5Janina Wilmskoetter6Mark G. Bowden7Mark G. Bowden8Mark G. Bowden9Chris M. Gregory10Chris M. Gregory11Chris M. Gregory12Na Jin Seo13Na Jin Seo14Na Jin Seo15Colleen A. Hanlon16Leonardo Bonilha17Truman R. Brown18Richard R. Neptune19Steven A. Kautz20Steven A. Kautz21Steven A. Kautz22Ralph H. Johnson VA Medical Center, Charleston, SC, United StatesDepartment of Health Sciences and Research, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesRalph H. Johnson VA Medical Center, Charleston, SC, United StatesDepartment of Health Sciences and Research, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesDivision of Physical Therapy, Department of Rehabilitation Sciences, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesDepartment of Neurology, College of Medicine, Medical University of South Carolina, Charleston, SC, United StatesDepartment of Health Sciences and Research, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesRalph H. Johnson VA Medical Center, Charleston, SC, United StatesDepartment of Health Sciences and Research, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesDivision of Physical Therapy, Department of Rehabilitation Sciences, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesRalph H. Johnson VA Medical Center, Charleston, SC, United StatesDepartment of Health Sciences and Research, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesDivision of Physical Therapy, Department of Rehabilitation Sciences, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesRalph H. Johnson VA Medical Center, Charleston, SC, United StatesDepartment of Health Sciences and Research, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesDivision of Occupational Therapy, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesDepartment of Cancer Biology, Wake Forest School of Medicine, Winston-Salem, NC, United StatesDepartment of Neurology, College of Medicine, Medical University of South Carolina, Charleston, SC, United StatesDepartment of Radiology and Radiological Science, College of Medicine, Medical University of South Carolina, Charleston, SC, United StatesWalker Department of Mechanical Engineering, The University of Texas at Austin, Austin, TX, United StatesRalph H. Johnson VA Medical Center, Charleston, SC, United StatesDepartment of Health Sciences and Research, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesDivision of Physical Therapy, Department of Rehabilitation Sciences, College of Health Professions, Medical University of South Carolina, Charleston, SC, United StatesBackgroundMass 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.MethodsSeventeen 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.ResultsInterhemispheric 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.ConclusionBoth 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.https://www.frontiersin.org/articles/10.3389/fneur.2022.968385/fullstrokegaitcorticospinal tract (CST)corticoreticular pathways (CRP)EMGmuscle modules |
| spellingShingle | Shraddha Srivastava Shraddha Srivastava Bryant A. Seamon Bryant A. Seamon Bryant A. Seamon Barbara K. Marebwa Janina Wilmskoetter Mark G. Bowden Mark G. Bowden Mark G. Bowden Chris M. Gregory Chris M. Gregory Chris M. Gregory Na Jin Seo Na Jin Seo Na Jin Seo Colleen A. Hanlon Leonardo Bonilha Truman R. Brown Richard R. Neptune Steven A. Kautz Steven A. Kautz Steven A. Kautz The relationship between motor pathway damage and flexion-extension patterns of muscle co-excitation during walking Frontiers in Neurology stroke gait corticospinal tract (CST) corticoreticular pathways (CRP) EMG muscle modules |
| 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 | stroke gait corticospinal tract (CST) corticoreticular pathways (CRP) EMG muscle modules |
| url | https://www.frontiersin.org/articles/10.3389/fneur.2022.968385/full |
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