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Epidural stimulation restores muscle synergies by modulating neural drives in participants with sensorimotor complete spinal cord injuries

Multiple studies have corroborated the restoration of volitional motor control after motor-complete spinal cord injury (SCI) through the use of epidural spinal cord stimulation (eSCS), but rigorous quantitative descriptions of muscle coordination have been lacking. Six participants with chronic, mot...

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Autores principales: Singh, Rajat Emanuel, Ahmadi, Aliya, Parr, Ann M., Samadani, Uzma, Krassioukov, Andrei V., Netoff, Theoden I., Darrow, David P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10155428/
https://www.ncbi.nlm.nih.gov/pubmed/37138361
http://dx.doi.org/10.1186/s12984-023-01164-1
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author Singh, Rajat Emanuel
Ahmadi, Aliya
Parr, Ann M.
Samadani, Uzma
Krassioukov, Andrei V.
Netoff, Theoden I.
Darrow, David P.
author_facet Singh, Rajat Emanuel
Ahmadi, Aliya
Parr, Ann M.
Samadani, Uzma
Krassioukov, Andrei V.
Netoff, Theoden I.
Darrow, David P.
author_sort Singh, Rajat Emanuel
collection PubMed
description Multiple studies have corroborated the restoration of volitional motor control after motor-complete spinal cord injury (SCI) through the use of epidural spinal cord stimulation (eSCS), but rigorous quantitative descriptions of muscle coordination have been lacking. Six participants with chronic, motor and sensory complete SCI underwent a brain motor control assessment (BMCA) consisting of a set of structured motor tasks with and without eSCS. We investigated how muscle activity complexity and muscle synergies changed with and without stimulation. We performed this analysis to better characterize the impact of stimulation on neuromuscular control. We also recorded data from nine healthy participants as controls. Competition exists between the task origin and neural origin hypotheses underlying muscle synergies. The ability to restore motor control with eSCS in participants with motor and sensory complete SCI allows us to test whether changes in muscle synergies reflect a neural basis in the same task. Muscle activity complexity was computed with Higuchi Fractal Dimensional (HFD) analysis, and muscle synergies were estimated using non-negative matrix factorization (NNMF) in six participants with American Spinal Injury Association (ASIA) Impairment Score (AIS) A. We found that the complexity of muscle activity was immediately reduced by eSCS in the SCI participants. We also found that over the follow-up sessions, the muscle synergy structure of the SCI participants became more defined, and the number of synergies decreased over time, indicating improved coordination between muscle groups. Lastly, we found that the muscle synergies were restored with eSCS, supporting the neural hypothesis of muscle synergies. We conclude that eSCS restores muscle movements and muscle synergies that are distinct from those of healthy, able-bodied controls. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12984-023-01164-1.
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spelling pubmed-101554282023-05-04 Epidural stimulation restores muscle synergies by modulating neural drives in participants with sensorimotor complete spinal cord injuries Singh, Rajat Emanuel Ahmadi, Aliya Parr, Ann M. Samadani, Uzma Krassioukov, Andrei V. Netoff, Theoden I. Darrow, David P. J Neuroeng Rehabil Research Multiple studies have corroborated the restoration of volitional motor control after motor-complete spinal cord injury (SCI) through the use of epidural spinal cord stimulation (eSCS), but rigorous quantitative descriptions of muscle coordination have been lacking. Six participants with chronic, motor and sensory complete SCI underwent a brain motor control assessment (BMCA) consisting of a set of structured motor tasks with and without eSCS. We investigated how muscle activity complexity and muscle synergies changed with and without stimulation. We performed this analysis to better characterize the impact of stimulation on neuromuscular control. We also recorded data from nine healthy participants as controls. Competition exists between the task origin and neural origin hypotheses underlying muscle synergies. The ability to restore motor control with eSCS in participants with motor and sensory complete SCI allows us to test whether changes in muscle synergies reflect a neural basis in the same task. Muscle activity complexity was computed with Higuchi Fractal Dimensional (HFD) analysis, and muscle synergies were estimated using non-negative matrix factorization (NNMF) in six participants with American Spinal Injury Association (ASIA) Impairment Score (AIS) A. We found that the complexity of muscle activity was immediately reduced by eSCS in the SCI participants. We also found that over the follow-up sessions, the muscle synergy structure of the SCI participants became more defined, and the number of synergies decreased over time, indicating improved coordination between muscle groups. Lastly, we found that the muscle synergies were restored with eSCS, supporting the neural hypothesis of muscle synergies. We conclude that eSCS restores muscle movements and muscle synergies that are distinct from those of healthy, able-bodied controls. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12984-023-01164-1. BioMed Central 2023-05-03 /pmc/articles/PMC10155428/ /pubmed/37138361 http://dx.doi.org/10.1186/s12984-023-01164-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Singh, Rajat Emanuel
Ahmadi, Aliya
Parr, Ann M.
Samadani, Uzma
Krassioukov, Andrei V.
Netoff, Theoden I.
Darrow, David P.
Epidural stimulation restores muscle synergies by modulating neural drives in participants with sensorimotor complete spinal cord injuries
title Epidural stimulation restores muscle synergies by modulating neural drives in participants with sensorimotor complete spinal cord injuries
title_full Epidural stimulation restores muscle synergies by modulating neural drives in participants with sensorimotor complete spinal cord injuries
title_fullStr Epidural stimulation restores muscle synergies by modulating neural drives in participants with sensorimotor complete spinal cord injuries
title_full_unstemmed Epidural stimulation restores muscle synergies by modulating neural drives in participants with sensorimotor complete spinal cord injuries
title_short Epidural stimulation restores muscle synergies by modulating neural drives in participants with sensorimotor complete spinal cord injuries
title_sort epidural stimulation restores muscle synergies by modulating neural drives in participants with sensorimotor complete spinal cord injuries
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10155428/
https://www.ncbi.nlm.nih.gov/pubmed/37138361
http://dx.doi.org/10.1186/s12984-023-01164-1
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