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Emergence of functionally aberrant and subsequent reduction of neuromuscular connectivity and improved motor performance after cervical spinal cord injury in Rhesus

INTRODUCTION: The paralysis that occurs after a spinal cord injury, particularly during the early stages of post-lesion recovery (∼6 weeks), appears to be attributable to the inability to activate motor pools well beyond their motor threshold. In the later stages of recovery, however, the inability...

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Autores principales: Wai, Gregory, Zdunowski, Sharon, Zhong, Hui, Nielson, Jessica L., Ferguson, Adam R., Strand, Sarah C., Moseanko, Rod, Hawbecker, Stephanie, Nout-Lomas, Yvette S., Rosenzweig, Ephron S., Beattie, Michael S., Bresnahan, Jacqueline C., Tuszynski, Mark H., Roy, Roland R., Edgerton, V. Reggie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10291623/
https://www.ncbi.nlm.nih.gov/pubmed/37378049
http://dx.doi.org/10.3389/fresc.2023.1205456
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author Wai, Gregory
Zdunowski, Sharon
Zhong, Hui
Nielson, Jessica L.
Ferguson, Adam R.
Strand, Sarah C.
Moseanko, Rod
Hawbecker, Stephanie
Nout-Lomas, Yvette S.
Rosenzweig, Ephron S.
Beattie, Michael S.
Bresnahan, Jacqueline C.
Tuszynski, Mark H.
Roy, Roland R.
Edgerton, V. Reggie
author_facet Wai, Gregory
Zdunowski, Sharon
Zhong, Hui
Nielson, Jessica L.
Ferguson, Adam R.
Strand, Sarah C.
Moseanko, Rod
Hawbecker, Stephanie
Nout-Lomas, Yvette S.
Rosenzweig, Ephron S.
Beattie, Michael S.
Bresnahan, Jacqueline C.
Tuszynski, Mark H.
Roy, Roland R.
Edgerton, V. Reggie
author_sort Wai, Gregory
collection PubMed
description INTRODUCTION: The paralysis that occurs after a spinal cord injury, particularly during the early stages of post-lesion recovery (∼6 weeks), appears to be attributable to the inability to activate motor pools well beyond their motor threshold. In the later stages of recovery, however, the inability to perform a motor task effectively can be attributed to abnormal activation patterns among motor pools, resulting in poor coordination. METHOD: We have tested this hypothesis on four adult male Rhesus monkeys (Macaca mulatta), ages 6-10 years, by recording the EMG activity levels and patterns of multiple proximal and distal muscles controlling the upper limb of the Rhesus when performing three tasks requiring different levels of skill before and up to 24 weeks after a lateral hemisection at C7. During the recovery period the animals were provided routine daily care, including access to a large exercise cage (5' × 7' × 10') and tested every 3-4 weeks for each of the three motor tasks. RESULTS: At approximately 6-8 weeks the animals were able to begin to step on a treadmill, perform a spring-loaded task with the upper limb, and reaching, grasping, and eating a grape placed on a vertical stick. The predominant changes that occurred, beginning at ∼6-8 weeks of the recovery of these tasks was an elevated level of activation of most motor pools well beyond the pre-lesion level. DISCUSSION: As the chronic phase progressed there was a slight reduction in the EMG burst amplitudes of some muscles and less incidence of co-contraction of agonists and antagonists, probably contributing to an improved ability to selectively activate motor pools in a more effective temporal pattern. Relative to pre-lesion, however, the EMG patterns even at the initial stages of recovery of successfully performing the different motor tasks, the level of activity of most muscle remained higher. Perhaps the most important concept that emerges from these data is the large combinations of adaptive strategies in the relative level of recruitment and the timing of the peak levels of activation of different motor pools can progressively provide different stages to regain a motor skill.
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spelling pubmed-102916232023-06-27 Emergence of functionally aberrant and subsequent reduction of neuromuscular connectivity and improved motor performance after cervical spinal cord injury in Rhesus Wai, Gregory Zdunowski, Sharon Zhong, Hui Nielson, Jessica L. Ferguson, Adam R. Strand, Sarah C. Moseanko, Rod Hawbecker, Stephanie Nout-Lomas, Yvette S. Rosenzweig, Ephron S. Beattie, Michael S. Bresnahan, Jacqueline C. Tuszynski, Mark H. Roy, Roland R. Edgerton, V. Reggie Front Rehabil Sci Rehabilitation Sciences INTRODUCTION: The paralysis that occurs after a spinal cord injury, particularly during the early stages of post-lesion recovery (∼6 weeks), appears to be attributable to the inability to activate motor pools well beyond their motor threshold. In the later stages of recovery, however, the inability to perform a motor task effectively can be attributed to abnormal activation patterns among motor pools, resulting in poor coordination. METHOD: We have tested this hypothesis on four adult male Rhesus monkeys (Macaca mulatta), ages 6-10 years, by recording the EMG activity levels and patterns of multiple proximal and distal muscles controlling the upper limb of the Rhesus when performing three tasks requiring different levels of skill before and up to 24 weeks after a lateral hemisection at C7. During the recovery period the animals were provided routine daily care, including access to a large exercise cage (5' × 7' × 10') and tested every 3-4 weeks for each of the three motor tasks. RESULTS: At approximately 6-8 weeks the animals were able to begin to step on a treadmill, perform a spring-loaded task with the upper limb, and reaching, grasping, and eating a grape placed on a vertical stick. The predominant changes that occurred, beginning at ∼6-8 weeks of the recovery of these tasks was an elevated level of activation of most motor pools well beyond the pre-lesion level. DISCUSSION: As the chronic phase progressed there was a slight reduction in the EMG burst amplitudes of some muscles and less incidence of co-contraction of agonists and antagonists, probably contributing to an improved ability to selectively activate motor pools in a more effective temporal pattern. Relative to pre-lesion, however, the EMG patterns even at the initial stages of recovery of successfully performing the different motor tasks, the level of activity of most muscle remained higher. Perhaps the most important concept that emerges from these data is the large combinations of adaptive strategies in the relative level of recruitment and the timing of the peak levels of activation of different motor pools can progressively provide different stages to regain a motor skill. Frontiers Media S.A. 2023-06-12 /pmc/articles/PMC10291623/ /pubmed/37378049 http://dx.doi.org/10.3389/fresc.2023.1205456 Text en © 2023 Wai, Zdunowski, Zhong, Nielson, Ferguson, Strand, Moseanko, Hawbecker, Nout-Lomas, Rosenzweig, Beattie, Bresnahan, Tuszynski, Roy and Edgerton. 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) (https://creativecommons.org/licenses/by/4.0/) . 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 Rehabilitation Sciences
Wai, Gregory
Zdunowski, Sharon
Zhong, Hui
Nielson, Jessica L.
Ferguson, Adam R.
Strand, Sarah C.
Moseanko, Rod
Hawbecker, Stephanie
Nout-Lomas, Yvette S.
Rosenzweig, Ephron S.
Beattie, Michael S.
Bresnahan, Jacqueline C.
Tuszynski, Mark H.
Roy, Roland R.
Edgerton, V. Reggie
Emergence of functionally aberrant and subsequent reduction of neuromuscular connectivity and improved motor performance after cervical spinal cord injury in Rhesus
title Emergence of functionally aberrant and subsequent reduction of neuromuscular connectivity and improved motor performance after cervical spinal cord injury in Rhesus
title_full Emergence of functionally aberrant and subsequent reduction of neuromuscular connectivity and improved motor performance after cervical spinal cord injury in Rhesus
title_fullStr Emergence of functionally aberrant and subsequent reduction of neuromuscular connectivity and improved motor performance after cervical spinal cord injury in Rhesus
title_full_unstemmed Emergence of functionally aberrant and subsequent reduction of neuromuscular connectivity and improved motor performance after cervical spinal cord injury in Rhesus
title_short Emergence of functionally aberrant and subsequent reduction of neuromuscular connectivity and improved motor performance after cervical spinal cord injury in Rhesus
title_sort emergence of functionally aberrant and subsequent reduction of neuromuscular connectivity and improved motor performance after cervical spinal cord injury in rhesus
topic Rehabilitation Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10291623/
https://www.ncbi.nlm.nih.gov/pubmed/37378049
http://dx.doi.org/10.3389/fresc.2023.1205456
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