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Alterations of Spinal Epidural Stimulation-Enabled Stepping by Descending Intentional Motor Commands and Proprioceptive Inputs in Humans With Spinal Cord Injury

Background: Regaining control of movement following a spinal cord injury (SCI) requires utilization and/or functional reorganization of residual descending, and likely ascending, supraspinal sensorimotor pathways, which may be facilitated via task-specific training through body weight supported trea...

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Autores principales: Gill, Megan L., Linde, Margaux B., Hale, Rena F., Lopez, Cesar, Fautsch, Kalli J., Calvert, Jonathan S., Veith, Daniel D., Beck, Lisa A., Garlanger, Kristin L., Sayenko, Dimitry G., Lavrov, Igor A., Thoreson, Andrew R., Grahn, Peter J., Zhao, Kristin D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7875885/
https://www.ncbi.nlm.nih.gov/pubmed/33584209
http://dx.doi.org/10.3389/fnsys.2020.590231
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author Gill, Megan L.
Linde, Margaux B.
Hale, Rena F.
Lopez, Cesar
Fautsch, Kalli J.
Calvert, Jonathan S.
Veith, Daniel D.
Beck, Lisa A.
Garlanger, Kristin L.
Sayenko, Dimitry G.
Lavrov, Igor A.
Thoreson, Andrew R.
Grahn, Peter J.
Zhao, Kristin D.
author_facet Gill, Megan L.
Linde, Margaux B.
Hale, Rena F.
Lopez, Cesar
Fautsch, Kalli J.
Calvert, Jonathan S.
Veith, Daniel D.
Beck, Lisa A.
Garlanger, Kristin L.
Sayenko, Dimitry G.
Lavrov, Igor A.
Thoreson, Andrew R.
Grahn, Peter J.
Zhao, Kristin D.
author_sort Gill, Megan L.
collection PubMed
description Background: Regaining control of movement following a spinal cord injury (SCI) requires utilization and/or functional reorganization of residual descending, and likely ascending, supraspinal sensorimotor pathways, which may be facilitated via task-specific training through body weight supported treadmill (BWST) training. Recently, epidural electrical stimulation (ES) combined with task-specific training demonstrated independence of standing and stepping functions in individuals with clinically complete SCI. The restoration of these functions may be dependent upon variables such as manipulation of proprioceptive input, ES parameter adjustments, and participant intent during step training. However, the impact of each variable on the degree of independence achieved during BWST stepping remains unknown. Objective: To describe the effects of descending intentional commands and proprioceptive inputs, specifically body weight support (BWS), on lower extremity motor activity and vertical ground reaction forces (vGRF) during ES-enabled BWST stepping in humans with chronic sensorimotor complete SCI. Furthermore, we describe perceived changes in the level of assistance provided by clinicians when intent and BWS are modified. Methods: Two individuals with chronic, mid thoracic, clinically complete SCI, enrolled in an IRB and FDA (IDE G150167) approved clinical trial. A 16-contact electrode array was implanted in the epidural space between the T11-L1 vertebral regions. Lower extremity motor output and vertical ground reaction forces were obtained during clinician-assisted ES-enabled treadmill stepping with BWS. Consecutive steps were achieved during various experimentally-controlled conditions, including intentional participation and varied BWS (60% and 20%) while ES parameters remain unchanged. Results: During ES-enabled BWST stepping, the knee extensors exhibited an increase in motor activation during trials in which stepping was passive compared to active or during trials in which 60% BWS was provided compared to 20% BWS. As a result of this increased motor activation, perceived clinician assistance increased during the transition from stance to swing. Intentional participation and 20% BWS resulted in timely and purposeful activation of the lower extremities muscles, which improved independence and decreased clinician assistance. Conclusion: Maximizing participant intention and optimizing proprioceptive inputs through BWS during ES-enabled BWST stepping may facilitate greater independence during BWST stepping for individuals with clinically complete SCI. Clinical Trial Registration: ClinicalTrials.gov identifier: NCT02592668.
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spelling pubmed-78758852021-02-12 Alterations of Spinal Epidural Stimulation-Enabled Stepping by Descending Intentional Motor Commands and Proprioceptive Inputs in Humans With Spinal Cord Injury Gill, Megan L. Linde, Margaux B. Hale, Rena F. Lopez, Cesar Fautsch, Kalli J. Calvert, Jonathan S. Veith, Daniel D. Beck, Lisa A. Garlanger, Kristin L. Sayenko, Dimitry G. Lavrov, Igor A. Thoreson, Andrew R. Grahn, Peter J. Zhao, Kristin D. Front Syst Neurosci Neuroscience Background: Regaining control of movement following a spinal cord injury (SCI) requires utilization and/or functional reorganization of residual descending, and likely ascending, supraspinal sensorimotor pathways, which may be facilitated via task-specific training through body weight supported treadmill (BWST) training. Recently, epidural electrical stimulation (ES) combined with task-specific training demonstrated independence of standing and stepping functions in individuals with clinically complete SCI. The restoration of these functions may be dependent upon variables such as manipulation of proprioceptive input, ES parameter adjustments, and participant intent during step training. However, the impact of each variable on the degree of independence achieved during BWST stepping remains unknown. Objective: To describe the effects of descending intentional commands and proprioceptive inputs, specifically body weight support (BWS), on lower extremity motor activity and vertical ground reaction forces (vGRF) during ES-enabled BWST stepping in humans with chronic sensorimotor complete SCI. Furthermore, we describe perceived changes in the level of assistance provided by clinicians when intent and BWS are modified. Methods: Two individuals with chronic, mid thoracic, clinically complete SCI, enrolled in an IRB and FDA (IDE G150167) approved clinical trial. A 16-contact electrode array was implanted in the epidural space between the T11-L1 vertebral regions. Lower extremity motor output and vertical ground reaction forces were obtained during clinician-assisted ES-enabled treadmill stepping with BWS. Consecutive steps were achieved during various experimentally-controlled conditions, including intentional participation and varied BWS (60% and 20%) while ES parameters remain unchanged. Results: During ES-enabled BWST stepping, the knee extensors exhibited an increase in motor activation during trials in which stepping was passive compared to active or during trials in which 60% BWS was provided compared to 20% BWS. As a result of this increased motor activation, perceived clinician assistance increased during the transition from stance to swing. Intentional participation and 20% BWS resulted in timely and purposeful activation of the lower extremities muscles, which improved independence and decreased clinician assistance. Conclusion: Maximizing participant intention and optimizing proprioceptive inputs through BWS during ES-enabled BWST stepping may facilitate greater independence during BWST stepping for individuals with clinically complete SCI. Clinical Trial Registration: ClinicalTrials.gov identifier: NCT02592668. Frontiers Media S.A. 2021-01-28 /pmc/articles/PMC7875885/ /pubmed/33584209 http://dx.doi.org/10.3389/fnsys.2020.590231 Text en Copyright © 2021 Gill, Linde, Hale, Lopez, Fautsch, Calvert, Veith, Beck, Garlanger, Sayenko, Lavrov, Thoreson, Grahn and Zhao. http://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 Neuroscience
Gill, Megan L.
Linde, Margaux B.
Hale, Rena F.
Lopez, Cesar
Fautsch, Kalli J.
Calvert, Jonathan S.
Veith, Daniel D.
Beck, Lisa A.
Garlanger, Kristin L.
Sayenko, Dimitry G.
Lavrov, Igor A.
Thoreson, Andrew R.
Grahn, Peter J.
Zhao, Kristin D.
Alterations of Spinal Epidural Stimulation-Enabled Stepping by Descending Intentional Motor Commands and Proprioceptive Inputs in Humans With Spinal Cord Injury
title Alterations of Spinal Epidural Stimulation-Enabled Stepping by Descending Intentional Motor Commands and Proprioceptive Inputs in Humans With Spinal Cord Injury
title_full Alterations of Spinal Epidural Stimulation-Enabled Stepping by Descending Intentional Motor Commands and Proprioceptive Inputs in Humans With Spinal Cord Injury
title_fullStr Alterations of Spinal Epidural Stimulation-Enabled Stepping by Descending Intentional Motor Commands and Proprioceptive Inputs in Humans With Spinal Cord Injury
title_full_unstemmed Alterations of Spinal Epidural Stimulation-Enabled Stepping by Descending Intentional Motor Commands and Proprioceptive Inputs in Humans With Spinal Cord Injury
title_short Alterations of Spinal Epidural Stimulation-Enabled Stepping by Descending Intentional Motor Commands and Proprioceptive Inputs in Humans With Spinal Cord Injury
title_sort alterations of spinal epidural stimulation-enabled stepping by descending intentional motor commands and proprioceptive inputs in humans with spinal cord injury
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7875885/
https://www.ncbi.nlm.nih.gov/pubmed/33584209
http://dx.doi.org/10.3389/fnsys.2020.590231
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