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Corticospinal interface to restore voluntary control of joint torque in a paralyzed forearm following spinal cord injury in non-human primates

The corticospinal tract plays a major role in the control of voluntary limb movements, and its damage impedes voluntary limb control. We investigated the feasibility of closed-loop brain-controlled subdural spinal stimulation through a corticospinal interface for the modulation of wrist torque in th...

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Autores principales: Obara, Kei, Kaneshige, Miki, Suzuki, Michiaki, Yokoyama, Osamu, Tazoe, Toshiki, Nishimura, Yukio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10028188/
https://www.ncbi.nlm.nih.gov/pubmed/36960166
http://dx.doi.org/10.3389/fnins.2023.1127095
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author Obara, Kei
Kaneshige, Miki
Suzuki, Michiaki
Yokoyama, Osamu
Tazoe, Toshiki
Nishimura, Yukio
author_facet Obara, Kei
Kaneshige, Miki
Suzuki, Michiaki
Yokoyama, Osamu
Tazoe, Toshiki
Nishimura, Yukio
author_sort Obara, Kei
collection PubMed
description The corticospinal tract plays a major role in the control of voluntary limb movements, and its damage impedes voluntary limb control. We investigated the feasibility of closed-loop brain-controlled subdural spinal stimulation through a corticospinal interface for the modulation of wrist torque in the paralyzed forearm of monkeys with spinal cord injury at C4/C5. Subdural spinal stimulation of the preserved cervical enlargement activated multiple muscles on the paralyzed forearm and wrist torque in the range from flexion to ulnar-flexion. The magnitude of the evoked torque could be modulated by changing current intensity. We then employed the corticospinal interface designed to detect the firing rate of an arbitrarily selected “linked neuron” in the forearm territory of the primary motor cortex (M1) and convert it in real time to activity-contingent electrical stimulation of a spinal site caudal to the lesion. Linked neurons showed task-related activity that modulated the magnitude of the evoked torque and the activation of multiple muscles depending on the required torque. Unlinked neurons, which were independent of spinal stimulation and located in the vicinity of the linked neurons, exhibited task-related or -unrelated activity. Thus, monkeys were able to modulate the wrist torque of the paralyzed forearm by modulating the firing rate of M1 neurons including unlinked and linked neurons via the corticospinal interface. These results suggest that the corticospinal interface can replace the function of the corticospinal tract after spinal cord injury.
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spelling pubmed-100281882023-03-22 Corticospinal interface to restore voluntary control of joint torque in a paralyzed forearm following spinal cord injury in non-human primates Obara, Kei Kaneshige, Miki Suzuki, Michiaki Yokoyama, Osamu Tazoe, Toshiki Nishimura, Yukio Front Neurosci Neuroscience The corticospinal tract plays a major role in the control of voluntary limb movements, and its damage impedes voluntary limb control. We investigated the feasibility of closed-loop brain-controlled subdural spinal stimulation through a corticospinal interface for the modulation of wrist torque in the paralyzed forearm of monkeys with spinal cord injury at C4/C5. Subdural spinal stimulation of the preserved cervical enlargement activated multiple muscles on the paralyzed forearm and wrist torque in the range from flexion to ulnar-flexion. The magnitude of the evoked torque could be modulated by changing current intensity. We then employed the corticospinal interface designed to detect the firing rate of an arbitrarily selected “linked neuron” in the forearm territory of the primary motor cortex (M1) and convert it in real time to activity-contingent electrical stimulation of a spinal site caudal to the lesion. Linked neurons showed task-related activity that modulated the magnitude of the evoked torque and the activation of multiple muscles depending on the required torque. Unlinked neurons, which were independent of spinal stimulation and located in the vicinity of the linked neurons, exhibited task-related or -unrelated activity. Thus, monkeys were able to modulate the wrist torque of the paralyzed forearm by modulating the firing rate of M1 neurons including unlinked and linked neurons via the corticospinal interface. These results suggest that the corticospinal interface can replace the function of the corticospinal tract after spinal cord injury. Frontiers Media S.A. 2023-03-07 /pmc/articles/PMC10028188/ /pubmed/36960166 http://dx.doi.org/10.3389/fnins.2023.1127095 Text en Copyright © 2023 Obara, Kaneshige, Suzuki, Yokoyama, Tazoe and Nishimura. 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 Neuroscience
Obara, Kei
Kaneshige, Miki
Suzuki, Michiaki
Yokoyama, Osamu
Tazoe, Toshiki
Nishimura, Yukio
Corticospinal interface to restore voluntary control of joint torque in a paralyzed forearm following spinal cord injury in non-human primates
title Corticospinal interface to restore voluntary control of joint torque in a paralyzed forearm following spinal cord injury in non-human primates
title_full Corticospinal interface to restore voluntary control of joint torque in a paralyzed forearm following spinal cord injury in non-human primates
title_fullStr Corticospinal interface to restore voluntary control of joint torque in a paralyzed forearm following spinal cord injury in non-human primates
title_full_unstemmed Corticospinal interface to restore voluntary control of joint torque in a paralyzed forearm following spinal cord injury in non-human primates
title_short Corticospinal interface to restore voluntary control of joint torque in a paralyzed forearm following spinal cord injury in non-human primates
title_sort corticospinal interface to restore voluntary control of joint torque in a paralyzed forearm following spinal cord injury in non-human primates
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10028188/
https://www.ncbi.nlm.nih.gov/pubmed/36960166
http://dx.doi.org/10.3389/fnins.2023.1127095
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