Epidural combined optical and electrical stimulation induces high-specificity activation of target muscles in spinal cord injured rats

IntroductionEpidural electrical stimulation (EES) has been shown to improve motor dysfunction after spinal cord injury (SCI) by activating residual locomotor neural networks. However, the stimulation current often spreads excessively, leading to activation of non-target muscles and reducing the accu...

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Main Authors: Xiao-Jun Guo, Ziyi Zhao, Jia-Qi Chang, Le-Wei He, Wen-Nan Su, Ting Feng, Can Zhao, Meng Xu, Jia-Sheng Rao
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-11-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2023.1282558/full
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author Xiao-Jun Guo
Ziyi Zhao
Jia-Qi Chang
Le-Wei He
Wen-Nan Su
Ting Feng
Can Zhao
Meng Xu
Jia-Sheng Rao
author_facet Xiao-Jun Guo
Ziyi Zhao
Jia-Qi Chang
Le-Wei He
Wen-Nan Su
Ting Feng
Can Zhao
Meng Xu
Jia-Sheng Rao
author_sort Xiao-Jun Guo
collection DOAJ
description IntroductionEpidural electrical stimulation (EES) has been shown to improve motor dysfunction after spinal cord injury (SCI) by activating residual locomotor neural networks. However, the stimulation current often spreads excessively, leading to activation of non-target muscles and reducing the accuracy of stimulation regulation.ObjectivesNear-infrared nerve stimulation (nINS) was combined with EES to explore its regulatory effect on lower limb muscle activity in spinal-cord-transected rats.MethodsIn this study, stimulation electrodes were implanted into the rats’ L3–L6 spinal cord segment with T8 cord transected. Firstly, a series of EES parameters (0.2–0.6 mA and 20–60 Hz) were tested to determine those that specifically regulate the tibialis anterior (TA) and medial gastrocnemius (MG). Subsequently, to determine the effect of combined optical and electrical stimulation, near-infrared laser with a wavelength of 808 nm was used to irradiate the L3–L6 spinal cord segment while EES was performed. The amplitude of electromyography (EMG), the specific activation intensity of the target muscle, and the minimum stimulus current intensity to induce joint movement (motor threshold) under a series of optical stimulation parameters (power: 0.0–2.0 W; pulse width: 0–10 ms) were investigated and analyzed.ResultsEES stimulation with 40 Hz at the L3 and L6 spinal cord segments specifically activated TA and MG, respectively. High stimulation intensity (>2 × motor threshold) activated non-target muscles, while low stimulation frequency (<20 Hz) produced intermittent contraction. Compared to electrical stimulation alone (0.577 ± 0.081 mV), the combined stimulation strategy could induce stronger EMG amplitude of MG (1.426 ± 0.365 mV) after spinal cord injury (p < 0.01). The combined application of nINS effectively decreased the EES-induced motor threshold of MG (from 0.237 ± 0.001 mA to 0.166 ± 0.028 mA, p < 0.001). Additionally, the pulse width (PW) of nINS had a slight impact on the regulation of muscle activity. The EMG amplitude of MG only increased by ~70% (from 3.978 ± 0.240 mV to 6.753 ± 0.263 mV) when the PW increased by 10-fold (from 1 to 10 ms).ConclusionThe study demonstrates the feasibility of epidural combined electrical and optical stimulation for highly specific regulation of muscle activity after SCI, and provides a new strategy for improving motor dysfunction caused by SCI.
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spelling doaj.art-92c5b89a0e1d447e94047cd90ea1642d2023-11-13T09:56:10ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-11-011710.3389/fnins.2023.12825581282558Epidural combined optical and electrical stimulation induces high-specificity activation of target muscles in spinal cord injured ratsXiao-Jun Guo0Ziyi Zhao1Jia-Qi Chang2Le-Wei He3Wen-Nan Su4Ting Feng5Can Zhao6Meng Xu7Jia-Sheng Rao8Beijing Key Laboratory for Biomaterials and Neural Regeneration, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, ChinaDepartment of Orthopedics, The First Medical Center of PLA General Hospital, Beijing, ChinaSmart Fluid Equipment and Manufacture Lab, School of Automation Science and Electrical Engineering, Beihang Univeristy, Beijing, ChinaBeijing Key Laboratory for Biomaterials and Neural Regeneration, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, ChinaBeijing Key Laboratory for Biomaterials and Neural Regeneration, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, ChinaBeijing Key Laboratory for Biomaterials and Neural Regeneration, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, ChinaInstitute of Rehabilitation Engineering, China Rehabilitation Science Institute, Beijing, ChinaDepartment of Orthopedics, The First Medical Center of PLA General Hospital, Beijing, ChinaBeijing Key Laboratory for Biomaterials and Neural Regeneration, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, ChinaIntroductionEpidural electrical stimulation (EES) has been shown to improve motor dysfunction after spinal cord injury (SCI) by activating residual locomotor neural networks. However, the stimulation current often spreads excessively, leading to activation of non-target muscles and reducing the accuracy of stimulation regulation.ObjectivesNear-infrared nerve stimulation (nINS) was combined with EES to explore its regulatory effect on lower limb muscle activity in spinal-cord-transected rats.MethodsIn this study, stimulation electrodes were implanted into the rats’ L3–L6 spinal cord segment with T8 cord transected. Firstly, a series of EES parameters (0.2–0.6 mA and 20–60 Hz) were tested to determine those that specifically regulate the tibialis anterior (TA) and medial gastrocnemius (MG). Subsequently, to determine the effect of combined optical and electrical stimulation, near-infrared laser with a wavelength of 808 nm was used to irradiate the L3–L6 spinal cord segment while EES was performed. The amplitude of electromyography (EMG), the specific activation intensity of the target muscle, and the minimum stimulus current intensity to induce joint movement (motor threshold) under a series of optical stimulation parameters (power: 0.0–2.0 W; pulse width: 0–10 ms) were investigated and analyzed.ResultsEES stimulation with 40 Hz at the L3 and L6 spinal cord segments specifically activated TA and MG, respectively. High stimulation intensity (>2 × motor threshold) activated non-target muscles, while low stimulation frequency (<20 Hz) produced intermittent contraction. Compared to electrical stimulation alone (0.577 ± 0.081 mV), the combined stimulation strategy could induce stronger EMG amplitude of MG (1.426 ± 0.365 mV) after spinal cord injury (p < 0.01). The combined application of nINS effectively decreased the EES-induced motor threshold of MG (from 0.237 ± 0.001 mA to 0.166 ± 0.028 mA, p < 0.001). Additionally, the pulse width (PW) of nINS had a slight impact on the regulation of muscle activity. The EMG amplitude of MG only increased by ~70% (from 3.978 ± 0.240 mV to 6.753 ± 0.263 mV) when the PW increased by 10-fold (from 1 to 10 ms).ConclusionThe study demonstrates the feasibility of epidural combined electrical and optical stimulation for highly specific regulation of muscle activity after SCI, and provides a new strategy for improving motor dysfunction caused by SCI.https://www.frontiersin.org/articles/10.3389/fnins.2023.1282558/fullspinal cord injuryepidural electrical stimulationnear-infrared nerve stimulationmuscle activityneuromodulationmotor function
spellingShingle Xiao-Jun Guo
Ziyi Zhao
Jia-Qi Chang
Le-Wei He
Wen-Nan Su
Ting Feng
Can Zhao
Meng Xu
Jia-Sheng Rao
Epidural combined optical and electrical stimulation induces high-specificity activation of target muscles in spinal cord injured rats
Frontiers in Neuroscience
spinal cord injury
epidural electrical stimulation
near-infrared nerve stimulation
muscle activity
neuromodulation
motor function
title Epidural combined optical and electrical stimulation induces high-specificity activation of target muscles in spinal cord injured rats
title_full Epidural combined optical and electrical stimulation induces high-specificity activation of target muscles in spinal cord injured rats
title_fullStr Epidural combined optical and electrical stimulation induces high-specificity activation of target muscles in spinal cord injured rats
title_full_unstemmed Epidural combined optical and electrical stimulation induces high-specificity activation of target muscles in spinal cord injured rats
title_short Epidural combined optical and electrical stimulation induces high-specificity activation of target muscles in spinal cord injured rats
title_sort epidural combined optical and electrical stimulation induces high specificity activation of target muscles in spinal cord injured rats
topic spinal cord injury
epidural electrical stimulation
near-infrared nerve stimulation
muscle activity
neuromodulation
motor function
url https://www.frontiersin.org/articles/10.3389/fnins.2023.1282558/full
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