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

Xiao-Jun Guo; Ziyi Zhao; Jia-Qi Chang; Le-Wei He; Wen-Nan Su; Ting Feng; Can Zhao; Meng Xu; Jia-Sheng Rao

doi:10.3389/fnins.2023.1282558

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

Front Neurosci. 2023 Nov 10:17:1282558. doi: 10.3389/fnins.2023.1282558. eCollection 2023.

Authors

Xiao-Jun Guo^#¹, Ziyi Zhao^#², Jia-Qi Chang^#³, Le-Wei He¹, Wen-Nan Su¹, Ting Feng¹, Can Zhao⁴, Meng Xu², Jia-Sheng Rao¹

Affiliations

¹ Beijing Key Laboratory for Biomaterials and Neural Regeneration, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, China.
² Department of Orthopedics, The First Medical Center of PLA General Hospital, Beijing, China.
³ Smart Fluid Equipment and Manufacture Lab, School of Automation Science and Electrical Engineering, Beihang Univeristy, Beijing, China.
⁴ Institute of Rehabilitation Engineering, China Rehabilitation Science Institute, Beijing, China.

^# Contributed equally.

Abstract

Introduction: Epidural 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.

Objectives: Near-infrared nerve stimulation (nINS) was combined with EES to explore its regulatory effect on lower limb muscle activity in spinal-cord-transected rats.

Methods: In 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.

Results: EES 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).

Conclusion: The 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.

Keywords: epidural electrical stimulation; motor function; muscle activity; near-infrared nerve stimulation; neuromodulation; rehabilitation; spinal cord injury.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Natural Science Foundation of China (grant nos. 31970970 and 31900980), Fundamental Research Funds for Central Public Welfare Research Institutes (grant nos. 2021CZ-10 and 2022CZ-12), and Fundamental Research Funds for the Central Universities (grant no. YWF-23-YG-QB-010).