Interfacing With Alpha Motor Neurons in Spinal Cord Injury Patients Receiving Trans-spinal Electrical Stimulation

Trans-spinal direct current stimulation (tsDCS) provides a non-invasive, clinically viable approach to potentially restore physiological neuromuscular function after neurological impairment, e.g., spinal cord injury (SCI). Use of tsDCS has been hampered by the inability of delivering stimulation pat...

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Main Authors: Antonio Gogeascoechea, Alexander Kuck, Edwin van Asseldonk, Francesco Negro, Jan R. Buitenweg, Utku S. Yavuz, Massimo Sartori
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fneur.2020.00493/full
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author Antonio Gogeascoechea
Alexander Kuck
Edwin van Asseldonk
Francesco Negro
Jan R. Buitenweg
Utku S. Yavuz
Massimo Sartori
author_facet Antonio Gogeascoechea
Alexander Kuck
Edwin van Asseldonk
Francesco Negro
Jan R. Buitenweg
Utku S. Yavuz
Massimo Sartori
author_sort Antonio Gogeascoechea
collection DOAJ
description Trans-spinal direct current stimulation (tsDCS) provides a non-invasive, clinically viable approach to potentially restore physiological neuromuscular function after neurological impairment, e.g., spinal cord injury (SCI). Use of tsDCS has been hampered by the inability of delivering stimulation patterns based on the activity of neural targets responsible to motor function, i.e., α-motor neurons (α-MNs). State of the art modeling and experimental techniques do not provide information about how individual α-MNs respond to electrical fields. This is a major element hindering the development of neuro-modulative technologies highly tailored to an individual patient. For the first time, we propose the use of a signal-based approach to infer tsDCS effects on large α-MNs pools in four incomplete SCI individuals. We employ leg muscles spatial sampling and deconvolution of high-density fiber electrical activity to decode accurate α-MNs discharges across multiple lumbosacral segments during isometric plantar flexion sub-maximal contractions. This is done before, immediately after and 30 min after sub-threshold cathodal stimulation. We deliver sham tsDCS as a control measure. First, we propose a new algorithm for removing compromised information from decomposed α-MNs spike trains, thereby enabling robust decomposition and frequency-domain analysis. Second, we propose the analysis of α-MNs spike trains coherence (i.e., frequency-domain) as an indicator of spinal response to tsDCS. Results showed that α-MNs spike trains coherence analysis sensibly varied across stimulation phases. Coherence analyses results suggested that the common synaptic input to α-MNs pools decreased immediately after cathodal tsDCS with a persistent effect after 30 min. Our proposed non-invasive decoding of individual α-MNs behavior may open up new avenues for the design of real-time closed-loop control applications including both transcutaneous and epidural spinal electrical stimulation where stimulation parameters are adjusted on-the-fly.
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spelling doaj.art-ebfe082310a84e29bcf70a88f1939c8e2022-12-22T01:17:37ZengFrontiers Media S.A.Frontiers in Neurology1664-22952020-06-011110.3389/fneur.2020.00493528464Interfacing With Alpha Motor Neurons in Spinal Cord Injury Patients Receiving Trans-spinal Electrical StimulationAntonio Gogeascoechea0Alexander Kuck1Edwin van Asseldonk2Francesco Negro3Jan R. Buitenweg4Utku S. Yavuz5Massimo Sartori6Department of Biomechanical Engineering, University of Twente, Enschede, NetherlandsDepartment of Biomechanical Engineering, University of Twente, Enschede, NetherlandsDepartment of Biomechanical Engineering, University of Twente, Enschede, NetherlandsDepartment of Clinical and Experimental Sciences, Università degli Studi di Brescia, Brescia, ItalyBiomedical Signals and Systems Group, University of Twente, Enschede, NetherlandsBiomedical Signals and Systems Group, University of Twente, Enschede, NetherlandsDepartment of Biomechanical Engineering, University of Twente, Enschede, NetherlandsTrans-spinal direct current stimulation (tsDCS) provides a non-invasive, clinically viable approach to potentially restore physiological neuromuscular function after neurological impairment, e.g., spinal cord injury (SCI). Use of tsDCS has been hampered by the inability of delivering stimulation patterns based on the activity of neural targets responsible to motor function, i.e., α-motor neurons (α-MNs). State of the art modeling and experimental techniques do not provide information about how individual α-MNs respond to electrical fields. This is a major element hindering the development of neuro-modulative technologies highly tailored to an individual patient. For the first time, we propose the use of a signal-based approach to infer tsDCS effects on large α-MNs pools in four incomplete SCI individuals. We employ leg muscles spatial sampling and deconvolution of high-density fiber electrical activity to decode accurate α-MNs discharges across multiple lumbosacral segments during isometric plantar flexion sub-maximal contractions. This is done before, immediately after and 30 min after sub-threshold cathodal stimulation. We deliver sham tsDCS as a control measure. First, we propose a new algorithm for removing compromised information from decomposed α-MNs spike trains, thereby enabling robust decomposition and frequency-domain analysis. Second, we propose the analysis of α-MNs spike trains coherence (i.e., frequency-domain) as an indicator of spinal response to tsDCS. Results showed that α-MNs spike trains coherence analysis sensibly varied across stimulation phases. Coherence analyses results suggested that the common synaptic input to α-MNs pools decreased immediately after cathodal tsDCS with a persistent effect after 30 min. Our proposed non-invasive decoding of individual α-MNs behavior may open up new avenues for the design of real-time closed-loop control applications including both transcutaneous and epidural spinal electrical stimulation where stimulation parameters are adjusted on-the-fly.https://www.frontiersin.org/article/10.3389/fneur.2020.00493/fullalpha motor neuroncoherencecommon synaptic inputhigh-density EMGspinal cord injurytrans-spinal direct current stimulation
spellingShingle Antonio Gogeascoechea
Alexander Kuck
Edwin van Asseldonk
Francesco Negro
Jan R. Buitenweg
Utku S. Yavuz
Massimo Sartori
Interfacing With Alpha Motor Neurons in Spinal Cord Injury Patients Receiving Trans-spinal Electrical Stimulation
Frontiers in Neurology
alpha motor neuron
coherence
common synaptic input
high-density EMG
spinal cord injury
trans-spinal direct current stimulation
title Interfacing With Alpha Motor Neurons in Spinal Cord Injury Patients Receiving Trans-spinal Electrical Stimulation
title_full Interfacing With Alpha Motor Neurons in Spinal Cord Injury Patients Receiving Trans-spinal Electrical Stimulation
title_fullStr Interfacing With Alpha Motor Neurons in Spinal Cord Injury Patients Receiving Trans-spinal Electrical Stimulation
title_full_unstemmed Interfacing With Alpha Motor Neurons in Spinal Cord Injury Patients Receiving Trans-spinal Electrical Stimulation
title_short Interfacing With Alpha Motor Neurons in Spinal Cord Injury Patients Receiving Trans-spinal Electrical Stimulation
title_sort interfacing with alpha motor neurons in spinal cord injury patients receiving trans spinal electrical stimulation
topic alpha motor neuron
coherence
common synaptic input
high-density EMG
spinal cord injury
trans-spinal direct current stimulation
url https://www.frontiersin.org/article/10.3389/fneur.2020.00493/full
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