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

Megan L Gill, Margaux B Linde, Rena F Hale, Cesar Lopez, Kalli J Fautsch, Jonathan S Calvert, Daniel D Veith, Lisa A Beck, Kristin L Garlanger, Dimitry G Sayenko, Igor A Lavrov, Andrew R Thoreson, Peter J Grahn, Kristin D Zhao, Megan L Gill, Margaux B Linde, Rena F Hale, Cesar Lopez, Kalli J Fautsch, Jonathan S Calvert, Daniel D Veith, Lisa A Beck, Kristin L Garlanger, Dimitry G Sayenko, Igor A Lavrov, Andrew R Thoreson, Peter J Grahn, Kristin D Zhao

Abstract

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.

Keywords: body weight supported stepping; epidural spinal stimulation; multi- modal rehabilitation; paralysis; spinal cord injury; spinal neuromodulation; task-specific training.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Gill, Linde, Hale, Lopez, Fautsch, Calvert, Veith, Beck, Garlanger, Sayenko, Lavrov, Thoreson, Grahn and Zhao.

Figures

Figure 1
Figure 1
Visual description of transition from stance to swing during BWST stepping (A). Red limb indicates inadequate movement of the limb during swing phase demonstrating increased knee extension during toe off and toe drag during mid swing. An exemplary vGRF trace during one step cycle demonstrating increased difficulty transitioning from stance to swing with oscillatory force pattern representing toe drag (B). Box represents the time during the gait cycle where assistance level increased as perceived by the clinicians assistance level increased as perceived by the clinicians. During the transition from stance to swing, clinician assistance facilitation technique increased during passive and 60% BWS stepping conditions compared to active and 20% BWS stepping (C). Image used in Panel A was created by Mayo Clinic's Medical Illustration Department.
Figure 2
Figure 2
Participant 1(right limb) and participant 2 (left limb), mean ± SD vGRF during passive (solid line) and active (dashed line) stepping across the gait cycle. Vertical lines represent transition from stance to swing for each respective condition. Boxes represent time during the gait cycle where assistance level increased as perceive by the clinicians.
Figure 3
Figure 3
Participant 1 (right limb) and participant 2 (left limb), mean ± SD RMS values of rectus femoris (RF) and vastus lateralis (VL) results separated by stance and swing phase (dashed line) during passive (dark gray) and active (light gray) stepping. Error bars represent one standard deviation. Asterisk denotes P < 0.01.
Figure 4
Figure 4
Participant 1 (right limb) and participant 2 (left limb), mean ± SD electromyography activation of the rectus femoris (RF) and vastus lateralis (VL) for Participant 1 and Participant 2 during passive (dark gray) and active (light gray) stepping conditions. Vertical lines represent transition from stance to swing for each respective condition. Boxes represent time during the gait cycle were clinicians perceived an increase in the level of assistance.
Figure 5
Figure 5
Participant 1 (right limb) and participant 2 (left limb), mean ± SD vGRF during 60% (solid line) and 20% (dashed line) BWS stepping across the gait cycle. Vertical lines represent transition from stance to swing for each respective condition. Boxes represent time during the gait cycle where clinicians perceived an increase in the level of assistance.
Figure 6
Figure 6
Participant 1 (right limb) and participant 2 (left limb), mean ± SD RMS values of rectus femoris (RF) and vastus lateralis (VL) results separated by stance and swing phase (dashed line) during 60% (dark gray) and 20% (light gray) BWS stepping. Error bars represent one standard deviation. Asterisk denotes P < 0.01.
Figure 7
Figure 7
Participant 1 (right limb) and participant (left limb), mean ± SD electromyography activation of the rectus femoris (RF) and vastus lateralis (VL) during 60% (dark gray) and 20% (light gray) BWS stepping conditions. Vertical lines represent transition from stance to swing for each respective condition. Boxes represent time during the gait cycle were clinicians perceived an increase in the level of assistance.

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