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

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.

Spinal cord imaging markers and recovery of standing with epidural stimulation in individuals with clinically motor complete spinal cord injury

“…However, unexpected recovery of volitional lower limb movement with scES in supine position was also observed in individuals with clinically motor complete SCI (Harkema et al 2011;Angeli et al 2014). Our research group and others subsequently showed that supraspinal inputs can also be integrated by the spinal circuitry together with peripheral sensory information during weight-bearing standing and stepping, modulating the motor pattern promoted by scES (Angeli et al 2014;Grahn et al 2017;Rejc and Angeli 2019;Gill et al 2020). Volitional intent to contribute to motor pattern generation was a key component in the recovery of walking in individuals with motor complete SCI (Angeli et al 2018;Gill et al 2018).…”

Quantitative Assessment of Clinician Assistance During Dynamic Rehabilitation Using Force Sensitive Resistors

“…Each gait cycle duration was identified by Tekscan in-shoe sensors. The stance and swing phase of the gait cycle were identified similar to our previous publication (7). The duration of the applied force was identified through FSRs and a minimum threshold of 5 N determined initiation and termination of assistance.…”

Voluntary Modulation of Evoked Responses Generated by Epidural and Transcutaneous Spinal Stimulation in Humans with Spinal Cord Injury

“…Study participants sustained an SCI at least two years prior to study enrollment. Two study participants were part of a study at the Mayo Clinic whose functional motor responses have previously been reported [ 4 , 7 , 13 , 30 , 31 ]. These publications focused on motor outputs during functional tasks such as voluntary control of lower-extremity muscles, stepping, standing, and sitting [ 7 , 13 , 30 , 31 ], as well as intraoperative recordings [ 4 ].…”

“…Two study participants were part of a study at the Mayo Clinic whose functional motor responses have previously been reported [ 4 , 7 , 13 , 30 , 31 ]. These publications focused on motor outputs during functional tasks such as voluntary control of lower-extremity muscles, stepping, standing, and sitting [ 7 , 13 , 30 , 31 ], as well as intraoperative recordings [ 4 ]. All data and analyses from these participants in this report were recorded at low (0.2–2 Hz) non-functional stimulation frequencies while the subjects were supine.…”