Vestibulospinal and Corticospinal Modulation of Lumbosacral Network Excitability in Human Subjects

As part of a project aimed to develop a novel, non-invasive techniques for comprehensive assessment of supraspinal-spinal connectivity in humans, the present study sought to explore the convergence of descending vestibulospinal and corticospinal pathways onto lumbosacral motor pools. Transcutaneous electrical spinal stimulation-evoked motor potentials were recorded from knee and ankle flexors and extensors in resting neurologically intact participants. Descending influences on lumbosacral motor neurons were studied using galvanic vestibular (GVS) or transcranial magnetic stimulation (TMS) to elicit descending vestibulospinal or corticospinal volleys, respectively. Facilitatory conditioning effects of descending corticospinal volleys were manifested by a significant increase of spinally evoked motor potentials in recorded knee and ankle muscles bilaterally, and were observed at the 10–30 ms conditioning-test intervals (CTIs); whereas, facilitatory conditioning effects of vestibulospinal volleys manifested at longer latencies (CTIs of 90 and 110 ms), and lasted up to 250 ms. TMS mediated volleys revealed the conditioning effects at both short and long latencies, suggestive of both direct and indirect influence. In contrast, vestibulospinally mediated conditioning effects occurred at longer latencies, consistent with this pathway’s known anatomical and functional interfaces with other descending systems including the reticulospinal pathway and, suggestively, propriospinal interneurons. Our work demonstrates the utility and sensitivity of transcutaneous spinal stimulation in human neurophysiological studies as a technique for quantitative characterization of excitatory conditioning effects in multiple lumbosacral motor pools, obtained through descending pathways. This characterization becomes critical in understanding the neuroplasticity in the central nervous system during motor learning and neurological recovery

Electrophysiological Guidance of Epidural Electrode Array Implantation over the Human Lumbosacral Spinal Cord to Enable Motor Function after Chronic Paralysis.

Epidural electrical stimulation (EES) of the spinal cord has been shown to restore function after spinal cord injury (SCI). Characterization of EES-evoked motor responses has provided a basic understanding of spinal sensorimotor network activity related to EES-enabled motor activity of the lower extremities. However, the use of EES-evoked motor responses to guide EES system implantation over the spinal cord and their relation to post-operative EES-enabled function in humans with chronic paralysis attributed to SCI has yet to be described. Herein, we describe the surgical and intraoperative electrophysiological approach used, followed by initial EES-enabled results observed in 2 human subjects with motor complete paralysis who were enrolled in a clinical trial investigating the use of EES to enable motor functions after SCI. The 16-contact electrode array was initially positioned under fluoroscopic guidance. Then, EES-evoked motor responses were recorded from select leg muscles and displayed in real time to determine electrode array proximity to spinal cord regions associated with motor activity of the lower extremities. Acceptable array positioning was determined based on achievement of selective proximal or distal leg muscle activity, as well as bilateral muscle activation. Motor response latencies were not significantly different between intraoperative recordings and post-operative recordings, indicating that array positioning remained stable. Additionally, EES enabled intentional control of step-like activity in both subjects within the first 5 days of testing. These results suggest that the use of EES-evoked motor responses may guide intraoperative positioning of epidural electrodes to target spinal cord circuitry to enable motor functions after SCI

Reducing muscle fatigue during transcutaneous neuromuscular electrical stimulation by spatially and sequentially distributing electrical stimulation sources

Purpose: A critical limitation with transcutaneous neuromuscular electrical stimulation is the rapid onset of muscle fatigue. We have previously demonstrated that spatially distributed sequential stimulation (SDSS) shows a drastically greater fatigue-reducing ability compared to a single active electrode stimulation (SES). The purposes of this study were to investigate (1) the fatigue-reducing ability of SDSS in more detail focusing on the muscle contractile properties and (2) the mechanism of this effect using array-arranged electromyogram (EMG). Methods: SDSS was delivered through four active electrodes applied to the plantarflexors, sending a stimulation pulse to each electrode one after another with 90° phase shift between successive electrodes. In the first experiment, the amount of exerted ankle torque and the muscle contractile properties were investigated during a 3 min fatiguing stimulation. In the second experiment, muscle twitch potentials with SDSS and SES stimulation electrode setups were compared using the array-arranged EMG. Results: The results demonstrated negligible torque decay during SDSS in contrast to considerable torque decay during SES. Moreover, small changes in the muscle contractile properties during the fatiguing stimulation using SDSS were observed, while slowing of muscle contraction and relaxation was observed during SES. Further, the amplitude of the M-waves at each muscle portion was dependent on the location of the stimulation electrodes during SDSS. Conclusion: We conclude that SDSS is more effective in reducing muscle fatigue compared to SES, and the reason is that different sets of muscle fibers are activated alternatively by different electrodes.ISSN:1439-6319ISSN:1439-632

Method to reduce muscle fatigue during transcutaneous neuromuscular electrical stimulation in major knee and ankle muscle groups

Background: A critical limitation with transcutaneous neuromuscular electrical stimulation as a rehabilitative approach is the rapid onset of muscle fatigue during repeated contractions. We have developed a method called spatially distributed sequential stimulation (SDSS) to reduce muscle fatigue by distributing the center of electrical field over a wide area within a single stimulation site, using an array of surface electrodes. Objective: To extend the previous findings and to prove feasibility of the method by exploring the fatigue-reducing ability of SDSS for lower limb muscle groups in the able-bodied population, as well as in individuals with spinal cord injury (SCI). Methods: SDSS was delivered through four active electrodes applied to the knee extensors and flexors, plantarflexors, and dorsiflexors, sending a stimulation pulse to each electrode one after another with 90° phase shift between successive electrodes. Isometric ankle torque was measured during fatiguing stimulations using SDSS and conventional single active electrode stimulation lasting 2 min. Results: We demonstrated greater fatigue-reducing ability of SDSS compared to the conventional protocol, as revealed by larger values of fatigue index and/or torque peak mean in all muscles except knee flexors of able-bodied individuals, and in all muscles tested in individuals with SCI. Conclusions: Our study has revealed improvements in fatigue tolerance during transcutaneous neuromuscular electrical stimulation using SDSS, a stimulation strategy that alternates activation of subcompartments of muscles. The SDSS protocol can provide greater stimulation times with less decrement in mechanical output compared to the conventional protocol

Characterization of Spinal Sensorimotor Network Using Transcutaneous Spinal Stimulation during Voluntary Movement Preparation and Performance

Transcutaneous electrical spinal stimulation (TSS) can be used to selectively activate motor pools based on their anatomical arrangements in the lumbosacral enlargement. These spatial patterns of spinal motor activation may have important clinical implications, especially when there is a need to target specific muscle groups. However, our understanding of the net effects and interplay between the motor pools projecting to agonist and antagonist muscles during the preparation and performance of voluntary movements is still limited. The present study was designed to systematically investigate and differentiate the multi-segmental convergence of supraspinal inputs on the lumbosacral neural network before and during the execution of voluntary leg movements in neurologically intact participants. During the experiments, participants (N = 13) performed isometric (1) knee flexion and (2) extension, as well as (3) plantarflexion and (4) dorsiflexion. TSS consisting of a pair pulse with 50 ms interstimulus interval was delivered over the T12-L1 vertebrae during the muscle contractions, as well as within 50 to 250 ms following the auditory or tactile stimuli, to characterize the temporal profiles of net spinal motor output during movement preparation. Facilitation of evoked motor potentials in the ipsilateral agonists and contralateral antagonists emerged as early as 50 ms following the cue and increased prior to movement onset. These results suggest that the descending drive modulates the activity of the inter-neuronal circuitry within spinal sensorimotor networks in specific, functionally relevant spatiotemporal patterns, which has a direct implication for the characterization of the state of those networks in individuals with neurological conditions

An Autonomic Neuroprosthesis: Noninvasive Electrical Spinal Cord Stimulation Restores Autonomic Cardiovascular Function in Individuals with Spinal Cord Injury.

Despite autonomic dysfunction after spinal cord injury (SCI) being the major cause of death and a top health priority, the clinical management options for these conditions are limited to drugs with delayed onset and nonpharmacological interventions with equivocal effectiveness. We tested the capacity of electrical stimulation, applied transcutaneously over the spinal cord, to manage autonomic dysfunction in the form of orthostatic hypotension after SCI. We assessed beat-by-beat blood pressure (BP), stroke volume, and cardiac contractility (dP/dt; Finometer), as well as cerebral blood flow (transcranial Doppler) in 5 individuals with motor-complete SCI (4 cervical, 1 thoracic) during an orthostatic challenge with and without transcutaneous electrical stimulation applied at the TVII level. During the orthostatic challenge, all individuals experienced hypotension characterized by a 37 ± 4 mm Hg decrease in systolic BP, a 52 ± 10% reduction in cardiac contractility, and a 23 ± 6% reduction in cerebral blood flow (all p < 0.05), along with severe self-reported symptoms. Electrical stimulation completely normalized BP, cardiac contractility, cerebral blood flow, and abrogated all symptoms. Noninvasive transcutaneous electrical spinal cord stimulation may be a viable therapy for restoring autonomic cardiovascular control after SCI

Action possibility judgments of people with varying motor abilities due to spinal cord injury.

Predictions about one's own action capabilities as well as the action capabilities of others are thought to be based on a simulation process involving linked perceptual and motor networks. Given the central role of motor experience in the formation of these networks, one's present motor capabilities are thought to be the basis of their perceptual judgments about actions. However, it remains unknown whether the ability to form these action possibility judgments is affected by performance related changes in the motor system. To determine if judgments of action capabilities are affected by long-term changes in one's own motor capabilities, participants with different degrees of upper-limb function due to their level (cervical vs. below cervical) of spinal cord injury (SCI) were tested on a perceptual-motor judgment task. Participants observed apparent motion videos of reciprocal aiming movements with varying levels of difficulty. For each movement, participants determined the shortest movement time (MT) at which they themselves and a young adult could perform the task while maintaining accuracy. Participants also performed the task. Analyses of MTs revealed that perceptual judgments for participant's own movement capabilities were consistent with their actual performance- people with cervical SCI had longer judged and actual MTs than people with below cervical SCI. However, there were no between-group differences in judged MTs for the young adult. Although it is unclear how the judgments were adjusted (altered simulation vs. threshold modification), the data reveal that people with different motor capabilities due to SCI are not completely biased by their present capabilities and can effectively adjust their judgments to estimate the actions of others