Dimitry G. Sayenko

Neuromodulation of evoked muscle potentials induced by epidural spinal-cord stimulation in paralyzed individuals

Epidural stimulation (ES) of the lumbosacral spinal cord has been used to facilitate standing and voluntary movement after clinically motor-complete spinal-cord injury. It seems of importance to examine how the epidurally evoked potentials are modulated in the spinal circuitry and projected to various motor pools. We hypothesized that chronically implanted electrode arrays over the lumbosacral spinal cord can be used to assess functionally spinal circuitry linked to specific motor pools. The purpose of this study was to investigate the functional and topographic organization of compound evoked potentials induced by the stimulation. Three individuals with complete motor paralysis of the lower limbs participated in the study. The evoked potentials to epidural spinal stimulation were investigated after surgery in a supine position and in one participant, during both supine and standing, with body weight load of 60%. The stimulation was delivered with intensity from 0.5 to 10 V at a frequency of 2 Hz. Recruitment curves of evoked potentials in knee and ankle muscles were collected at three localized and two wide-field stimulation configurations. Epidural electrical stimulation of rostral and caudal areas of lumbar spinal cord resulted in a selective topographical recruitment of proximal and distal leg muscles, as revealed by both magnitude and thresholds of the evoked potentials. ES activated both afferent and efferent pathways. The components of neural pathways that can mediate motor-evoked potentials were highly dependent on the stimulation parameters and sensory conditions, suggesting a weight-bearing-induced reorganization of the spinal circuitries.

Acute effects of whole body vibration during passive standing on soleus H-reflex in subjects with and without spinal cord injury

Whole-body vibration (WBV) is being used to enhance neuromuscular performance including muscle strength, power, and endurance in many settings among diverse patient groups including elite athletes. However, the mechanisms underlying the observed neuromuscular effects of WBV have not been established. The extent to which WBV will produce similar neuromuscular effects among patients with neurological impairments unable to voluntarily contract their lower extremity muscles is unknown. We hypothesized that modulation of spinal motorneuronal excitability during WBV may be achieved without voluntary contraction. The purpose of our study was to describe and compare the acute effects of WBV during passive standing in a standing frame on the soleus H-reflex among men with and without spinal cord injury (SCI). In spinal cord intact participants, WBV caused significant inhibition of the H-reflex as early as 6s after vibration onset (9.0+/-3.9%) (p<0.001). The magnitude of the H-reflex gradually recovered after WBV, but remained significantly below initial values until 36s post-WBV (57.5+/-22.0%) (p=0.01). Among participants with SCI, H-reflex inhibition was less pronounced with onset 24 s following WBV (54.2+/-18.7%) (p=0.03). The magnitude of the H-reflex fully recovered after 60s of WBV exposure. These results concur with prior reports of inhibitory effects of local vibration application on the H-reflex. Our results suggest that acute modulation of spinal motoneuronal excitability during WBV can be achieved in the absence of voluntary leg muscle contractions. Nonetheless, WBV has implications for rehabilitation service delivery through modulation of spinal motoneuronal excitability in individuals with SCI.

Positive effect of balance training with visual feedback on standing balance abilities in people with incomplete spinal cord injury

Objectives:(1) To evaluate the learning potential and performance improvements during standing balance training with visual feedback (VBT) in individuals with incomplete spinal cord injury (SCI) and (2) to determine whether standing static and dynamic stability during training-irrelevant tasks can be improved after the VBT.Setting:National Rehabilitation Center for Persons with Disabilities, Tokorozawa, Japan.Methods:Six participants with chronic motor and sensory incomplete SCI who were able to stand for at least 5 min without any form of assistive device performed the VBT, 3 days per week, for a total of 12 sessions. During the training, participants stood on a force platform and were instructed to shift their center of pressure in the indicated directions as represented by a cursor on a monitor. The performance and the rate of learning were monitored throughout the training period. Before and after the program, static and dynamic stability was assessed.Results:All participants showed substantial improvements in the scores, which varied between 236±94 and 130±14% of the initial values for different exercises. The balance performance during training-irrelevant tasks was significantly improved: for example, the area inside the stability zone after the training reached 221±86% of the pre-training values.Conclusion:Postural control can be enhanced in individuals with incomplete SCI using VBT. All participants showed substantial improvements during standing in both game performance and training-irrelevant tasks after the VBT.

Effects of balance training with visual feedback during mechanically unperturbed standing on postural corrective responses.

Evidence of a non-specific effect of balance training on postural control mechanisms suggests that balance training during mechanically unperturbed standing may improve postural corrective responses following external perturbations. The purpose of the present study was to examine kinematics of the trunk as well as muscular activity of the lower leg and paraspinal muscles during postural responses to support-surface rotations after short-term balance training. Experiments were performed in control (n=10) and experimental (n=11) groups. The experimental group participated in the 3-day balance training program. During the training, participants stood on a force platform and were instructed to voluntarily shift their center of pressure in indicated directions as represented by a cursor on a monitor. Postural perturbation tests were executed before and after the training period: the slow and fast 10° dorsiflexions were induced at angular velocities of approximately 50°s(-1) and 200°s(-1), respectively. In the experimental group, the amplitude of the trunk displacements during slow and fast perturbations was up to 33.4% and 26.7% lower, respectively, following the training. The magnitude of the muscular activity was reduced in both the early and late components of the response. The kinematic parameters and muscular responses did not change in the control group. The results suggest that balance training during unperturbed standing has the potential to improve postural corrective responses to unexpected balance perturbation through (1) improved neuromuscular coordination of the involved muscles and (2) adaptive neural modifications on the spinal and cortical levels facilitated by voluntary activity.

Differential effects of plantar cutaneous afferent excitation on soleus stretch and H-reflex

Previous studies have demonstrated that plantar cutaneous afferents can adjust motoneuron excitability, which may contribute significantly to the control of human posture and locomotion. However, the role of plantar cutaneous afferents in modulating the excitability of stretch and H‐reflex with respect to the location of their excitation remains unclear. In the present study, it was hypothesized that electrical stimulation delivered to the sole of the foot might be followed by modulation of spinal excitability that depends on: (1) the stimulation location and (2) the reflex studied. In these experiments, conditioned and unconditioned stretch and H‐reflexes were evoked in 16 healthy subjects in a seated position. Both reflexes were conditioned by non‐noxious electrical plantar cutaneous afferent stimulation at two different sites, the heel and metatarsal regions, at four different conditioning–test (CT) intervals. The conditioning stimulation delivered to the heel caused a significant facilitation of the soleus stretch reflex for all CT intervals, whereas the soleus H‐reflex had significant facilitation only at CT interval of 50 ms and significant inhibition at longer CT intervals. Stimulation delivered to the metatarsal region, however, resulted mainly in reduced stretch and H‐reflex sizes. This study extends the reported findings on the contribution of plantar cutaneous afferents within spinal interneuron reflex circuits as a function of their location and the reflex studied. Muscle Nerve, 2008

Spinal segment-specific transcutaneous stimulation differentially shapes activation pattern among motor pools in humans

Transcutaneous and epidural electrical spinal cord stimulation techniques are becoming more valuable as electrophysiological and clinical tools. Recently, we observed selective activation of proximal and distal motor pools during epidural spinal stimulation. In the present study, we hypothesized that the characteristics of recruitment curves obtained from leg muscles will reflect a relative preferential activation of proximal and distal motor pools based on their arrangement along the lumbosacral enlargement. The purpose was to describe the electrophysiological responses to transcutaneous stimulation in leg muscles innervated by motoneurons from different segmental levels. Stimulation delivered along the rostrocaudal axis of the lumbosacral enlargement in the supine position resulted in a selective topographical recruitment of proximal and distal leg muscles, as described by threshold intensity, slope of the recruitment curves, and plateau point intensity and magnitude. Relatively selective recruitment of proximal and distal motor pools can be titrated by optimizing the site and intensity level of stimulation to excite a given combination of motor pools. The slope of the recruitment of particular muscles allows characterization of the properties of afferents projecting to specific motoneuron pools, as well as to the type and size of the motoneurons. The location and intensity of transcutaneous spinal electrical stimulation are critical to target particular neural structures across different motor pools in investigation of specific neuromodulatory effects. Finally, the asymmetry in bilateral evoked potentials is inevitable and can be attributed to both anatomical and functional peculiarities of individual muscles or muscle groups.

What triggers the continuous muscle activity during upright standing

The ankle extensors play a dominant role in controlling the equilibrium during bipedal quiet standing. Their primary role is to resist the gravity toppling torque that pulls the body forward. The purpose of this study was to investigate whether the continuous muscle activity of the anti-gravity muscles during standing is triggered by the joint torque requirement for opposing the gravity toppling torque, rather than by the vertical load on the lower limbs. Healthy adults subjects stood on a force plate. The ankle torque, ankle angle, and electromyograms from the right lower leg muscles were measured. A ground-fixed support device was used to support the subject at his/her knees, without changing the posture from the free standing one. During the supported condition, which eliminates the ankle torque requirement while maintaining both the vertical load on the lower limbs and the natural upright standing posture, the plantarflexor activity was attenuated to the resting level. Also, this attenuated plantarflexor activity was found only in one side when the ipsilateral leg was supported. Our results suggest that the vertical load on the lower limb is not determinant for inducing the continuous muscle activity in the anti-gravity muscles, but that it depends on the required joint torque to oppose the gravity toppling torque.

Enabling Task-Specific Volitional Motor Functions via Spinal Cord Neuromodulation in a Human With Paraplegia

Abstract We report a case of chronic traumatic paraplegia in which epidural electrical stimulation (EES) of the lumbosacral spinal cord enabled (1) volitional control of task‐specific muscle activity, (2) volitional control of rhythmic muscle activity to produce steplike movements while side‐lying, (3) independent standing, and (4) while in a vertical position with body weight partially supported, voluntary control of steplike movements and rhythmic muscle activity. This is the first time that the application of EES enabled all of these tasks in the same patient within the first 2 weeks (8 stimulation sessions total) of EES therapy.

Effects of paired transcutaneous electrical stimulation delivered at single and dual sites over lumbosacral spinal cord.

It was demonstrated previously that transcutaneous electrical stimulation of multiple sites over the spinal cord is more effective in inducing robust locomotor behavior as compared to the stimulation of single sites alone in both animal and human models. To explore the effects and mechanisms of interactions during multi-site spinal cord stimulation we delivered transcutaneous electrical stimulation to the single or dual locations over the spinal cord corresponding to approximately L2 and S1 segments. Spinally evoked motor potentials in the leg muscles were investigated using single and paired pulses of 1ms duration with conditioning-test intervals (CTIs) of 5 and 50ms. We observed considerable post-stimulation modulatory effects which depended on CTIs, as well as on whether the paired stimuli were delivered at a single or dual locations, the rostro-caudal relation between the conditioning and test stimuli, and on the muscle studied. At CTI-5, the paired stimulation delivered at single locations (L2 or S1) provided strong inhibitory effects, evidenced by the attenuation of the compound responses as compared with responses from either single site. In contrast, during L2-S1 paradigm, the compound responses were potentiated. At CTI-50, the magnitude of inhibition did not differ among paired stimulation paradigms. Our results suggest that electrical stimuli delivered to dual sites over the lumbosacral enlargement in rostral-to-caudal order, may recruit different populations of motor neurons initially through projecting sensory and intraspinal connections and then directly, resulting in potentiation of the compound spinally evoked motor potentials. The interactive and synergistic effects indicate multi-segmental convergence of descending and ascending influences on the neuronal circuitries during electrical spinal cord stimulation.

Weight Bearing Over-ground Stepping in an Exoskeleton with Non-invasive Spinal Cord Neuromodulation after Motor Complete Paraplegia

We asked whether coordinated voluntary movement of the lower limbs could be regained in an individual having been completely paralyzed (>4 year) and completely absent of vision (>15 year) using two novel strategies—transcutaneous electrical spinal cord stimulation at selected sites over the spine as well as pharmacological neuromodulation by buspirone. We also asked whether these neuromodulatory strategies could facilitate stepping assisted by an exoskeleton (EKSO, EKSO Bionics, CA) that is designed so that the subject can voluntarily complement the work being performed by the exoskeleton. We found that spinal cord stimulation and drug enhanced the level of effort that the subject could generate while stepping in the exoskeleton. In addition, stimulation improved the coordination patterns of the lower limb muscles resulting in a more continuous, smooth stepping motion in the exoskeleton along with changes in autonomic functions including cardiovascular and thermoregulation. Based on these data from this case study it appears that there is considerable potential for positive synergistic effects after complete paralysis by combining the over-ground step training in an exoskeleton, combined with transcutaneous electrical spinal cord stimulation either without or with pharmacological modulation.