Robert A. Gaunt

Intracortical microstimulation of human somatosensory cortex

Tactile percepts were consistently elicited in the hand of a person with cervical spinal cord injury using intracortical microstimulation of the somatosensory cortex. A sense of touch Touch is essential for hand use. Yet, brain-controlled prosthetic limbs have not been endowed with this critical sense. In a new study by Flesher et al., microelectrode arrays were implanted into the primary somatosensory cortex of a person with spinal cord injury and, by delivering current through the electrodes, generated sensations of touch that were perceived as coming from his own paralyzed hand. These sensations often felt like pressure, could be graded in intensity, and were stable for months. The authors suggest that this approach could be used to convey information about contact location and pressure necessary for prosthetic hands to interact with objects. Intracortical microstimulation of the somatosensory cortex offers the potential for creating a sensory neuroprosthesis to restore tactile sensation. Whereas animal studies have suggested that both cutaneous and proprioceptive percepts can be evoked using this approach, the perceptual quality of the stimuli cannot be measured in these experiments. We show that microstimulation within the hand area of the somatosensory cortex of a person with long-term spinal cord injury evokes tactile sensations perceived as originating from locations on the hand and that cortical stimulation sites are organized according to expected somatotopic principles. Many of these percepts exhibit naturalistic characteristics (including feelings of pressure), can be evoked at low stimulation amplitudes, and remain stable for months. Further, modulating the stimulus amplitude grades the perceptual intensity of the stimuli, suggesting that intracortical microstimulation could be used to convey information about the contact location and pressure necessary to perform dexterous hand movements associated with object manipulation.

Control of urinary bladder function with devices: successes and failures

The management of urinary tract dysfunction is crucial for the health and well-being of people with spinal cord injury. Devices, specifically catheters, play an important role in the daily regime of bladder management for most people with spinal cord injury. However, the high incidence of complications associated with the use of catheters, and the fact that the spinal segments involved in lower urinary tract control remain intact in most cord-injured people, continue to motivate research into devices that could harness the nervous system to provide greater control over lower urinary tract function. Mechanical devices discussed in this review include catheters, artificial urethral sphincters, urethral stents and intraurethral pumps. Additionally, many attempts to restore control of the lower urinary tract with electrical stimulation have been made. Stimulation sites have included: inside the bladder, bladder wall, thigh, pelvic floor, dorsal penile nerve, pelvic nerve, tibial nerve, sacral roots, sacral nerves and spinal cord. Catheters and sacral root stimulators are two techniques whose efficacy is well established. Some approaches have proven less successful and others are still in the development stage. Modifications to sacral root stimulation including posterior root stimulation, anodal blockade and high-frequency blockade as well as new techniques including intraspinal microstimulation, urethral afferent stimulation and injectable microstimulators are also discussed. No single device has yet restored the control and function of the lower urinary tract to the pre-injury state, but new techniques are bringing this possibility closer to reality.

Transcutaneously Coupled, High-Frequency Electrical Stimulation of the Pudendal Nerve Blocks External Urethral Sphincter Contractions

Background. Detrusor-sphincter dyssynergia is a condition in which reflexive contractions of the external urethral sphincter occur during bladder contractions, preventing the expulsion of urine. High-frequency stimulation (kHz range) has been shown to elicit a fast-acting and reversible block of action potential propagation in peripheral nerves, which may be a useful technique in the management of this condition. Objective. The aim of these experiments was to see if a newly developed stimulus delivery system, capable of transmitting current transcutaneously to remote peripheral nerves using a passive implanted conductor, was an effective way to transmit high-frequency waveforms to the pudendal nerve to block ongoing sphincter contractions. Methods. High-frequency waveforms were delivered through the skin to the pudendal nerve using a passive implanted conductor in 6 adult cats anesthetized with isoflurane. Five of the experiments were acute, terminal procedures, and the remaining cat was implanted with a permanent electrode system allowing evaluation for 6 months. Typical stimulation parameters were in the range of 1 to 10 kHz and 1 to 10 mA. Results. Complete blocking of external urethral sphincter contractions was achieved in 5 of the 6 animals. High-frequency stimulation was also tested in the chronically implanted animal without anesthesia, and the stimulation was tolerated with minimal aversive reactions. Conclusions. The transcutaneous passive implanted conductor stimulus delivery system is an effective way to stimulate the pudendal nerve at high frequency, leading to sphincter relaxation. This system may provide a simple means to implement this stimulation paradigm in people with detrusor-sphincter dyssynergia.

Microstimulation of primary afferent neurons in the L7 dorsal root ganglia using multielectrode arrays in anesthetized cats: thresholds and recruitment properties

Current research in motor neural prosthetics has focused primarily on issues related to the extraction of motor command signals from the brain (e.g. brain-machine interfaces) to direct the motion of prosthetic limbs. Patients using these types of systems could benefit from a somatosensory neural interface that conveys natural tactile and kinesthetic sensations for the prosthesis. Electrical microstimulation within the dorsal root ganglia (DRG) has been proposed as one method to accomplish this, yet little is known about the recruitment properties of electrical microstimulation in activating nerve fibers in this structure. Current-controlled microstimulation pulses in the range of 1-15 microA (200 micros, leading cathodic pulse) were delivered to the L7 DRG in four anesthetized cats using penetrating microelectrode arrays. Evoked responses and their corresponding conduction velocities (CVs) were measured in the sciatic nerve with a 5-pole nerve cuff electrode arranged as two adjacent tripoles. It was found that in 76% of the 69 electrodes tested, the stimulus threshold was less than or equal to 3 microA, with the lowest recorded threshold being 1.1 microA. The CVs of afferents recruited at threshold had a bimodal distribution with peaks at 70 m s(-1) and 85 m s(-1). In 53% of cases, the CV of the response at threshold was slower (i.e. smaller diameter fiber) than the CVs of responses observed at increasing stimulation amplitudes. In summary, we found that microstimulation applied through penetrating microelectrodes in the DRG provides selective recruitment of afferent fibers from a range of sensory modalities (as identified by CVs) at very low stimulation intensities. We conclude that the DRG may serve as an attractive location from which to introduce surrogate somatosensory feedback into the nervous system.

Neuroprosthetic technology for individuals with spinal cord injury

Abstract Context Spinal cord injury (SCI) results in a loss of function and sensation below the level of the lesion. Neuroprosthetic technology has been developed to help restore motor and autonomic functions as well as to provide sensory feedback. Findings This paper provides an overview of neuroprosthetic technology that aims to address the priorities for functional restoration as defined by individuals with SCI. We describe neuroprostheses that are in various stages of preclinical development, clinical testing, and commercialization including functional electrical stimulators, epidural and intraspinal microstimulation, bladder neuroprosthesis, and cortical stimulation for restoring sensation. We also discuss neural recording technologies that may provide command or feedback signals for neuroprosthetic devices. Conclusion/clinical relevance Neuroprostheses have begun to address the priorities of individuals with SCI, although there remains room for improvement. In addition to continued technological improvements, closing the loop between the technology and the user may help provide intuitive device control with high levels of performance.

Collaborative approach in the development of high-performance brain-computer interfaces for a neuroprosthetic arm: Translation from animal models to human control

Our research group recently demonstrated that a person with tetraplegia could use a brain–computer interface (BCI) to control a sophisticated anthropomorphic robotic arm with skill and speed approaching that of an able‐bodied person. This multiyear study exemplifies important principles in translating research from foundational theory and animal experiments into a clinical study. We present a roadmap that may serve as an example for other areas of clinical device research as well as an update on study results. Prior to conducting a multiyear clinical trial, years of animal research preceded BCI testing in an epilepsy monitoring unit, and then in a short‐term (28 days) clinical investigation. Scientists and engineers developed the necessary robotic and surgical hardware, software environment, data analysis techniques, and training paradigms. Coordination among researchers, funding institutes, and regulatory bodies ensured that the study would provide valuable scientific information in a safe environment for the study participant. Finally, clinicians from neurosurgery, anesthesiology, physiatry, psychology, and occupational therapy all worked in a multidisciplinary team along with the other researchers to conduct a multiyear BCI clinical study. This teamwork and coordination can be used as a model for others attempting to translate basic science into real‐world clinical situations.

Behavioral assessment of sensitivity to intracortical microstimulation of primate somatosensory cortex.

Significance Electrical stimulation of sensory structures in the brain is a powerful tool to investigate neural circuits and may provide a means to restore sensation for patients for whom stimulation of the nerve is not an option. For both purposes, however, it is critical to understand how the design of the stimulation shapes the evoked sensory experience. With this in mind, we investigate the ability of monkeys to detect and discriminate trains of electrical pulses delivered to their somatosensory cortex through chronically implanted electrode arrays. We show that artificial touch is highly dependent on various features of the electrical stimuli and discuss the implications of our results for the use of electrical stimulation in neuroscience and neural engineering. Intracortical microstimulation (ICMS) is a powerful tool to investigate the functional role of neural circuits and may provide a means to restore sensation for patients for whom peripheral stimulation is not an option. In a series of psychophysical experiments with nonhuman primates, we investigate how stimulation parameters affect behavioral sensitivity to ICMS. Specifically, we deliver ICMS to primary somatosensory cortex through chronically implanted electrode arrays across a wide range of stimulation regimes. First, we investigate how the detectability of ICMS depends on stimulation parameters, including pulse width, frequency, amplitude, and pulse train duration. Then, we characterize the degree to which ICMS pulse trains that differ in amplitude lead to discriminable percepts across the range of perceptible and safe amplitudes. We also investigate how discriminability of pulse amplitude is modulated by other stimulation parameters—namely, frequency and duration. Perceptual judgments obtained across these various conditions will inform the design of stimulation regimes for neuroscience and neuroengineering applications.

Real-time control of hind limb functional electrical stimulation using feedback from dorsal root ganglia recordings

OBJECTIVE Functional electrical stimulation (FES) approaches often utilize an open-loop controller to drive state transitions. The addition of sensory feedback may allow for closed-loop control that can respond effectively to perturbations and muscle fatigue. APPROACH We evaluated the use of natural sensory nerve signals obtained with penetrating microelectrode arrays in lumbar dorsal root ganglia (DRG) as real-time feedback for closed-loop control of FES-generated hind limb stepping in anesthetized cats. MAIN RESULTS Leg position feedback was obtained in near real-time at 50 ms intervals by decoding the firing rates of more than 120 DRG neurons recorded simultaneously. Over 5 m of effective linear distance was traversed during closed-loop stepping trials in each of two cats. The controller compensated effectively for perturbations in the stepping path when DRG sensory feedback was provided. The presence of stimulation artifacts and the quality of DRG unit sorting did not significantly affect the accuracy of leg position feedback obtained from the linear decoding model as long as at least 20 DRG units were included in the model. SIGNIFICANCE This work demonstrates the feasibility and utility of closed-loop FES control based on natural neural sensors. Further work is needed to improve the controller and electrode technologies and to evaluate long-term viability.

Multielectrode array recordings of bladder and perineal primary afferent activity from the sacral dorsal root ganglia

The development of bladder and bowel neuroprostheses may benefit from the use of sensory feedback. We evaluated the use of high-density penetrating microelectrode arrays in sacral dorsal root ganglia (DRG) for recording bladder and perineal afferent activity. Arrays were inserted in S1 and S2 DRG in three anesthetized cats. Neural signals were recorded while the bladder volume was modulated and mechanical stimuli were applied to the perineal region. In two experiments, 48 units were observed that tracked bladder pressure with their firing rates (79% from S2). At least 50 additional units in each of the three experiments (274 total; 60% from S2) had a significant change in their firing rates during one or more perineal stimulation trials. This study shows the feasibility of obtaining bladder-state information and other feedback signals from the pelvic region with a sacral DRG electrode interface located in a single level. This natural source of feedback would be valuable for providing closed-loop control of bladder or other pelvic neuroprostheses.

The effect of chronic intracortical microstimulation on the electrode–tissue interface

OBJECTIVE Somatosensation is critical for effective object manipulation, but current upper limb prostheses do not provide such feedback to the user. For individuals who require use of prosthetic limbs, this lack of feedback transforms a mundane task into one that requires extreme concentration and effort. Although vibrotactile motors and sensory substitution devices can be used to convey gross sensations, a direct neural interface is required to provide detailed and intuitive sensory feedback. The viability of intracortical microstimulation (ICMS) as a method to deliver feedback depends in part on the long-term reliability of implanted electrodes used to deliver the stimulation. The objective of the present study is to investigate the effects of chronic ICMS on the electrode-tissue interface. APPROACH We stimulate the primary somatosensory cortex of three Rhesus macaques through chronically implanted electrodes for 4 h per day over a period of six months, with different electrodes subjected to different regimes of stimulation. We measure the impedance and voltage excursion as a function of time and of ICMS parameters. We also test the sensorimotor consequences of chronic ICMS by having animals grasp and manipulate small treats. MAIN RESULTS We show that impedance and voltage excursion both decay with time but stabilize after 10-12 weeks. The magnitude of this decay is dependent on the amplitude of the ICMS and, to a lesser degree, the duration of individual pulse trains. Furthermore, chronic ICMS does not produce any deficits in fine motor control. SIGNIFICANCE The results suggest that chronic ICMS has only a minor effect on the electrode-tissue interface and may thus be a viable means to convey sensory feedback in neuroprosthetics.