Tim M. Bruns

Functional priorities, assistive technology, and brain-computer interfaces after spinal cord injury

Spinal cord injury (SCI) often affects a persons ability to perform critical activities of daily living and can negatively affect his or her quality of life. Assistive technology aims to bridge this gap in order to augment function and increase independence. It is critical to involve consumers in the design and evaluation process as new technologies such as brain-computer interfaces (BCIs) are developed. In a survey study of 57 veterans with SCI participating in the 2010 National Veterans Wheelchair Games, we found that restoration of bladder and bowel control, walking, and arm and hand function (tetraplegia only) were all high priorities for improving quality of life. Many of the participants had not used or heard of some currently available technologies designed to improve function or the ability to interact with their environment. The majority of participants in this study were interested in using a BCI, particularly for controlling functional electrical stimulation to restore lost function. Independent operation was considered to be the most important design criteria. Interestingly, many participants reported that they would consider surgery to implant a BCI even though noninvasiveness was a high-priority design requirement. This survey demonstrates the interest of individuals with SCI in receiving and contributing to the design of BCIs.

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.

Variable Patterned Pudendal Nerve Stimuli Improves Reflex Bladder Activation

We evaluated variable patterns of pudendal nerve (PN) stimuli for reflex bladder excitation. Reflex activation of the bladder has been demonstrated previously with 20-33 Hz continuous stimulation of PN afferents. Neuronal circuits accessed by afferent mediated pathways may respond better to physiological patterned stimuli than continuous stimulation. Unilateral PN nerve cuffs were placed in neurologically intact male cats. PN stimulation (0.5-100 Hz) was performed under isovolumetric conditions at bladder volumes up to the occurrence of distension evoked reflex contractions. Stimulus evoked reflex bladder contractions were elicited in eight cats. Across all experiments, bursting of 2-10 pulses at 100-200 Hz repeated at continuous stimulation frequencies evoked significantly larger bladder responses than continuous (single pulse) stimulation (52.0 plusmn 44.5%). Bladder excitation was also effective at 1 Hz continuous stimuli, which is lower than typically reported. Variable patterned pulse bursting resulted in greater evoked reflex bladder pressures and increased the potential stimulation parameter space for effective bladder excitation. Improved bladder excitation should increase the efficacy of neuroprostheses for bladder control.

Intraurethral stimulation for reflex bladder activation depends on stimulation pattern and location

Reflex bladder excitation has been demonstrated by stimulation of the pudendal nerve and several of its distal branches. However, excitation parameters have not been consistent and the relationship to anatomical locations within the urethra has not been fully investigated. An improved understanding of the lower urinary tract neurophysiology will improve human studies and neuroprosthetic device development.

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.

Estimating bladder pressure from sacral dorsal root ganglia recordings

Individuals with dysfunctional bladders may benefit from devices that track the bladder state. Recordings from pelvic and sacral nerve cuffs can detect bladder contractions, however they often have low signal quality and are susceptible to interference from non-bladder signals. Microelectrode recordings from sacral dorsal root ganglia (DRG) neurons may provide an alternate source for obtaining high quality sensory signals for bladder pressure monitoring. In this study, penetrating microelectrode arrays were inserted in the S1 and S2 DRG in two cats to record afferent spiking activity at different bladder pressures. Multivariate linear regression models were used to estimate bladder pressure from the spiking activity of DRG neurons. The best estimates were obtained with populations of 5–10 units primarily from the S2 DRG, with root mean square errors of 3.0–3.2 cm H2O (correlation coefficients of 0.5–0.9). This work demonstrates the feasibility of monitoring bladder pressure from DRG recordings.

Microstimulation of afferents in the sacral dorsal root ganglia can evoke reflex bladder activity

Pudendal afferent fibers can be excited using electrical stimulation to evoke reflex bladder activity. While this approach shows promise for restoring bladder function, stimulation of desired pathways, and integration of afferent signals for sensory feedback remains challenging. At sacral dorsal root ganglia (DRG), the convergence of pelvic and pudendal afferent fibers provides a unique location for access to lower urinary tract neurons. Our goal in this study was to demonstrate the potential of microstimulation in sacral DRG for evoking reflex bladder responses.

Single- and multi-unit activity recorded from the surface of the dorsal root ganglia with non-penetrating electrode arrays

Non-penetrating surface electrode recording techniques are typically associated with field potential recordings, while extracellular recordings from single neurons are made using penetrating metal wire or microfabricated microelectrode arrays. Here, we report on single- and multi-unit neuronal recordings made using non-penetrating electrodes placed on the epineural surface of the dorsal root ganglia (DRG). Across four experiments in anesthetized cats, approximately 40% of the electrodes recorded single- and multi-unit spiking activity with spike-rates that covaried significantly with hindlimb movement. In two intraoperative experiments in humans, compound activity was recorded from the DRG surface in response to peripheral stimulation of the common peroneal nerve. This approach may have advantages over penetrating electrode arrays in terms of clinical acceptability and recording longevity.

Bursting stimulation of proximal urethral afferents improves bladder pressures and voiding

Reflex bladder excitation has been evoked via pudendal nerve, pudendal nerve branch and intraurethral stimulation; however, afferent-evoked bladder emptying has been less efficient than direct activation of the bladder via sacral root stimulation. A stimulation method that improves activation of the urethra-bladder excitatory reflex with minimal sphincter recruitment may lead to improved bladder emptying. Fine wire electrodes were placed in the wall of the urethra in five cats. Placement of electrodes near the proximal urethra evoked bladder contractions with minimal sphincter activation. On these electrodes, lower frequency burst-patterned stimuli evoked greater bladder voiding efficiencies (71.2 +/- 27.8%) than other stimulus patterns on the same electrodes (50.4 +/- 41.5%, p > 0.05) or any stimulus pattern on electrodes that elicited urethral closure (16.5 +/- 12.7%, p < 0.05). Fine wire electrodes specifically targeted afferent fibers in the urethra, indicating the feasibility of clinical evaluations using the same method. This work may improve the translation of next generation neuroprostheses for bladder control.