Designing a Thalamic Somatosensory Neural Prosthesis: Consistency ...

IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 19, NO. 5, OCTOBER 2011

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Designing a Thalamic Somatosensory Neural Prosthesis: Consistency and Persistence of Percepts Evoked by Electrical Stimulation Ethan A. Heming, Ryan Choo, Jonathan N. Davies, and Zelma H. T. Kiss

Abstract—Intuitive somatosensory feedback is required for fine motor control. Here we explored whether thalamic electrical stimulation could provide the necessary durations and consistency of percepts for a human somatosensory neural prosthetic. Continuous and cycling high-frequency (185 Hz, 0.21 ms pulse duration charge balanced square wave) electrical pulses with the cycling patterns varying between 7% and 67% of duty cycle were applied in five patients with chronically implanted deep brain stimulators. Stimulation produced similar percepts to those elicited immediately after surgery. While consecutive continuous stimuli produced decreasing durations of sensation, the amplitude and type of percept did not change. Cycling stimulation with shorter duty cycles produced more persisting percepts. These features suggest that the thalamus could provide a site for stable and enduring sensations necessary for a long term somatosensory neural prosthesis. Index Terms—Deep brain stimulation, microstimulation, neural prostheses, psychophysics.

I. INTRODUCTION

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OMATOSENSORY feedback is a crucial element of complex and smooth motor control [1], even as far as producing direct motor control through the somatosensory cortex [2]. While much research has gone into restoring other senses such as hearing [3] or vision [4] and into controlling motor output by brain–computer interfaces [5], only recently have attempts been made to recreate somatosensory function [6], [7]. Previously we investigated the quality and naturalness of percepts evoked by different brief electrical stimulus patterns applied in human thalamus [6]. “Natural” pulse trains, digitized from other human’s somatosensory thalamic neurons, did not evoke more natural percepts than high-frequency stimulation at 333 Hz (0.2 ms pulse duration) did. An important issue we did not investigate was the persistence of the percepts. Naturally produced somatic sensation conveys information not only about transient touch, but also constant pressure. These sensations are especially important for those at risk for pressure sores, such as those with spinal cord injury. Another important issue to consider when designing a somatosensory prosthetic is the consistency of the percepts elicited. If stimulation results in a different sensation every time it is applied, or changes rapidly over time, Manuscript received February 02, 2011; revised April 14, 2011; accepted April 27, 2011. Date of publication May 27, 2011; date of current version October 07, 2011. The authors are with the Department of Clinical Neuroscience, University of Calgary, Calgary, T2N 4N1 AB, Canada. Color versions of one or more of the figures in this paper are available online at http://ieeexplore.ieee.org. Digital Object Identifier 10.1109/TNSRE.2011.2152858

there would be no way to associate that sensation with a touch or pressure. In order for a thalamic somatosensory neural prosthetic to be viable, the same stimulation pattern should produce the same sensation over the lifetime of the device. In order to investigate these two issues, time course and stability of percepts evoked by thalamic stimulation, we retested the same patients we originally studied during and immediately after their deep brain stimulation (DBS) surgery [6], applying similar patterns of pulses (as close as could be applied with their implanted pulse generator). We tested two hypotheses: 1) the same or similar patterns of pulses would evoke the same percepts over time, and 2) because the persistence of sensations involve habituation of neural elements to constant high-frequency stimulation, varying the duty cycle could alter the time course of percepts. We found that stimulation patterns applied after years of chronic continuous stimulation produced comparable percepts as when the DBS electrode was first introduced, although with fewer natural responses. High-frequency (185 Hz, 0.21 ms pulse duration) stimulation in cycling patterns ranging from 7% to 67% of duty cycle produced longer lasting percepts than continuous stimulation. II. METHODS Five subjects, all of whom participated in our previous project [6], had chronic DBS systems for a mean of 29.1 10.1 (SD) months (range 16.5–43) before the present study. Four patients had essential tremor and had electrodes implanted in ventrointermedius nucleus (Vim) of thalamus and one patient suffered from right hand chronic neuropathic pain and had both ventrocaudal (Vc) thalamic and periventricular grey electrodes. These patients were studied because the same brain regions are explored during DBS surgery, despite the fact that the Vim target for tremor is 2–4 mm anterior to the Vc nucleus, the target for pain. The DBS electrode is passed from antero–dorsal to postero–ventral, meaning that the distal pole of the quadripolar DBS lead (Model 3387, Medtronic Inc., Minneapolis, MN) extends either into Vc or at least to the Vim–Vc junction [8]. Summaries of each patient’s clinical settings and relevant dates are in Table I. The protocol was part of one approved by the Conjoint Health Region Ethics Board and informed consent was obtained. We first built a homemade continuous sliding scale psychophysical response device to measure the intensity of a percept. It consisted of a simple lever-controlled rotary potentiometer, with the lever allowed to pivot approximately 90 , one side of which was “0” rating and the other was “10.” The

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TABLE I CLINICAL DATA FOR PARTICIPATING SUBJECTS. IMPEDANCES ARE MEASURED BY THE IMPLANTED PULSE GENERATOR AT 1.5 V, 210 s, 30 Hz. WHERE ONLY ONE POLE IS LISTED AS THE ACTIVE ONE, THE SETTINGS ARE MONOPOLAR WITH THE PULSE GENERATOR AS ANODE

device was housed in a metal box with a simple scale attached along the end of the lever’s path. The device output a voltage signal, which scaled linearly with angular displacement of the lever. Only after validation in eight normal controls did we use it on the study patients. The study protocol involved bipolar stimulation applied through each patient’s thalamic DBS electrode (Model 3387, Medtronic Inc., Minneapolis, MN) using the following com. The DBS binations: electrode has four contacts (1.5 mm long, 6 mm surface area each) called 0, 1, 2, 3 from distal to proximal. We controlled the constant voltage implantable pulse generators (Kinetra or Soletra, Medtronic Inc., Minneapolis, MN) by telemetry using the N’Vision Clinician Programmer (Model 8840, Medtronic Inc., Minneapolis, MN). Stimulating electrode pair, voltage, frequency, and duty cycle were varied within the limits of the programmer for each application of the following protocol. For each electrode combination we first applied 185 Hz continuous stimulation (pulse width 0.21 ms), increasing the voltage gradually and using a staircase method to find sensory threshold. We chose these parameters to best match those used intra-operatively and during the immediate postoperative phase as described in our previous protocol [6]. While previously we used 333 Hz and 0.2 ms, the maximum frequency that can be applied through the implanted pulse generator is 185 Hz and the closest pulse width was 0.21 ms. We defined threshold as an obvious sensory percept, one that was more than transient. When this was determined, stimulation at threshold voltage was applied 5–10 times. Stimulation was left on at threshold until the subject reported that the percept had disappeared or approximately 3 min ( 170 s) had elapsed. This same protocol was repeated using a supra-threshold (20%–50% higher) voltage. After these continuous stimulation patterns were determined, we applied cycling stimulation profiles with duty cycles from 0.1 s and 0.2 s on and 0.1–1.2 s off at an average of 115% (100%–180% if necessary to produce sensation) of threshold voltage. All stimulations were separated by at least 30 s to reduce effects of prior trials. Subjects were asked to respond to a psychophysical questionnaire [9] describing the percepts elicited at various time points in this protocol. With continuous stimulation, the subjects described the percepts evoked immediately succeeding the first and preceding the last trial. They were questioned after each cycling stimulus application. This questionnaire rated the naturalness, location, painfulness, and quality of sensation [6]. In addition, we quantified the duration of each percept using our psy-

chophysical response device that provided intensities ranging from 0 to 10, where 0 was no sensation and 10 was the strongest sensation the subject perceived. Patients were also instructed to verbally indicate when they could no longer feel a sensation. Coil antennae over each patient’s implanted pulse generator were used to indicate stimulation start and end times. All data were digitally recorded at 2000 Hz (Harmonie, Stellate Inc., Montreal, QC, Canada). Statistical analysis consisted of Chi-squared tests for contingency with sensations and naturalness. One-way analysis of variance (ANOVA) with post-hoc t-tests and linear regression were employed to examine duration of percepts. III. RESULTS A total of 440 stimulus trains were applied using four contact combinations in each of the five subjects (171 stimulations had unique parameters, with repeats making up the remainder). Unlike our prior study, some stimulation patterns were perceived as painful. Any stimulation that caused distress was aborted as soon as pain was elicited. Stimulation thresholds ranged from 0.6 to 6.0 V, averaging 1.3 0.6 V across subjects at the most ventral electrode pair , and 3.5 1.7 V across sub. All stimulations utilized jects at the most dorsal pair 185 Hz at 0.21 ms pulse width. An effect of electrode combi, ) with nation was seen (one-way ANOVA, having a significantly lower threshold than (student’s t-test, , ). There were no significant differences in thresholds between subjects (one-way ANOVA, , ). A. Psychophysical Response Device Validation To ensure that the responses given on the physical sliding scale of the homemade psychophysical response device were reproducible and valid, control subjects were electrically stimulated with various randomized amplitudes on the palm of their nondominant hand using a constant current stimulus isolator in combination with a stimulus generator (A360, A365, and A310, WPI, Sarasota, FL). The subjects rated the sensations in two sets, one with pen and paper and one using the response device. Responses between the two systems were highly corre, ) confirming the validity of the lated ( device for measuring intensity of a percept. B. Sensations Elicited and Naturalness of the Percepts As with our prior study, the majority of elicited percepts using all stimulation patterns were tingle sensations (55%), followed

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Fig. 1. Percepts evoked. A: The majority of sensations elicited in this study with both continuous and cycling stimulation were tingle sensations (tickle, itch, electric current), with some mechanical (touch, pressure, sharp) and movement (vibration, movement through the body or across the skin). There were no differences in these descriptors in the current and prior study aside from the additional descriptor, “pulsing,” noted only with cycling patterns. B: The majority of sensations elicited were classified as unnatural, with no difference between cycling and continuous stimulus patterns applied. There were more “rather unnatural” and fewer “possibly natural” sensations in the current compared to the prior study. C: Projected field (PF) sizes for continuous and cycling stimulations at all electrode combinations used in this study were spread between small, medium, and large, with no hemibody PFs. They were not significantly different from the previous study. D: An example of the maximal intensity of sensation as rated on the psychophysical response device over multiple trials for one condition in one subject. The maximal amplitude of percepts generally remained constant over repeated trials.

by movement (24%), mechanical (12%), temperature (2%), and pain (7%). There were no differences with continuous or cycling , , , Fig. 1(A)]. stimulus patterns [ Painful percepts were elicited in three subjects and referred to with such words as “throbbing,” “stabbing,” “cutting,” or “a flash.” In subjects 1021 and 1022 these only occurred with elec, but occurred with all combinations in trode poles subject 1018. As well, most sensations were felt as either totally unnatural (35%) or rather unnatural (49%) with fewer ratings of possibly (10%), almost (4%), or totally natural (2%) and no differences noted between continuous and cycling patterns , , , Fig. 1(B)]. [ To determine if percepts elicited might have changed over a longer period of time, the results from this study were compared to those of the prior one [6]. Comparisons were only made to macro-electrode stimulation data from the prior study. While there were slight variations in the terms selected, overall , , no significant differences were obtained (

). Because of the small number of responses for each electrode, of which most were tingle, statistical analysis for each electrode combination could not be performed. It was noted that some of the cycling stimuli was described as “pulsing,” which was not a perceptual term in the original questionnaire. In the current study years after DBS surgery, the subjects’ perceived degree of naturalness shifted slightly when compared , , to immediately postoperatively ( ). There were significantly more “rather unnatural” sen, , ) and fewer “possibly sations ( natural” sensations ( , , ) without changes at the extremes of the naturalness scale (totally natural: , , ; almost natural: , , ; totally unnatural: , , ). Because one subject (1021) had a Vc-DBS and the other four had Vim-DBS, and one may expect that DBS applied in the somatosensory nucleus (Vc) may provide more natural percepts,

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we compared responses by grouping them into number of natural (totally unnatural, almost natural) and unnatural (rather unnatural, totally unnatural). The responses of patient 1021 did not , , ). differ from the other patients ( As with the prior study, the body location where stimulations were perceived, referred to as projected fields (PFs), were categorized for threshold continuous stimulation and lowest duty cycle cycling stimulation at each electrode combination into four size groups: “small” for highly localized sensations such as single digits; “medium” for sensations that covered parts of limbs, such as multiple digits or parts of limbs, “large” for entire limbs, torso, or face; and “hemibody” if the sensation spanned the entire contralateral side [Fig. 1(C)]. “Small,” “medium,” and “large” PFs were not significantly different for either contin, , ) or cycling ( , uous ( , ) stimulation. As well, when compared to macro-electrode stimulation from our prior study, no differences , , ). were found ( To examine the stability of percepts over the course of several trials, the maximum psychophysical response was derived for each trial. As in the example of Fig. 1(D), there was no obvious difference in the intensity of percepts with multiple successive trials. There was also no difference in naturalness or percept elicited with repeated applications of the same stimulus. C. Duration of Percepts The duration of each percept was determined by measuring the time between the first rise in psychophysical response, and the time when the rating again reached zero. Four subjects used the device reliably. However, duration data from subject 1018 was excluded because of inconsistent responses. For example, this subject reported that the sensation had ended only after being asked, and she sometimes reported that the sensation returned after telling us it had passed. With successive applications of the same continuous stimulus (applied 30 s apart), there was a gradual decrease in duration of percepts elicited [Fig. 2(A)]. A linear regression of duration of percept by trial showed a significant and gradual reduction , ). ( Cycling stimulation produced significantly longer percept du, ; 1020: rations in all patients (1019: , ; 1021: , ; 1022: , ). Interestingly each subject experienced similar average duration of percepts ( , ) despite the electrodes being located in different brain regions [Fig. 2(B)]. Finally, the duration of percept was investigated by duty cycle. Each of the cycling parameters lead to a different duty cycle for that particular stimulation, with continuous stimulation being 100% duty cycle and 0.1 s on / 1.2 s off being the shortest duty cycle at 7.7%. Since all stimulations were stopped at approximately 3 min where they were considered “constant,” comparing duty cycle to duration of percept would not yield valid results. Instead we compared the percent of all stimulations at each duty cycle category that reached at least 170 s, or “constant” sensation to the duty cycle applied. As in Fig. 2(C), we found a significant negative correlation , ). (

Fig. 2. Duration of percepts. A: Over repeated trials of continuous high-frequency stimulation, duration of percepts decreased. Average data from all valid trials from all patients analyzed for duration of percept are shown as mean SEM. B: Total percept duration was significantly longer when cycling stimulation was applied rather than continuous stimulation in all subjects. There were no differences in percept duration between subjects. C: A significant correlation between persisting percepts (as defined by lasting 170 s) and the duty cycle of the stimulation applied. Note that 100% duty cycle is continuous stimulation.

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IV. DISCUSSION In this study we examined electrical stimulation in patients with chronically implanted DBS electrodes in order to determine the consistency and duration of percepts achieved by thalamic stimulation. We studied the same subjects who had previously participated in a similar study examining the percepts produced by acute thalamic stimulation at the time of DBS implant. As with the prior study, stimulation produced mostly unnatural and tingling percepts. While the descriptive nature of these percepts were similar to those experienced at the time of DBS implant, more were described as unnatural, years after the subjects had become accustomed to using their thalamic stimulator. In addition, the persistence of a percept was related to the time that high-frequency stimulation was applied. For example,

HEMING et al.: DESIGNING A THALAMIC SOMATOSENSORY NEURAL PROSTHESIS

repeated trials of continuous stimulation, and higher duty cycles both reduced the duration of percepts evoked. While it was encouraging to see that the general nature of percepts evoked by thalamic stimulation do not change over short (minutes) or long (years) time periods, the reduction in naturalness perceived with electrical stimulation 29 months after DBS implant was unexpected. The shift in naturalness description was very small, from “possibly natural” to “rather unnatural,” and may have occurred because initially subjects do not know what to think is natural and may be more willing to refer to a percept as “possibly natural.” The nervous system is remarkably adaptable to changes in input and other prostheses, such as cochlear implants, generally become more useful to the user with ongoing use [10]. Somatosensory prostheses would be disadvantageous if the naturalness of a sensation produced by an implanted electrode were to decrease consistently over time. However it is important to note that the patients in this study were not using their implants for somatosensory restoration. As such, there was no pairing of stimulation with natural phenomena. It is likely that, if anything, the reverse was true—that any sensations elicited by the implant were viewed as a hindrance by the subjects. If it were the case that naturalness of percepts from a given stimulation parameter drifted slowly over time, controls could be incorporated into a neural prosthetic whereby the user, technician, or the device itself, could compensate by making small adjustments to the stimulation parameters. Unlike the previous study, painful sensations were elicited by both continuous and cycling stimulations in three patients. Since these subjects did not describe painful sensations with comparable stimulation patterns in the original study, this could pose a problem for thalamus as a potential target for somatosensory restoration. Previous studies of acute stimulation have reported pain with thalamic stimulation [9], however no one has examined the psychophysics of stimulation in patients with these devices implanted over the long term. Another finding important to the development of a somatosensory neural prosthesis is that while the duration of percepts evoked by continuous stimulation over several trials dropped slowly, the naturalness of the sensations did not show such a trend. This occurred even in the subject whose DBS electrode was located in somatosensory Vc nucleus of thalamus. Therefore it is likely that the same neural pathways were activated by each stimulus train, but they were adapting to the high-frequency stimulation [11]. In fact, the use of a lower duty cycle, as with cycling stimulation, may eliminate this reduction in duration of percepts, just as percepts lasted longer with lower duty cycles. No previous literature exists on the psychophysical responses to cycling stimulation applied to somatosensory thalamus. Birdno et al. [12], [13] described effects of different patterns of electrical stimulation on tremor. Psychophysics of electrical stimulation in somatosensory thalamus has mainly been investigated in the context of pain [9] and more recently mechanical stimulation and movement [14]. These studies applied only continuous microstimulation in thalamus of patients undergoing surgery and did not examine the extinction point of the sensations. There are several limitations to this study. There were few subjects, four had electrodes targeted in Vim whereas the fifth

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had a DBS electrode in Vc somatosensory thalamus. A DBS implanted for somatosensory restoration would most likely be located in Vc to target the most relevant tactile somatosensory nucleus [9]. However the Vim is the kinesthetic nucleus of thalamus [15] and therefore also a relevant potential target for a somatosensory prosthesis to reproduce the perception of limb movement. The patterns of electrical stimulation applied in our previous study could not be reproduced exactly with the implanted pulse generator. Also only a limited number of cycling patterns of stimulation are possible with the implanted pulse generator. The length of time required for psychophysical testing did not allow us to test patterns for longer than 3 min, therefore we assumed that if a subject felt sensation for 3 min this represented persistence. The psychophysical questionnaire we used had been developed for an intra-operative testing protocol [9] and was not optimized for some of the percepts patients experienced. For example, we added the term “pulsing” because so many subjects used this word to describe the sensation elicited by cycling stimulation at lower duty cycles. We have yet to elicit the perception of movement. The term “movement” as it was used for this protocol means vibration or movement through the body or across the skin. It does not mean movement about a joint or a position of the limb in space. We have never been able to elicit such percepts without the electrical stimulation actually producing movement, and others have described such percepts or intentions of movement occurring only with cortical stimulation [16]. A useful tactile somatosensory prosthesis requires several features. It must 1) evoke small PFs such that individual fingers can be targeted, 2) provide graded sensation without increasing the PF size, 3) have reproducibility and persistence, and 4) provide the perception of slip and pressure. In this study we focused on reproducibility and persistence. The distribution of PFs and nature of the percepts did not change over the time. We could evoke more persistent percepts with various duty cycle patterns of electrical stimulation. In addition we could produce graded sensations however the PF increased, due to the large electrode surface area used for chronic DBS. Even though some small PFs could be elicited with the large DBS electrode [Fig. 1(C)], having only four contacts allowed only a few combinations thus obtaining only a few PFs. Therefore the ideal thalamic somatosensory prosthesis design requires much smaller electrode surfaces, closely packed sites, but distributed in the optimal somatotopically appropriate cellular region. This will require an array spanning medial to lateral and anterior to posterior not a simple cylindrical electrode that exists for DBS today. With such an electrode design, it is likely that we could evoke small PFs that remain so with increasing amplitude of stimulation. Despite these limitations, the thalamus remains a reasonable site to investigate further on the road to a somatosensory neural prosthesis. The percepts evoked by thalamic high-frequency stimulation are consistent and by varying duty cycle could also provide longer percept durations. Evoking natural percepts by thalamic electrical stimulation remains a challenge, as does the ability to evoke kinesthesia, the perception of limb movement, and position sense, which are critical to developing a sensorimotor prosthesis.

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ACKNOWLEDGMENT This project was part of the AHFMR Interdisciplinary Team Grant in Smart Neural Prostheses. REFERENCES [1] A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Braincontrolled interfaces: Movement restoration with neural prosthetics,” Neuron, vol. 52, no. 1, pp. 205–220, Oct. 5, 2006. [2] F. Matyas, V. Sreenivasan, F. Marbach, C. Wacongne, B. Barsy, C. Mateo, R. Aronoff, and C. C. Petersen, “Motor control by sensory cortex,” Science, vol. 330, no. 6008, pp. 1240–1243, Nov. 26, 2010. [3] D. S. Haynes, J. A. Young, G. B. Wanna, and M. E. Glasscock, 3rd, “Middle ear implantable hearing devices: An overview,” Trends Amplif., vol. 13, no. 3, pp. 206–214, Sep. 2009. [4] S. J. Chen, M. Mahadevappa, R. Roizenblatt, J. Weiland, and M. Humayun, “Neural responses elicited by electrical stimulation of the retina,” Trans. Am. Ophthalmol. Soc., vol. 104, pp. 252–259, 2006. [5] T. Stieglitz, B. Rubehn, C. Henle, S. Kisban, S. Herwik, P. Ruther, and M. Schuettler, “Brain-computer interfaces: An overview of the hardware to record neural signals from the cortex,” Prog. Brain Res., vol. 175, pp. 297–315, 2009. [6] E. Heming, A. Sanden, and Z. H. Kiss, “Designing a somatosensory neural prosthesis: Percepts evoked by different patterns of thalamic stimulation,” J. Neural Eng., vol. 7, no. 6, p. 064001, Dec. 2010. [7] G. S. Dhillon and K. W. Horch, “Direct neural sensory feedback and control of a prosthetic arm,” IEEE Trans. Neural Syst. Rehabil. Eng., vol. 13, no. 4, pp. 468–472, Dec. 2005. [8] Z. H. T. Kiss, M. Wilkinson, J. Krcek, O. Suchowersky, B. Hu, W. Murphy, D. Hobson, and R. R. Tasker, “Is the target for thalamic DBS the same as for thalamotomy?,” Mov Disord., vol. 18, no. 10, pp. 1169–1175, 2003. [9] F. A. Lenz, M. Seike, R. T. Richardson, Y. E. Lin, F. H. Baker, I. Khoja, C. J. Yeager, and R. H. Gracely, “Thermal and pain sensations evoked by microstimulation in the area of human ventrocaudal nucleus,” J. Neurophysiol., vol. 70, no. 1, pp. 200–212, 1993. [10] E. A. Beadle, D. J. McKinley, T. P. Nikolopoulos, J. Brough, G. M. O’Donoghue, and S. M. Archbold, “Long-term functional outcomes and academic-occupational status in implanted children after 10 to 14 years of cochlear implant use,” Otol. Neurotol., vol. 26, no. 6, pp. 1152–1160, Nov. 2005. [11] G. Werner and V. B. Mountcastle, “Neural activity in mechanoreceptive cutaneous afferents: Stimulus-response relations, weber functions, and information transmission,” J. Neurophysiol., vol. 28, pp. 359–397, Mar. 1965. [12] M. J. Birdno, A. M. Kuncel, A. D. Dorval, D. A. Turner, and W. M. Grill, “Tremor varies as a function of the temporal regularity of deep brain stimulation,” Neuroreport, vol. 19, no. 5, pp. 599–602, 2008. [13] M. J. Birdno, S. E. Cooper, A. R. Rezai, and W. M. Grill, “Pulse-topulse changes in the frequency of deep brain stimulation affect tremor and modeled neuronal activity,” J. Neurophysiol., vol. 98, no. 3, pp. 1675–1684, 2007.

[14] S. Ohara, N. Weiss, and F. A. Lenz, “Microstimulation in the region of the human thalamic principal somatic sensory nucleus evokes sensations like those of mechanical stimulation and movement,” J. Neurophysiol., vol. 91, no. 2, pp. 736–745, Feb. 2004. [15] Z. H. T. Kiss, K. D. Davis, R. R. Tasker, A. M. Lozano, B. Hu, and J. O. Dostrovsky, “Kinaesthetic neurons in thalamus of humans with and without tremor,” Exp. Brain Res., vol. 150, no. 1, pp. 85–94, 2003. [16] M. Desmurget, K. T. Reilly, N. Richard, A. Szathmari, C. Mottolese, and A. Sirigu, “Movement intention after parietal cortex stimulation in humans,” Science, vol. 324, no. 5928, pp. 811–813, 2009.

Ethan A. Heming received the B.S. degrees in physics and psychology and the M.S. degree in neuroscience from the University of Calgary, Calgary, AB, Canada. Currently, he is working toward the Ph.D. degree at Queen’s University, Kingston, ON, Canada. His research interests include sensory and motor neural prosthetics, brain–computer interfaces, and motor control.

Ryan Choo is a mechanical engineering student with a biomedical specialization at the Schulich School of Engineering, University of Calgary, Calgary, AB, Canada. In 2010, he was a summer student in the Therapeutic Brain Stimulation & Research Program, University of Calgary.

Jonathan N. Davies is a neuroscientist and science writer, and former research associate with the Department of Clinical Neuroscience, University of Calgary, Calgary, AB, Canada. His background includes clinical and basic neuroscience, using a variety of techniques including electrophysiology, imaging, and molecular biology.

Zelma H. T. Kiss received the M.D. from the University of Ottawa, Ottawa, ON, Canada, in 1988, the Ph.D. degree in addition to residency training from the University of Toronto, Toronto, ON, Canada, in 1998, and postdoctoral fellowship at Universitaire Joseph Fourier, Grenoble, France. She is a neurosurgeon/scientist and Associate Professor at the Hotchkiss Brain Institute and Department of Clinical Neurosicences, University of Calgary, Calgary, AB, Canada. She is a Clinical Scholar of the Alberta Heritage Foundation for Medical Research. Her research interests are focused on the mechanisms of action of deep brain stimulation and other indications for neuromodulation therapies. Her recent work has extended to the development of Neural Prostheses to restore sensorimotor function. Along with co-leaders in Edmonton, she was recently awarded an AHFMR Interdisciplinary Team Grant on this theme.