Designing a Thalamic Somatosensory Neural Prosthesis: Consistency and Persistence of Percepts Evoked by Electrical Stimulation

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DOI: 10.1109/TNSRE.2011.2152858 · Source: PubMed
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.

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IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 19, NO. 5, OCTOBER 2011 477
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 stim-
ulation could provide the necessary durations and consistency of
percepts for a human somatosensory neural prosthetic. Contin-
uous and cycling high-frequency (185 Hz, 0.21 ms pulse duration
charge balanced square wave) electrical pulses with the cycling pat-
terns 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 immedi-
ately after surgery. While consecutive continuous stimuli produced
decreasing durations of sensation, the amplitude and type of per-
cept 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
S
OMATOSENSORY feedback is a crucial element of com-
plex and smooth motor control [1], even as far as pro-
ducing 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 at-
tempts been made to recreate somatosensory function [6], [7].
Previously we investigated the quality and naturalness of per-
cepts evoked by different brief electrical stimulus patterns ap-
plied 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 con-
sider when designing a somatosensory prosthetic is the consis-
tency 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 Oc-
tober 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 pros-
thetic 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 sta-
bility 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 per-
cepts over time, and 2) because the persistence of sensations in-
volve 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, al-
though 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. M
ETHODS
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 ventroin-
termedius nucleus (Vim) of thalamus and one patient suffered
from right hand chronic neuropathic pain and had both ventro-
caudal (Vc) thalamic and periventricular grey electrodes. These
patients were studied because the same brain regions are ex-
plored 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) ex-
tends either into Vc or at least to the Vim–Vc junction [8]. Sum-
maries of each patient’s clinical settings and relevant dates are
in Table I. The protocol was part of one approved by the Con-
joint Health Region Ethics Board and informed consent was
obtained.
We first built a homemade continuous sliding scale psy-
chophysical response device to measure the intensity of a
percept. It consisted of a simple lever-controlled rotary poten-
tiometer, with the lever allowed to pivot approximately 90
,
one side of which was “0” rating and the other was “10.” The
1534-4320/$26.00 © 2011 IEEE
478 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 19, NO. 5, OCTOBER 2011
TABLE I
C
LINICAL
DATA FOR
PARTICIPATING
SUBJECTS.IMPEDANCES ARE
MEASURED BY THE
IMPLANTED PULSE
GENERATOR AT
1.5 V, 210
s, 30 Hz.
W
HERE
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-
binations:
. The DBS
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 approx-
imately 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 question-
naire [9] describing the percepts elicited at various time points
in this protocol. With continuous stimulation, the subjects de-
scribed the percepts evoked immediately succeeding the first
and preceding the last trial. They were questioned after each cy-
cling stimulus application. This questionnaire rated the natural-
ness, location, painfulness, and quality of sensation [6]. In addi-
tion, 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 sensa-
tion. Coil antennae over each patient’s implanted pulse gener-
ator 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 con-
tingency 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. R
ESULTS
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). Un-
like 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-
jects at the most dorsal pair
. All stimulations utilized
185 Hz at 0.21 ms pulse width. An effect of electrode combi-
nation was seen (one-way ANOVA,
, ) with
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 stim-
ulated 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 de-
vice. Responses between the two systems were highly corre-
lated (
, ) confirming the validity of the
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
HEMING et al.: DESIGNING A THALAMIC SOMATOSENSORY NEURAL PROSTHESIS 479
Fig. 1. Percepts evoked. A: The majority of sensations elicited in this study with both continuous and cycling stimulation were tingle sensations (tickle, itch, elec-
tric 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
stimulus patterns [
, , , Fig. 1(A)].
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-
trode poles
, but occurred with all combinations in
subject 1018. As well, most sensations were felt as either to-
tally unnatural (35%) or rather unnatural (49%) with fewer rat-
ings 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 com-
pared 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-
sations (
, , ) and fewer “possibly
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 so-
matosensory nucleus (Vc) may provide more natural percepts,
480 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 19, NO. 5, OCTOBER 2011
we compared responses by grouping them into number of nat-
ural (totally unnatural, almost natural) and unnatural (rather un-
natural, 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 cat-
egorized 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-
uous (
, , ) or cycling ( ,
, ) 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 re-
turned 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-
rations in all patients (1019:
, ; 1020:
, ; 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 stimu-
lation 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-fre-
quency 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 stimula-
tion 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.
IV. DISCUSSION
In this study we examined electrical stimulation in patients
with chronically implanted DBS electrodes in order to deter-
mine the consistency and duration of percepts achieved by tha-
lamic stimulation. We studied the same subjects who had pre-
viously participated in a similar study examining the percepts
produced by acute thalamic stimulation at the time of DBS im-
plant. As with the prior study, stimulation produced mostly un-
natural 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 stimu-
lator. 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 481
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 per-
cepts evoked by thalamic stimulation do not change over short
(minutes) or long (years) time periods, the reduction in nat-
uralness perceived with electrical stimulation 29 months after
DBS implant was unexpected. The shift in naturalness descrip-
tion was very small, from “possibly natural” to “rather unnat-
ural, 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 re-
markably 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 restora-
tion. As such, there was no pairing of stimulation with nat-
ural 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 compen-
sate 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 compa-
rable 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 exam-
ined the psychophysics of stimulation in patients with these de-
vices implanted over the long term.
Another finding important to the development of a somatosen-
sory 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 re-
sponses 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 ap-
plied 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
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 sen-
sation 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 sensori-
motor prosthesis.
482 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 19, NO. 5, OCTOBER 2011
ACKNOWLEDGMENT
This project was part of the AHFMR Interdisciplinary Team
Grant in Smart Neural Prostheses.
R
EFERENCES
[1] A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-
controlled 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 Am-
plif., 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 hard-
ware 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 mechanorecep-
tive 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-to-
pulse 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 sen-
sations like those of mechanical stimulation and movement,J. Neuro-
physiol., 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 specializa-
tion 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 molec-
ular 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 fel-
lowship 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.
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