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OCCUPATIONAL THERAPY INTERNATIONAL

Occup. Ther. Int. 16(34): 190203 (2009)


Published online 10 June 2009 in Wiley InterScience
(www.interscience.wiley.com) DOI: 10.1002/oti.277

A review of bilateral training for


upper extremity hemiparesis
MARY ELLEN STOYKOV, Rehabilitation Institute of Chicago, Chicago, IL
DANIEL M. CORCOS, University of Illinois at Chicago, Chicago, IL
ABSTRACT: Upper extremity hemiparesis is the most common post-stroke disability. Longitudinal studies have indicated that 3066% of stroke survivors do not have
full arm function 6 months post-stroke. The current gold standard for treatment of
mild post-stroke upper limb impairment is constraint-induced therapy but, because of
the inclusion criteria, alternative treatments are needed which target more impaired
subjects. Bilateral arm training has been investigated as a potential rehabilitation
intervention. Bilateral arm training encompasses a number of methods including: (1)
bilateral isokinematic training; (2) mirror therapy using bilateral training; (3) devicedriven bilateral training; and (4) bilateral motor priming. Neural mechanisms mediating bilateral training are first reviewed. The key bilateral training studies that have
demonstrated evidence of efficacy will then be discussed. Finally, conclusions are
drawn concerning clinical implications based on the reviewed literature. Copyright
2009 John Wiley & Sons, Ltd.
Key words: bilateral training, stroke, upper extremity

Introduction
Post-stroke hemiparesis, weakness of one side of the body, is one of the most
common conditions that occupational therapists address. The level of disability
is often determined by the severity of hemiparesis. According to Kwakkel et al.
(2003), 3066% of all individuals with hemiparesis have poor arm function 6
months post-stroke. Prior to the 1990s, occupational and physical therapists
treating patients with hemiparesis used popular treatment approaches that
lacked evidence of efficacy. Also, medical professionals assumed that recovery
of motor function would plateau at 6 months post-stroke (Dobkin, 2004).
However, there is evidence that, even at the chronic stage, stroke survivors can
improve upper extremity motor skills following rehabilitation interventions
(Taub et al., 1993; Whitall et al., 2000). The therapeutic approaches that have
Occup. Ther. Int. 16(34): 190203 (2009)
Copyright 2009 John Wiley & Sons, Ltd
DOI: 10.1002/oti

Bilateral training

emerged attempt to exploit the plasticity of the nervous system, and both neurophysiologic and behavioral evidence are demonstrating the efficacy of these
approaches (Dobkin, 2004).
One therapeutic technique that has been described at length in the literature
is constraint-induced movement therapy (CIMT) (Taub et al., 1993; Wolf et al.,
2006, 2008). However, this technique has strict inclusion criteria which are only
present in more mildly impaired stroke survivors. Although the most recent
EXCITE trial included both higher functioning and lower functioning subjects (Wolf et al., 2008), the lower functioning subjects were those who had at
least 10 degrees of wrist extension, 10 degrees of thumb abduction and extension
and 10 degrees of finger extension in at least two fingers. This degree of function
is generally considered mildly impaired or higher functioning in clinical
neurorehabilitation practice. Nevertheless, positive results have been achieved
through CIMT, and it is currently the best known upper extremity treatment
for stroke survivors with mild impairment.
Bilateral training has been investigated as a potential rehabilitation intervention, although to a lesser extent than CIMT. Bilateral training is a nonspecific phrase for a number of different training techniques which use both
limbs to complete a task. This review is limited to upper limb bilateral training.
In a meta-analysis, Stewart et al. (2006) found convincing evidence for the
efficacy of bilateral training.
McCombe Waller and Whitall (2008) have argued that, even within a
primarily unilateral training regimen, it is important to include bilateral training. The authors state that, in comparison to unilateral training, bilateral
training is superior for training bimanual activities. Bilateral training has
been used in treating stroke survivors with minimal, moderate and severe arm
impairment. Here, we present a review of bilateral training for post-stroke hemiparesis. First, we will discuss proposed neural mechanisms of bilateral training.
We will then review the current bilateral training studies which have shown
efficacious results for stroke survivors with various upper limb impairment
levels.

Proposed neural mechanisms of bilateral training


Researchers have speculated on the neural mechanisms underlying bilateral
training. Brain mapping techniques, including transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (fMRI), continue to
inform stroke researchers about the brains response to training. According
to the current literature, possible mechanisms underlying improvement
from bilateral training include recruitment of the ipsilateral corticospinal
pathways, increased control from the contralesional hemisphere and a normalization of inhibitory mechanisms. These neural mechanisms are described as
follows.
Occup. Ther. Int. 16(34): 190203 (2009)
Copyright 2009 John Wiley & Sons, Ltd
DOI: 10.1002/oti

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Stoykov and Corcos

Ipsilateral corticospinal pathway


It is well established that there are corticospinal pathways which do not cross
at the pyramidal decussation. The estimated percentage of uncrossed pathways
is approximately 1020%. These uncrossed, ipsilateral pathways have been
implicated as a possible post-stroke recovery mechanism (Chollet et al., 1991),
and some researchers suggested they could be facilitated with bilateral training
(Mudie and Matyas, 2000).
It is well documented that, when both arms are coupled symmetrically,
movements are more temporally and spatially stable than those performed
asymmetrically. In symmetrical movement, there is a propensity towards identical spatial parameters and timing, especially when speed increases. This phenomenon is known as the symmetry constraint (Kelso et al., 1981). Researchers
have proposed that post-stroke bilateral symmetrical movement training may
exploit the symmetry constraint by allowing greater use of the ipsilateral pathways (Cauraugh and Summers, 2005). A study of TMS and fMRI investigating
these pathways concluded that ipsilateral pathways are, in fact, used in congenital hemiparesis (cerebral palsy) if the lesion in the affected hemisphere is large
(Staudt et al., 2002). At present, the role of ipsilateral pathways in post-stroke
recovery upper limb recovery has not been clarified. There is some evidence
indicating that recruitment of the ipsilateral pathways following stroke is associated with a less than optimal motor outcome (Netz et al., 1997).

Activation of healthy (contralesional) hemisphere


There are a variety of manifestations of neural reorganization after a stroke, one
of which is increased activity in the contralesional cortex. In some stroke
patients, contralesional activation increases after injury and then declines as
ipsilesional recovery progresses (Cramer, 2008). The function of increased contralesional activation is the subject of much debate in the stroke literature.
Research in healthy subjects indicates that activation of both hemispheres
is common during complex tasks, as well as tasks performed by the nondominant hand (Debaere et al., 2004). An fMRI study examining the effect of
force amplitude during grip found that both contralateral and ipsilateral sensorimotor cortices in normal subjects had positive increases in percent signal
change and activation volume as a function of increasing force amplitude
(Spraker et al., 2007). As expected, the contralateral hemisphere had a greater
percent signal change and activation volume in comparison to the ipsilateral
hemisphere. An fMRI study examining stroke and normal subjects found that
stroke subjects had increased activation in the contralesional cortex as compared to the healthy controls. The magnitude of contralesional activation was
even greater in the stroke subjects during a more complex task (Schaechter and
Perdue, 2008). Thus, a reasonable explanation for the increase in post-stroke
bilateral cortical recruitment is that, after an injury, the contralesional
Occup. Ther. Int. 16(34): 190203 (2009)
Copyright 2009 John Wiley & Sons, Ltd
DOI: 10.1002/oti

Bilateral training

hemisphere becomes more involved in the control of movements, and this


involvement is greatest in complex tasks. However, it is not known if these
cortical circuits detected by fMRI are facilitory or inhibitory. The contralesional
hemisphere has been implicated in improving post-stroke motor function, particularly following bilateral training (Luft et al., 2004). However, the degree to
which contralesional activation is related to resumption of post-stroke motor
performance remains unclear.
Cortical inhibition and disinhibition
The balance of inhibition and disinhibition between the cortices is disrupted
after a stroke. The affected hemisphere has reduced excitability, while the nonaffected hemisphere has increased excitability. Transcallosal inhibition from the
ipsilesional hemisphere to the contralesional one is greatly decreased (Stinear
et al., 2008), and there are abnormally high levels of inhibition transferred from
the contralesional to the lesioned hemisphere (Murase et al., 2004). Intracortical inhibition is also decreased. In well-recovered stroke survivors, inhibitory
mechanisms return to more normal levels. However, if disturbed inhibitory
mechanisms persist, upper extremity recovery may be negatively impacted.
Researchers contend that a possible neural mechanism underlying post-stroke
functional improvements following bilateral training is the normalization of
inhibitory mechanisms between the hemispheres (Stinear et al., 2008).
Bilateral training
Bilateral training includes a number of different training techniques which use
both limbs to complete a task. One type of training, which is very common in
clinical practice, is assisted bilateral training. The latter involves linking the
two arms together so that the less affected arm holds the affected one while
both move in the same trajectory. Because of lack of evidence, assisted bilateral
movement will not be discussed. We will discuss other bilateral paradigms with
evidence of efficacy including bilateral isokinematic training (BIT), machineassisted bilateral training, bilateral mirror therapy and bilateral priming.
The reader should note that some of the bilateral therapy studies have
used augmented feedback which is feedback that is not inherent to the task.
Feedback may include, for example, auditory cueing using a metronome or
electromyogram-triggered neuromuscular stimulation (e-stim). Further details of
particular studies can be found in Table 1.
BIT
The term bilateral isokinematic training has been applied to bilateral training
where both arms perform unassisted, symmetrical movements (Mudie and
Matyas, 2000). In an attempt to exploit the well-documented systematic bias
Occup. Ther. Int. 16(34): 190203 (2009)
Copyright 2009 John Wiley & Sons, Ltd
DOI: 10.1002/oti

193

Chronic

Chronic

14

25

Subacute
and
chronic

12

Mudie and Matyas


(2000).
Disability and
Rehabilitation
22: 2337.
Whitall et al.
(2000). Stroke
31: 23902395.

Cauraugh and Kim


(2002). Stroke
33: 15891594.

Post-stroke
temporal
phase

Total
(N)

Study

Active
elecgromyogramtriggered
neuromuscular
stimulation

Rhythmic auditory
cueing using a
metronome

None

Adjunctive therapy

Shoulder and elbow

Wrist

Two control groups


both receiving
training in
unilateral wrist
movement of
affected arm only.
One group with
e-stim and
another group
without e-stim.

Whole arm
movements
including distal
extremity

Joints trained

No control group

No control group.
Subjects acted as
own controls during
unilateral training.

Control group training

TABLE 1: Selected key bilateral training studies for post-stroke hemiparesis

Improvements in FMUE,
Wolf motor function
test, strength, range of
motion.
Improvements in box and
block, reaction time,
sustained contraction
favouring bilateral
e-stim group.

Improvements in
observational kinematic
assessment

Outcomes

194
Stoykov and Corcos

Occup. Ther. Int. 16(34): 190203 (2009)


Copyright 2009 John Wiley & Sons, Ltd
DOI: 10.1002/oti

Chronic
and
subacute

Subacute

Chronic

Chronic

44

12

32

Stinear and
Byblow (2004).
Journal of
Clinical
Neurophysiology
21: 124131.
Hesse et al. (2005).
Stroke 36:
19601966.

Bilateral training
was used to
prime motor
cortex prior to
performing tasks
requiring
dexterity.

None

None

None

Adjunctive therapy

Unilateral hand
function activities
only

Electrical stimulation
to wrist extensors
while practicing
unilateral wrist
movement
Unilateral reach and
grasp dowel rod
with affected hand
only.

No control group

Control group training

Larger changes in bilateral


group for FMUE, but
both groups improved.

Improvements in MAS in
the bilateral group.
Decrease in cortical
asymmetry in some
bilateral subjects.
Improvements in FMUE
in both groups. Gains
persisted in priming
group. Normalization of
inhibitory mechanisms
in priming group.

Wrist and forearm

Whole arm
including distal
extremity

Continuous wrist
flexion and
extension for
priming. Actual
training included
unilateral
training for the
distal extremity.

Improvements in FMUE
and increased cortical
excitability noted in
five subjects.

Outcomes

Wrist

Joints trained

e-stim = electrical stimulation; FMUE = Fugl-Meyer test of upper extremity function; MAS = motor assessment scale.

Summers et al.
(2007). Journal
of Neurological
Sciences 252:
7682.
Stinear, et al.
(2008). Brain
131: 13811390.

Post-stroke
temporal
phase

Total
(N)

Study

TABLE 1: Continued

Bilateral training

Occup. Ther. Int. 16(34): 190203 (2009)


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towards spatial and temporal synergy, both arms are used symmetrically
to perform a task. The intention is that the interlimb coupling dynamics
that emerge during bilateral movement will produce more similar parameters
between the two limbs and, thus, enhance performance of the affected one
(Cunningham et al., 2002).
In a controlled case series (N = 12) examining the effect of BIT, individuals
first trained in a unilateral condition before switching to a bilateral condition
(Mudie and Matyas, 2000). The subjects demonstrated improved task performance after switching to bilateral training. The improvement noted was specific to the task being trained. Improvements were noted in the observational
kinematic assessment, an assessment with limited published reliability and
validity.
Cauraugh and Kim (2002) examined a combination of e-stim and symmetrical bilateral movement in mildly impaired, chronic stroke subjects. The study
had three groups including: (1) a control group (training in unilateral wrist
extension exercises without stimulation); (2) a unilateral training group (wrist
exercises augmented with e-stim); and (3) a bilateral training group (wrist exercises augmented with e-stim). They found significant differences in the box and
block score (Mathiowetz et al., 1985), decreased reaction times and improved
sustained muscle contraction capability in favour of the bilateral stimulation
group. The unilateral plus e-stim e group also had significantly better preintervention to post-intervention improvements when compared to the control
group which did not use e-stim. Thus, part of the effect from the bilateral
therapy in this study can be attributed to e-stim which provides some afferent
feedback.
In a short-term (six sessions) comparative study (bilateral versus unilateral)
using 12 mildly impaired subjects, Summers et al. (2007) reported significantly
greater improvements in subjects receiving bilateral training on the motor
assessment scaleupper limb items. The unilateral group made no improvement.
Training was task specific and consisted of reaching and placing a wooden
dowel. TMS was used to measure the volume of a bordered map (a measure of
cortical excitability) representing the extensor communis on both hemispheres.
The cortical map volume of the unaffected hemisphere significantly decreased
in the three bilateral subjects who were evaluated with TMS. This decrease in
map volume indicates that the contralesional hemisphere became less excitable,
possibly because of the normalization of intrahemispheric and interhemispheric
inhibition.
Mirror therapy using bilateral training
Bilateral training augmented with mirror therapy has also shown to be efficacious (Altschuler et al., 1999; Stevens and Stoykov, 2004; Yavuzer et al., 2008).
In mirror therapy, a mirror is set in the saggital plane where the subject views
the less affected arm as if it were the affected one. Mirror therapy can be
Occup. Ther. Int. 16(34): 190203 (2009)
Copyright 2009 John Wiley & Sons, Ltd
DOI: 10.1002/oti

Bilateral training

performed in the bilateral condition where the affected arm is out of view
behind the mirror. The subject is asked to move his affected hand at the same
time as the less affected one. One possible rationale for the success of this
therapy is that the view of the less affected arm, in place of the affected one,
provides a successful movement experience beyond what could otherwise be
achieved (Stevens and Stoykov, 2004).
In a study with subacute stroke patients, Yavuzer et al. (2008) compared
bilateral mirror therapy to a control group which received sham mirror therapy.
In the sham condition, subjects performed the same exercises while viewing the
non-reflecting side of the mirror. It was not clear whether controls practiced
only with their less affected arm or if they practiced bilaterally. Significant
improvements between the groups were found in favour of the mirror therapy
plus bilateral movement in the self-care section of the functional independence
measure, as well as the Brunnstrom stages of motor recovery. In both measures,
the post-intervention score was higher than the pre-intervention one.
Device-driven bilateral training
Many bilateral studies use a device which provides varying levels of assistance
to the paretic arm so that it can perform symmetrical or asymmetrical movements more efficiently. The device may be a low-tech one or a computercontrolled robotic device. One possible advantage of a device is that the
individual can practice many repetitions of rhythmic movement without requiring the full attention of a therapist. Another advantage is that the devices allow
practice with varying levels of support including active, passive and active
assisted movement (Stinear and Byblow, 2004; Hesse et al., 2005), and movement phases can be varied very precisely. In fact, several studies have provided
both in-phase (symmetrical) and anti-phase (asymmetrical) movement training
(Whitall et al., 2000; Luft et al., 2004; McCombe Waller and Whitall, 2004,
2005; Stinear and Byblow, 2004; McCombe Waller et al., 2008).
One group has used a device known as the BATRAC which is associated
with a protocol known as bilateral arm training with rhythmic auditory cueing.
This protocol uses bilateral symmetrical and asymmetrical movement accompanied by rhythmic auditory cueing. After 6 weeks of BATRAC training,
Whitall et al. (2000) reported significant improvement in strength, range of
motion, the Fugl Meyer test of upper extremity motor function (FMUE) (FuglMeyer et al., 1975), and the scores on the University of Maryland arm questionnaire for stroke. Other work by this group has compared BATRAC training for
individuals with non-dominant hemisphere lesions to the same training for
individuals with dominant hemisphere lesions (McCombe Waller and Whitall,
2005). Although both groups improved, the group with dominant hemisphere
lesions had a superior effect. McCombe Waller and Whitall (2004) have also
examined the effect of BATRAC training (which targets the proximal extremity) on the distal extremity. After 6 weeks of BATRAC training targeted to the
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shoulder and elbow, two out of four subjects decreased movement time for
tapping tasks, and a third subject unable to tap at pre-intervention was able to
tap at post-intervention.
Luft et al. (2004) reported on a study using the BATRAC protocol, previously described by Whitall et al. (2000). Bilateral training with rhythmic auditory cueing was compared to dose-matched response therapy (DMRT) which
used neurodevelopmental treatment techniques. The results of the study found
improvements in the FMUE in six of the nine subjects in the BATRAC group,
and no improvements in the DMRT group. All six subjects with FMUE improvements also had increases in contralesional hemispheric activation as documented by fMRI.
Hesse et al. (2005) used a robotic device, known as the Bi-manu-track, to
examine the effect of bilateral symmetrical therapy of the forearm in subjects
in the subacute phase of stroke recovery. The Bi-manu-track group was compared to a group receiving e-stim of the wrist extensors. The Bi-manu-track
group performed 850 bilateral symmetrical movement repetitions per session,
whereas the e-stim group performed 6080 wrist extension movements, if able,
per session. There was significantly greater improvement in the bilateral group.
The increased repetitions per session in the bilateral group might have accounted
for some of the difference. Although the nature of the two treatments does not
allow a fair comparison, the change in FMUE scores for the bilateral group
(average was 16.7) is one of the largest reported in the literature.
Stinear and Byblow (2004) examined changes in measures of motor function
and cortical activity using TMS following a combination of active and passive
bilateral training (APBT). The participants were in the subacute or chronic
phase of stroke recovery. Subjects trained on a simple device, the Rocker, which
coordinated active wrist movement of the unaffected arm with passive movement of the affected one. The subjects were assigned either to symmetrical or
asymmetrical bilateral training, and practiced continuous wrist movement for
1 h per day at a preferred frequency (approximately 1.2 Hz). After training,
results from the TMS evaluation included a decrease in the cortical excitability
of the contralesional hemisphere (decreased cortical map volume) coinciding
with significant improvement on the FMUE in five out of nine subjects.
Bilateral priming
Another bilateral paradigm that has recently appeared in the literature is bilateral priming, a technique which induces cortical excitability prior to motor
practice (Stinear et al., 2008). The bilateral movement is used as preparation
for the brain prior to motor practice of unilateral or bilateral functional tasks.
Stinear et al. (2008) reported on the first bilateral priming study to date. Bilateral priming, which consisted of APBT described earlier via the Rocker device,
was provided to subjects for 1015 min prior to performing tasks requiring hand
dexterity. A control group performed the hand tasks alone. Both groups improved
Occup. Ther. Int. 16(34): 190203 (2009)
Copyright 2009 John Wiley & Sons, Ltd
DOI: 10.1002/oti

Bilateral training

on the FMUE and had increases in cortical excitability in the ipsilesional


hemisphere at post-treatment. However, unlike the control group, the bilateral
priming group continued to improve (at follow-up) on the behavioral measures.
They also demonstrated re-establishment of transcallosal inhibition from the
ipsilesional onto the contralesional cortex and normalization of intracortical
inhibitory mechanisms.

Conclusion
This paper has reviewed selected bilateral training studies that have shown
evidence of efficacy and discussed possible neural mechanisms mediating bilateral training. Symmetrical bilateral arm movement in healthy people has been
well researched in the motor control literature (Kelso et al., 1981; Kelso, 1984;
Jeka and Kelso, 1995; Wenderoth et al., 2003; Swinnen et al., 2004). Post-stroke
bilateral symmetrical movement training aims to exploit the symmetry constraint by coupling both arms together in order to improve performance of the
affected one. Other bilateral training regimes have used a combination of symmetrical and asymmetrical movements.
There are few indicators which suggest the best course of intervention following a stroke based on either the time since stroke or level of impairment.
Stinear et al. (2007) examined stroke survivors undergoing therapy and used
multiple regression to predict functional potential for upper extremity recovery
and to identify optimal treatment options. The model was based on behavioural
and neurophysiologic measures. The latter were used to evaluate corticospinal
tract integrity, and included the presence or absence of motor evoked potentials
(MEPs) induced by TMS, as well as measures of corticospinal tract asymmetry
in the posterior limb of the internal capsule (PLIC) documented by MRI.
According to the predictive model, stroke survivors who retain adequate corticospinal tract integrity, as evidenced by the presence of MEPs following stimulation, should undergo intensive unilateral therapy (such as CIMT). Those
individuals without MEPs but with evidence of relative symmetry in the PLIC
should initially be treated with techniques to induce cortical excitability in the
ipsilesional hemisphere followed by augmented unilateral therapy. Those individuals without evidence of corticospinal tract integrity (as noted by TMS and
MRI measures) are likely to have lower scores on the FMUE. Techniques to
induce general cortical excitability should be provided and then followed with
augmented training which targets both ipsilesional and contralesional cortex.
Examples of the latter include bilateral training with rhythmic auditory feedback or electrical simulation. Although this algorithm was based on basic scientific research, it has little relevance for the ordinary clinician because,
presently, practicing clinicians do not have easy access to fMRI and TMS measures. This is because MRI and TMS equipment is primarily located in research
institutes or universities, and the expenses related to such studies are high.
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Patient has motor evoked potentials


from TMS -or - has individual
finger movement

Patient has absent MEPs -or


has no isolated finger
movement

Constraint Induced Movement


Therapy until hand is functional.
Next stage of therapy is training in
bilateral functional activities.

Look at FMUE score:


= or < 35

>35

Bilateral Priming
followed by
Augmented therapy
which targets both
hemispheres

Bilateral Priming
followed by
Unilateral Therapy
with augmented
feedback

Example: Bilateral
Therapy with
auditory cueing

Example: Unilateral
upper limb training
coupled with e-stim.

FIGURE 1: Post-stroke rehabilitation indications for bilateral and unilateral therapy.

However, clinicians can derive some benefit from this model based on observation. It is well accepted that the lateral corticospinal tract controls hand and
finger movement (Lawrence and Kuypers, 1968). Thus, those individuals with
little or no distal movement are more likely to lack corticospinal tract integrity
and might benefit more from bilateral training. Also, mildly impaired subjects
are likely to benefit from practice of bilateral tasks requiring bimanual dexterity
as this type of training is more suitable for improving outcomes in activities of
daily living. Figure 1 presents a flow chart for determining bilateral versus unilateral therapy based on the presence of hand movement and FMUE scores.
Researchers have cautioned against using an exclusively unilateral training
paradigm (Rose and Winstein, 2005). This is because when both arms move
together, there is a temporal component which is qualitatively different than if
the same task was performed with exclusive unilateral movement. Thus, some
types of bilateral training or priming might be appropriate for any level of poststroke impairment. In the future, access to neurophysiologic measures may
inform clinicians more specifically about brain recovery. This information may
help clinicians be more systematic about treatment selection.
Occup. Ther. Int. 16(34): 190203 (2009)
Copyright 2009 John Wiley & Sons, Ltd
DOI: 10.1002/oti

Bilateral training

Acknowledgement
This work was supported by a pre-doctoral fellowship for the first author from
the American Heart Association (AHA grant no. 0610001Z) as well as NIH
grants R01 NS28127 and R01 NS40902 for the second author.

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DOI: 10.1002/oti

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