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Comparison of Bilateral and Unilateral Training for Upper Extremity


Hemiparesis in Stroke

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DOI: 10.1177/1545968309338190 · Source: PubMed

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Comparison of Bilateral and Unilateral Training for Upper Extremity Hemiparesis in Stroke
Mary Ellen Stoykov, Gwyn N. Lewis and Daniel M. Corcos
Neurorehabil Neural Repair 2009 23: 945 originally published online 16 June 2009
DOI: 10.1177/1545968309338190

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Neurorehabilitation and
Neural Repair
Volume 23 Number 9
November/December 2009 945-953
© 2009 The Author(s)

Comparison of Bilateral and Unilateral Training 10.1177/1545968309338190


http://nnr.sagepub.com

for Upper Extremity Hemiparesis in Stroke


Mary Ellen Stoykov, PhD, Gwyn N. Lewis, PhD, and Daniel M. Corcos, PhD

Background. Upper extremity hemiparesis is the most common poststroke disability. Longitudinal studies have indicated that 30% to 66%
of stroke survivors do not have full arm function 6 months poststroke. One promising treatment approach is bilateral training. To date,
no randomized, blinded study of efficacy comparing 2 groups (bilateral training vs unilateral training) using analogous tasks has been
performed in chronic stroke survivors with moderate upper extremity impairment. Objective. To compare the effectiveness of bilateral
training with unilateral training for individuals with moderate upper limb hemiparesis. The authors hypothesized that bilateral training
would be superior to unilateral training in the proximal extremity but not the distal one. Methods. Twenty-four subjects participated in a
randomized, single-blind training study. Subjects in the bilateral group (n = 12) practiced bilateral symmetrical activities, whereas the
unilateral group (n = 12) performed the same activity with the affected arm only. The activities consisted of reaching-based tasks that
were both rhythmic and discrete. The Motor Assessment Scale (MAS), Motor Status Scale (MSS), and muscle strength were used as
outcome measures. Assessments were administered at baseline and posttraining by a rater blinded to group assignment. Results. Both
groups had significant improvements on the MSS and measures of strength. The bilateral group had significantly greater improvement
on the Upper Arm Function scale (a subscale of the MAS-Upper Limb Items). Conclusion. Both bilateral and unilateral training are
efficacious for moderately impaired chronic stroke survivors. Bilateral training may be more advantageous for proximal arm function.

Keywords:  Stroke; Bilateral; Upper extremity

S troke is a leading cause of disability in the United States


with more than 1 100 000 Americans reporting poststroke
functional limitations.1 Upper extremity hemiparesis is one of
dissimilar training protocols,10,15-17 whereas others have com-
pared unilateral versus bilateral training with mildly impaired
subjects.6,8
the most common conditions requiring extensive rehabilita- There are no universally accepted specifications in the lit-
tion. Approximately 30% to 36% of all individuals with hemi- erature for stratifying subjects. Kwakkel et al2 have deter-
paresis have poor arm function 6 months poststroke.2 mined that, at 4 weeks poststroke, a stroke survivor with a
Therapeutic techniques are needed to address the problem. Fugl-Meyer Test of Arm Function Upper Extremity (FMUE)
One technique that has been described at length in the litera- score of less than 19 has a 9% probability of developing
ture is constraint-induced movement therapy.3-5 Although dexterity. We used this prognostic indicator as a cutoff for
positive therapeutic benefits have been demonstrated, a major stroke survivors with “severe” upper extremity impairment.
limitation is that the majority of stroke survivors are not eli- Individuals with severe impairments typically have no use of
gible because of the strict inclusion criteria that specifically their affected arm. An upper-level FMUE score of 40 to 60
target patients with mild impairment. was determined as “mildly” impaired. Typically, these indi-
Alternative treatments are needed that target more impaired viduals have some degree of wrist and finger extension and
survivors. One example of an alternative treatment is bilateral have the potential to perform fine motor activities with their
arm training. This promising technique has been shown to be affected hand. These individuals are eligible for constraint-
efficacious not only with stroke survivors who are only mildly induced therapy. We used the middle range of FMUE scores
impaired6-9 but also those with moderate10-13 and severe motor (19-40) as our definition of “moderately” impaired. Moderately
impairments.14,15 To date, however, no study comparing 2 dif- impaired individuals may or may not use their arm but have,
ferent training groups has addressed the comparative efficacy at the very least, the potential to use the arm as a stabilizer, and
of bilateral training versus unilateral training using similar some may be able to use the arm as a functional assist.
treatment activities for chronic, moderately impaired patients. Researchers have suggested that bilateral training may be
Some studies have used unilateral control groups with more advantageous for the proximal limb.18 This speculation is

From the Department of Kinesiology and Nutrition, the University of Illinois at Chicago (MES, DMC); Sensorimotor Performance Program, Rehabilitation
Institute of Chicago, Chicago, Illinois (MES, GNL); and the Health and Rehabilitation Research Centre, AUT University, Northcote, Auckland, New Zealand
(GNL). Address correspondence to Mary Ellen Stoykov, PhD, Department of Kinesiology and Nutrition, the University of Illinois at Chicago, 1919 W Taylor
Street, 690 CMET, Chicago, IL 60612. E-mail: mphillips@ric.org.

945
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946   Neurorehabilitation and Neural Repair

based on the presence of descending motor pathways that are Table 1


bilateral and support postural and proximal limb function.19,20 Inclusion and Exclusion Criteria for Subjects
Also, there is recent evidence that bilateral training is better Inclusion Criteria Exclusion Criteria
for proximal control than constraint-induced therapy.21 Thus,
we hypothesized that the bilateral training group would FMUE score between, and Symptomatic cardiac failure or
improve more in proximal function than the unilateral training    inclusive of, 19 and 40    unstable angina
Cortical or subcortical lesion Lesion in cerebellum or brainstem
group. Chronic—at least 6 months
The bilateral training protocols reported in the literature are    since onset
diverse. A recent review organized protocols presented in Ability to follow 2 step commands Uncontrolled hypertension
training studies into the following categories: (a) repetitive No evidence of field cut— Inability to give consent
reaching with hand fixed, (b) isolated muscle repetitive train-    (confrontational field testing)
No evidence of neglect Significant orthopedic or pain
ing, and (c) whole arm functioning.22 In the current study, the    (H-cancellation test)    conditions in affected upper
tasks emphasized repetitive reaching with the hand fixed as    extremity
well as whole arm functioning. For the latter, the requirements Age 18 to 80 years Severe obstructive pulmonary disease
of the distal musculature were minimized by having the thera-
Abbreviation: FMUE, Fugl-Meyer Test of Arm Function Upper Extremity.
pist place the objects in the hand and assist with grip mainte-
nance and release. Thus, whole arm functioning tasks required
no or very minimal grasp or manipulation. 2 training groups. Within each group of 12 subjects, a random-
Rhythmic auditory cueing has been used in a number of ized computer-generated list provided group assignment into
bilateral training studies, and it is coupled with repetitive bilateral or unilateral training groups. Both subsets of impair-
reaching with hand-fixed activities.10-13,23 Thaut et al24 suggest ment levels had 6 subjects in the unilateral training group and 6
that rehabilitation professionals explore rhythmic movement in the bilateral training group. The first author enrolled subjects
for upper extremity rehabilitation based on findings demon- and provided both treatment interventions.
strating significantly improved kinematic measures in a rhyth- The study was conducted over 2 years. The institutional
mic condition when compared with a discrete condition in review boards of both Northwestern University and the University
individuals with chronic stroke. Rhythmic and discrete move- of Illinois at Chicago approved study procedures. Written
ments are controlled by somewhat different patterns of neural informed consent was obtained prior to enrollment. To determine
activation.25 Evidence from functional magnetic resonance that subjects did not have a lesion in the cerebellum or brainstem,
imaging (fMRI) studies confirms that there is stronger activity MRI scans from previous studies were examined with the sub-
in contralateral sensorimotor cortex during rhythmic move- jects’ consent and/or subjects gave permission for their physi-
ment when compared with discrete movement.25 However, cians to respond to a letter requesting lesion site information.
discrete movement has a more extensive network that includes
structures associated with motor planning. Thus, we used both
Training
types of movement in our training protocols.
Both groups participated in an 8-week training protocol.
Dependent variables were measured at baseline and immedi-
Methods ately posttraining. Both groups received 3 training sessions of
1 hour duration per week, amounting to 24 hours of training
Subjects for all subjects. If a session was missed during any given
Twenty-four participants were involved in the training study. week, an extra session was added to the following week or at
Sample size was determined by reviewing previous training the end of the 8 weeks. At least 24 hours elapsed between
studies that had demonstrated significant improvements in func- consecutive training sessions.
tion in individuals with upper extremity hemiparesis.6,7,10,26-31 We chose tasks that were similar to or had similar move-
Inclusion criteria included an FMUE score of 19 to 40 (moder- ment patterns to those performed in other bilateral or unilateral
ate impairment), at least 6 months poststroke, and no evidence reach training studies.13,16,32,33 Tasks were selected because
of involvement in the cerebellum or brainstem. A full list of they could easily be completed in both the unilateral and bilat-
inclusion and exclusion criteria is included in Table 1. Subjects eral conditions (see Table 2 for details). Both groups had the
were recruited from the Clinical Neuroscience Registry, which same amount of time in training on the affected upper extrem-
provides researchers at Northwestern University and the ity. There were a total of 6 training tasks that incorporated both
Rehabilitation Institute of Chicago with a pool of possible discrete movements (2 tasks) and rhythmic movements (4
stroke subjects. Prior to randomization, the participants were tasks) paced by a metronome.
stratified into 2 impairment levels based on FMUE scores. The Subjects performed the tasks using blocked practice.
more impaired subset of subjects had scores ranging from 19 Individual instructions were relative to each task, such as
through 28 on the FMUE, whereas the less impaired subset “reach and point to the target and touch the target in time with
of subjects had scores from 29 through 40. Stratification was the beat of the metronome.” For most tasks, subjects initially
performed to minimize differences in impairment between the performed 20 repetitions (2 sets of 10 repetitions) and then

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Stoykov et al / Bilateral Versus Unilateral Training   947  

Table 2 patterns. Our rationale for increasing speed is that there is


Task Protocol fMRI evidence that increasing the rate of synchronized move-
ment facilitates an increase in brain activity in the sensorimo-
Unilateral Treatment Activities Bilateral Treatment Activities tor cortex.35 The number of movements and the frequencies for
1. Pushing and pulling activity 1. Pushing/pulling with both arms each task were recorded at each session.
(open/close drawer) (open/close 2 identical drawers)
Rhythmic task Rhythmic task Dependent Variables
2. Wipe a table with a towel using 2. Wipe a table with both arms using
the affected arm both arms symmetrically Our objective was to compare the outcomes of bilateral and
Discrete task Discrete task
unilateral training for the proximal upper extremity using analo-
3. One arm cycling using 3. Bilateral in-phase cycling
BTE 181 using BTE gous treatment activities in moderately impaired stroke survi-
Rhythmic task Rhythmic task vors. Thus, primary outcome measures that differentiated
4. Reaching and placing objects. 4. Bilateral reaching and placing proximal and distal function were selected. They included the
Moving small and medium-sized objects. Moving 2 identical small Motor Assessment Scale (MAS-Upper Limb Items)36 and the
grocery items from kitchen or medium-sized grocery objects
counter to shelves using only from countertop to shelf with
Motor Status Scale (MSS).37 The MAS-Upper Limb Items has 3
affected arm both hands separate subscales: Upper Arm Function, Hand Movements, and
Discrete task Discrete task Advanced Hand Activities.36,38 Each subscale consists of 6 items
5. Shoulder and elbow coupling. 5. Bilateral shoulder and elbow with increasing difficulty. A score of 0 to 6 is possible for each
Aim to target with affected hand coupling. Aim with both hands
subscale, with a total score of 18 for the MAS-Upper Limb
in various areas of work space to parallel targets (using varying
(using varying levels of arm levels of arm support, postural Items. We used all 3 scales because they are specific for proximal
support, postural sets, and sets, and positions in respect to and distal function. Upper Arm Function addresses shoulder
positions in relation to gravity). gravity). Includes a total of stability and movement at the task level. Hand Movement exam-
Includes a total of 4 subtasks 4 subtasks ines tasks that require gross distal function (eg, picking up a cup).
Rhythmic task Rhythmic task
6. Elbow extension during 6. Bilateral elbow extension during
Advanced Hand Activities addresses fine motor function.
horizontal reach horizontal reach The MSS is divided into 2 subscales including the Shoulder/
Rhythmic task Rhythmic task Elbow scale and the Wrist/Hand scale. It is based on the
FMUE, and the correlation between the 2 scales is high.37

However, the MSS has more items than the FMUE, and it
gradually increased this to 40 repetitions (4 sets of 10). An focuses on isolated movement while excluding synergy. The
exception to this was the task of opening and closing drawer(s), MSS-Shoulder/Elbow scale is a comprehensive examination
which all subjects performed 100 times per session. The task of the movements of the shoulder, elbow, and forearm. The
of reaching to different areas of the workspace included 4 MSS-Wrist/Hand scale examines hand and wrist movement
separate subtasks, each requiring approximately 5 minutes with more specificity than the FMUE hand section.
with a total task time of 20 minutes. Time taken on the other 5 Secondary outcome measures included selected measures
tasks approximated 5 to 6 minutes each. We chose to provide of arm strength. Shoulder, elbow, and wrist strength were mea-
a 1 or 2 minute rest period between each task because that was sured using a Chatillion MSC Muscle Strength Comparator
the time required to set up the next task. A 30-second rest was Dynamometer (Ametek, Inc, Largo, FL). Specifically, the
provided between each set. Thus, subjects were active for most tested muscle groups were flexors/extensors and external/
of the session. The order of the tasks was pseudo-randomized internal rotators of the shoulder, flexors/extensors of the
by the training therapist on a daily basis. elbow, and flexors/extensors of the wrist. Grip strength (finger
To set the initial movement frequency on the first day of flexor muscle strength) was measured using a standard, adjust-
treatment, subjects were given several trials to perform the able-handle JAMAR hydraulic hand dynamometer (JA Preston
activity, and the frequency of the metronome was increased. Corp, Jackson, MI).
The subject was given the instruction “move to the beat of the Primary and secondary outcome measurements were admin-
metronome.” When the subject was unable to keep up with the istered at baseline, 1 to 3 weeks before initiation of the training,
metronome, the frequency of the previously successful task and at posttraining, within 1 week after the training was com-
was used for training. Frequencies ranged from 0.25 to 1.5 Hz pleted. Measurements were administered using a single rater
depending on the ability of the subject. who was blinded to group assignment and methodology of the
Therapeutic challenge throughout the 8-week training study. The rater was trained on the assessment measures prior
period was increased by increasing speed requirements for the to commencement of the study. At the conclusion of the study,
rhythmic tasks, decreasing external support of the affected the rater reported that the blind was 100% successful and that
arm, and increasing cues to improve quality of movement she was not able to guess group assignment of any subjects.
(knowledge of performance). Knowledge of performance has
been shown to be more effective than knowledge of results for
Analysis
changing poststroke motor patterns.34 Although increasing the
speed of movement was a goal, subjects were not encouraged Because the behavioral scales are ordinal in nature, we
to increase speed if they were using compensatory movement analyzed the MAS and MSS using nonparametric statistics.
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948   Neurorehabilitation and Neural Repair

Table 3 no significant differences between preintervention and postint-


Baseline Participant Characteristics ervention (Figure 1A-D).
Bilateral Unilateral
There were no between-group differences for the MSS for
Characteristic Group Group any of the 3 scales. Figure 2 presents the means and standard
errors of the preintervention and postintervention data for the
Age (years), mean (SD) 63.8 (12.6) 64.75 (11.1) MSS scales. Results revealed significant preintervention to
Years poststroke, mean (SD) 9.5 (5.4) 10.2 (10.1)
Fugl-Meyer Assessment Score, mean (SD)a 28.75 (5.95) 27.16 (4.8)
postintervention changes for all 3 scales for both the bilateral
Male 9 7 and unilateral groups. The MSS-Total scale detected significant
Female 3 5 preintervention to postintervention changes for the bilateral
Married 5 4 group (P = .003) and the unilateral group (P = .002), indicating,
Paresis of prestroke dominant side 7 7 respectively, a 14% and 19% improvement (Figure 2A). The
Cortical stroke 5 2
Subcortical stroke 2 4
MSS-Shoulder/Elbow scale revealed improvement for the
Cortical and subcortical 5 6 bilateral group (P = .002) and the unilateral group (P = .002),
Race with a 14% improvement in each group (Figure 2B). The MSS-
   White 8 11 Wrist/Hand scale showed significant improvement for both the
   African American 3 1 bilateral (P = .045) and unilateral (P = .005) groups, with a
   Hispanic 1 0
14% and a 26% improvement, respectively (Figure 2C).
a
Maximum score, 66. Higher scores indicate better function.
Secondary Outcomes
Outcomes from the behavioral scales (difference between pre- There was no evidence for a beneficial effect of bilateral
intervention scores and postintervention scores) were com- training, when compared with unilateral training, in the mea-
pared between the bilateral and unilateral training groups sures of arm strength because both groups improved in
using the Mann–Whitney U test. Preintervention and postint- strength measures (Figure 3). There were no significant inter-
ervention data from each group were then analyzed separately actions with group for any of the strength measures (all P >
using Wilcoxon signed rank tests to determine if there was a .05). There were significant main effects of time found for
pre–post training effect within groups. Strength measurements shoulder flexion (P = .002), wrist flexion (P = .029), and wrist
were analyzed using 3-way repeated-measures analysis of extension (P = .05), indicating higher strength measures
variances with factors of group, time, and impairment level. following training (see Figure 3).
All analyses were calculated using the software package SPSS
15.0 (SPSS, Inc, Cary, NC). An α level of .05 was set for all
analyses.
Discussion
The present study is important because, to our knowledge,
Results it is the first intervention study to compare the outcome of
equivalent unilateral and bilateral training conditions in sepa-
Baseline Characteristics rate groups of subjects with moderate upper extremity hemipa-
resis. Significant differences were found between the bilateral
Table 3 presents baseline characteristics of the 24 partici- and unilateral groups in improvements in function measured
pants. Mann–Whitney U tests revealed no between-group dif- by the MAS-Upper Arm Function subscale. However, there
ferences in age, years poststroke, or baseline FMUE score. were no between-group differences in the MSS or in strength
measures. Both groups significantly improved from baseline
Primary Outcomes to posttreatment in these outcome measures.

There was evidence of a superior effect of bilateral training


Benefits of Bilateral Training
in the MAS. Figure 1A-D presents the mean and standard error
for all 4 MAS scales. A Mann–Whitney U test for the MAS- Previously, comparisons of unilateral and bilateral training
Upper Arm Function scale (Figure 1A) revealed a significant have documented positive effects for bilateral training over
between-groups effect (P = .021), with the bilateral group hav- unilateral training, but these studies have only examined
ing a higher mean change than the unilateral group. There were mildly impaired subjects.6,9 For example, Summers et al9 com-
no significant differences between the bilateral and unilateral pared a 1-week training course of either unilateral or bilateral
treatment groups for any other MAS scale (all P > .05). training using the MAS as the outcome measure. Both the
There were significant preintervention to postintervention present study and Summers et al found significantly greater
changes detected in the bilateral group for the MAS-Upper improvement in the bilateral groups on selected measures
Arm Function scale (P = .014; Figure 1A) and the MAS-Upper from the MAS. The training protocol of the latter study com-
Limb Items (P = .02; Figure 1D). The changes represent a 27% prised 1 whole arm functioning task. Improvement was most
and 18% improvement, respectively. The unilateral group had evident in the MAS-Upper Limb Items scale, which evaluates

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Stoykov et al / Bilateral Versus Unilateral Training   949  

Figure 1
Motor Assessment Scales (MAS) Preintervention and Postintervention Group Means and Standard Errors

Note: MAS-Upper Limb Items (D) is the combined score of the 3 scales (A-C). Note that scales are different values. *Significant at P < .05.

the entire arm. It should be noted that the subjects in this study unilateral group were more likely to report greater ease with
were at a much higher level with a mean baseline MAS-Upper activities having more distal requirements (ie, grasping com-
Arm Function scale score of 5.5 out of a possible 6, compared munion between the fingers).
with 1.8 for subjects in the present study. Cauraugh and Kim6 Some studies, investigating bilateral training for lower func-
showed a benefit of bilateral training for the wrist over unilat- tioning subjects, have used training tasks for control groups that
eral training in mildly impaired subjects, but this was for distal were not comparable with the bilateral tasks.10,15,17 For example,
function. When comparing the 3 studies, it is clear that the neurodevelopment treatment has been used as the control inter-
beneficial differential effect of bilateral training over unilateral vention in 2 studies.10,17 Another study used electric stimulation
training was most evident in the portion of the limb that was for control treatment.15 In this study, the control electric stimu-
emphasized in the training protocols. lation group performed 60 to 80 wrist extension repetitions
Using the standards reported by van der Lee et al,39 the dif- per session compared with 800 forearm and wrist repetitions
ference in the change score of the MAS-Upper Arm Function performed by the experimental group who received bilateral
scale between the groups was 8.6% of the total scale, which robotic training. Therefore, differences in the intensity of the
approaches the minimal clinical important difference of 10%. training also could explain why the bilateral groups in both stud-
Thus, the difference is clinically relevant to some of the sub- ies had a superior outcome. Our protocol of including the same
jects in the bilateral group. After training, some subjects in the training tasks in the unilateral and bilateral treatment groups is
bilateral training group reported that it was easier to perform a superior test of the benefits of bilateral training as it allows for
activities such as bathing and carrying objects. Subjects in the a direct comparison between the 2 training modalities.

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950   Neurorehabilitation and Neural Repair

Figure 2 Figure 3
Motor Status Scales (MSS) of Preintervention and Shoulder and Wrist Strength Measures
Postintervention Group Means and Standard Errors

Note: MSS-Total scale (A) is the combined score of the 2 scales (B and C). Note: *P < .05, **P < .01.
*P < .05, **P < .01.

Our results can also be compared with unilateral training to the improvements in distal movement found in the present
studies that have used equivalent outcome measures. One study that were not manifest in the robotics-based study.
study, using a robotics-based upper limb intervention (N = 42), The improvements in distal movement found in the present
reported a 6% improvement in the MSS.40 In comparison, the study are similar to a previous study that also found changes
present study found a 14% and 19% change in the bilateral and in distal movement following bilateral training targeting only
unilateral groups, respectively. This difference is partially due the proximal arm.11 These authors speculated that changes in

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Stoykov et al / Bilateral Versus Unilateral Training   951  

distal movement were the result of neural mechanisms inherent study reported evidence of normalization of inhibitory mecha-
in bilateral training. In the present study, there were distal nisms following rhythmic bilateral symmetrical movements of
improvements in both the bilateral and unilateral groups. the wrist.48 This study was unique as bilateral movement was
Therefore, the mechanism cannot be specific to bilateral train- used as a motor priming technique prior to training in func-
ing. We can speculate that the mechanism may be because of the tional hand tasks. In comparison to a control group performing
effects of rhythmic, synchronized movement, which, according only functional tasks, the bilateral priming group demon-
to Ackerley et al,41 facilitates a generalized increase in cortical strated reestablishment of interhemispheric inhibition from the
excitability, possibly leading to use dependent plasticity. ipsilesional on to the contralesional cortex as well as normal-
Results of the MAS-Upper Arm Function scale indicated ization of short-interval intracortical inhibition in the contral-
significant differences between the bilateral and unilateral esional hemisphere. These changes in inhibitory mechanisms
groups; however, the results of the MSS-Shoulder/Elbow scale are most likely responsible for the decrease in excitability of
detected no such differences. The differences in findings may be the contralesional cortex.
because of the characteristics of the respective scales and which Some of the previously reported beneficial effects of bilat-
component(s) of movement they measure. The MAS-Upper eral training10-13 and that seen in our study may be, in part,
Arm Function scale has only 6 items and measures the stability because of neural mechanisms controlling rhythmic move-
and movement of the shoulder in various postures including ment. Synchronized movement to a beat produces a general-
supine, sitting, and standing. Because scores on this scale range ized increase in cortical excitability, not exclusive to the
from 0 to 6, improvement on the scale requires a considerable cortical areas associated with the muscle being trained.41
increase in trunk and shoulder stability. The improvement on the Neurophysiological studies have also indicated that both bilat-
MAS-Upper Arm Function scale for the bilateral group is prob- eral and unilateral synchronized movements facilitate cortical
ably because of increased proximal stability. In contrast, the excitability.41,49 The increased cortical excitability during
MSS-Shoulder/Elbow scale measures the magnitude and con- rhythmic movement may result in longer-term improvements
trol of a variety of isolated shoulder and elbow joint movements in synaptic efficacy in the motor cortex. These neural changes
in unsupported sitting. The total possible score is 40 points. provide optimal conditions for learning a motor task and can
Thus, the MSS-Shoulder/Elbow scale detects improvements in account for translation to nonrhythmic movement conditions.
isolated joint movement. The absence of a differential bilateral Indeed, there is ample evidence documenting improvements in
effect on the MSS may indicate that both bilateral and unilateral behavioral measures after rhythmic movement training for a
training are efficacious for training of isolated joint motion. number of neurorehabilitation populations.11-13,50-55 Further
evidence in support of rhythmic movement includes a bilateral
Possible Mechanisms of Bilateral Training training study that did not use rhythmic movement and subse-
quently found no improvements following a course of bilateral
In support of the hypothesis that greater improvements in the training.56 However, others have speculated that discrete
bilateral group in the MAS-Upper Arm Function scale are movement may be more beneficial to bilateral training than
related to improved trunk stability, a study examining the effect rhythmic movement.57 Future studies should compare discrete
of upper extremity exercises on the trunk found that a bilateral and rhythmic training with auditory feedback in both unilat-
symmetrical exercise produced greater electromyography activ- eral and bilateral conditions to more specifically identify the
ity in the trunk muscles than unilateral exercises.42 Trunk stabil- effective components of rehabilitation protocols.
ity is extremely important to proximal upper extremity control.
Sitting unsupported or standing while reaching symmetrically
with both arms promotes trunk extension43 and requires signifi- Study Limitations
cantly more coactivation in the trunk musculature. Physical The sample size was small and may have affected the abil-
therapists have used bilateral symmetrical arm exercises to ity to detect differences between the groups in the MSS. It is
improve core stabilization in a variety of populations.44 Also, also important to note that, although the rater was blinded to
others have indicated that changes in postural stability can group assignment, the principal investigator enrolled subjects,
improve poststroke upper extremity control.45 provided the training, and analyzed the data. This could intro-
Neural mechanisms underlying bilateral training have been duce bias in the delivery of treatment. We believe this is
speculated on. Bilateral movement training may facilitate unlikely, however, because both groups improved equally on
rebalancing of the asymmetry of poststroke hemispheric corti- the majority of measures. Another limitation is that restraining
comotor excitability. Typically, the contralesional cortex of the trunk did not include a uniform method such as a piece
increases in excitability and the lesioned cortex decreases.46 of equipment. Instead, the therapist used verbal or tactile cues
Rebalancing of hemispheric asymmetry occurs because of a to restrain subjects.
change in inhibitory mechanisms including both short interval
intracortical inhibition and interhemispheric inhibition. In
Conclusion
several bilateral training studies, a decrease in cortical excit-
ability in contralesional motor cortex was associated with an We concur with previous studies that have found bilateral
improvement in motor skill of the affected arm.9,47 A recent training to be efficacious for stroke survivors.6-15 We have

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952   Neurorehabilitation and Neural Repair

extended the bilateral training research findings by including a   9. Summers JJ, Kagerer FA, Garry MI, Hiraga CY, Loftus A, Cauraugh JH.
unilateral training group that performed nearly identical activities. Bilateral and unilateral movement training on upper limb function in
chronic stroke patients: A TMS study. J Neurol Sci. 2007;252:76-82.
Although Summers et al9 found significant improvements in a 10. Luft AR, McCombe-Waller S, Whitall J, et al. Repetitive bilateral arm
short-term bilateral versus unilateral training study with mildly training and motor cortex activation in chronic stroke: a randomized con-
impaired subjects, our results also suggest a superior outcome trolled trial. JAMA. 2004;292:1853-1861.
with long-term bilateral training with subjects who were much 11. McCombe Waller S, Whitall J. Fine motor control in adults with and without
more impaired. Our working hypothesis was that there would be chronic hemiparesis: baseline comparison to nondisabled adults and effects
of bilateral arm training. Arch Phys Med Rehabil. 2004;85:1076-1083.
differences between the 2 groups in proximal arm improvement. 12. McCombe Waller S, Whitall J. Hand dominance and side of stroke affect
However, the hypothesis is only partially supported as both rehabilitation in chronic stroke. Clin Rehabil. 2005;19:544-551.
groups improved on the MSS scales. We also had secondary find- 13. Whitall J, McCombe Waller S, Silver KH, Macko RF. Repetitive bilateral
ings of improvement in distal function, which, although unex- arm training with rhythmic auditory cueing improves motor function in
pected, confirmed results of previous studies that investigated chronic hemiparetic stroke. Stroke. 2000;31:2390-2395.
14. Hesse S, Schulte-Tigges G, Konrad M, Bardeleben A, Werner C. Robot-
bilateral proximal training and distal movement outcomes.11 assisted arm trainer for the passive and active practice of bilateral forearm
Previous studies have examined the effect of bilateral training and wrist movements in hemiparetic subjects. Arch Phys Med Rehabil.
on unilateral activities rather than on bilateral ones.22 This is, in 2003;84:915-920.
part, because of an absence of motor assessments dedicated to 15. Hesse S, Werner C, Pohl M, Rueckriem S, Mehrholz J, Lingnau ML.
bimanual performance. More information about bilateral skill Computerized arm training improves the motor control of the severely
affected arm after stroke: a single-blinded randomized trial in two centers.
may better differentiate the benefits of bilateral versus unilateral Stroke. 2005;36:1960-1966.
training. It is likely that both unilateral and bilateral training 16. Desrosiers J, Bourbonnais D, Corriveau H, Gosselin S, Bravo G.
should be used during stroke rehabilitation. Indeed, others have Effectiveness of unilateral and symmetrical bilateral task training for arm
provided evidence that exclusive unilateral training may limit an during the subacute phase after stroke: a randomized controlled trial. Clin
individual’s movement repertoire.58 The amount of time spent on Rehabil. 2005;19:581-593.
17. McCombe Waller S, Liu W, Whitall J. Temporal and spatial control follow-
each may be based on individual clinical presentations and goals. ing bilateral versus unilateral training. Hum Mov Sci. 2008;27:749-758.
18. Lewis GN, Byblow WD. Neurophysiological and behavioural adaptations
to a bilateral training intervention in individuals following stroke. Clin
Acknowledgments Rehabil. 2004;18:48-59.
19. Bawa P, Hamm JD, Dhillon P, Gross PA. Bilateral responses of upper limb
This study was supported by an AHA predoctoral fellow- muscles to transcranial magnetic stimulation in human subjects. Exp Brain
ship, No. 0610000Z, and NIH grants RO1 NS28127 and RO1 Res. 2004;158:385-390.
NS40902. The authors thank James Cauraugh, PhD, for his 20. Colebatch JG, Rothwell JC, Day BL, Thompson PD, Marsden CD.
Cortical outflow to proximal arm muscles in man. Brain. 1990;113(pt
insightful comments on an earlier draft of this manuscript.
6):1843-1856.
21. Lin KC, Chang YF, Wu CY, Chen YA. Effects of constraint-induced
therapy versus bilateral arm training on motor performance, daily func-
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