Motor learning, retention and transfer after virtual-reality

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Physiotherapy xxx (2012) xxx–xxx
Motor learning, retention and transfer after virtual-reality-based training
in Parkinson’s disease – effect of motor and cognitive demands of games:
a longitudinal, controlled clinical study夽
Felipe Augusto dos Santos Mendes a,b,c,∗ , José Eduardo Pompeu a,b ,
Alexandra Modenesi Lobo a,b , Keyte Guedes da Silva a,b , Tatiana de Paula Oliveira b ,
Andrea Peterson Zomignani c , Maria Elisa Pimentel Piemonte a,b
a
Department of Neuroscience and Behaviour, Institute of Psychology, University of São Paulo, São Paulo, Brazil
b Department of Physical Therapy, Faculty of Medical Science, University of São Paulo, São Paulo, Brazil
c Faculty of Physical Therapy, Padre Anchieta University, Jundiai, Brazil
Abstract
Objectives To evaluate the learning, retention and transfer of performance improvements after Nintendo Wii FitTM training in patients with
Parkinson’s disease and healthy elderly people.
Design Longitudinal, controlled clinical study.
Participants Sixteen patients with early-stage Parkinson’s disease and 11 healthy elderly people.
Interventions Warm-up exercises and Wii Fit training that involved training motor (shifts centre of gravity and step alternation) and cognitive
skills. A follow-up evaluative Wii Fit session was held 60 days after the end of training. Participants performed a functional reach test before
and after training as a measure of learning transfer.
Main outcome measures Learning and retention were determined based on the scores of 10 Wii Fit games over eight sessions. Transfer of
learning was assessed after training using the functional reach test.
Results Patients with Parkinson’s disease showed no deficit in learning or retention on seven of the 10 games, despite showing poorer
performance on five games compared with the healthy elderly group. Patients with Parkinson’s disease showed marked learning deficits on
three other games, independent of poorer initial performance. This deficit appears to be associated with cognitive demands of the games which
require decision-making, response inhibition, divided attention and working memory. Finally, patients with Parkinson’s disease were able to
transfer motor ability trained on the games to a similar untrained task.
Conclusions The ability of patients with Parkinson’s disease to learn, retain and transfer performance improvements after training on the
Nintendo Wii Fit depends largely on the demands, particularly cognitive demands, of the games involved, reiterating the importance of game
selection for rehabilitation purposes.
© 2012 Chartered Society of Physiotherapy. Published by Elsevier Ltd. All rights reserved.
Keywords: Parkinson’s disease; Motor learning; Virtual reality; Executive function; Rehabilitation; Transfer
Introduction
Motor rehabilitation can be characterised as a process of
‘relearning’ how to move to respond satisfactorily to the
夽
This paper is based on a paper presented at WCPT in Amsterdam 2011.
Corresponding author. Address: Department of Physical Therapy, Faculty of Medical Science, University of São Paulo, Rua Cipotânea, 51, São
Paulo 05360-160, SP, Brazil. Tel.: +55 1130917463.
E-mail address: [email protected] (F.A.d.S. Mendes).
∗
demands of daily living [1], and is based on the premise
that training leads to improved performance both in terms
of acquiring new skills and adapting or refining previously
acquired skills [2]. Thus, knowledge on the effectiveness
of the motor learning process in patients with Parkinson’s
disease is pivotal for planning more effective rehabilitation
strategies [3].
Evidence shows that the basal ganglia, particularly the
striatum, play a role in the learning process [4]. However,
0031-9406/$ – see front matter © 2012 Chartered Society of Physiotherapy. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.physio.2012.06.001
Please cite this article in press as: Mendes FAdS, et al. Motor learning, retention and transfer after virtual-reality-based training in
Parkinson’s disease – effect of motor and cognitive demands of games: a longitudinal, controlled clinical study. Physiotherapy (2012),
http://dx.doi.org/10.1016/j.physio.2012.06.001
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the extent to which dopamine depletion secondary to nigral
degeneration seen in Parkinson’s disease impacts this process
remains unclear. Therefore, although numerous studies have
investigated motor learning in Parkinson’s disease, the results
vary considerably [5–15].
In the absence of a clear picture of the changes during the
learning process in Parkinson’s disease, and consequent lack
of definitive guidelines for devising more effective rehabilitation strategies, it is important to investigate the learning
potential of patients with Parkinson’s disease by applying
new therapeutic strategies and validating their utility.
Virtual reality, defined as computer-based technology providing a multisensorial environment with which the user can
interact [16], has been proposed as a novel therapeutic tool
for motor rehabilitation. Studies have identified a number of
benefits derived from the use of virtual reality: (i) the performance of tasks that cannot feasibly be performed safely in a
real-world environment; (ii) intensive repetition of complex
tasks directed by visual and auditory stimuli which create
dynamic patient–task interaction [17]; (iii) immediate feedback on performance and results; and (iv) a more motivating
training environment [18].
Combined, these advantages can serve to facilitate the
learning process in patients with Parkinson’s disease. To date,
two previous studies have investigated the effects of training
in a virtual environment in patients with Parkinson’s disease,
both of which showed performance improvements in virtual
reality and positive transfer [19,20].
Among the virtual reality devices with potential for use in
rehabilitation, the Nintendo WiiTM stands out as a portable,
easy-to-use, low-cost alternative that offers good reliability
[21–23]. Some studies in elderly and brain-damaged patients
have reported improvement in balance after training on Nintendo Wii FitTM games, whose interface incorporates a force
platform, the Wii Balance BoardTM , that provides information on force distribution, enabling the player to control the
displacement of their body’s centre of gravity in real time
[23–26].
Despite the positive results reported by these preliminary studies, the criteria for game selection have yet to be
addressed. Previous studies have employed several criteria, including: (i) predicted viability/benefit of games based
on the movements performed during play [21,25], and (ii)
choice/acceptance of the games by participants [27]. Thus,
in spite of growing use of Wii Fit games in rehabilitation,
there is a lack of criteria to help guide the use of Wii Fit as a
therapeutic tool.
Given that motor and cognitive impairments in Parkinson’s disease can have a negative effect on the learning
process, depending on the demands placed by the tasks
trained, the authors hold that investigation into learning and
retention in Wii Fit games with different characteristics,
and into the transfer of their effects to real-life tasks, are
of prime importance for defining criteria for the selection
of games with greater therapeutic potential for this patient
group. Therefore, the aim of this study was to investigate
learning, retention and transfer of learning in patients with
Parkinson’s disease for 10 Wii Fit games that place different
motor and cognitive demands on players.
The authors hypothesised that, depending on the motor
and cognitive requirements of the games, patients with
Parkinson’s disease, after extensive training, will be able to
learn, retain and transfer learning to a similar motor task,
with or without deficits compared with healthy elderly people. The results of this study will demonstrate the limitations
and therapeutic potential of Wii Fit games for rehabilitation
of patients with Parkinson’s disease.
Methods
Subjects
Sampling size was calculated using the mean score on
the Torso Twists (TTW) Wii Fit game, based on a pilot
study which showed that patients with early-stage Parkinson’s disease and healthy elderly people had the same
baseline performance on this game. Thus, a mean initial
value was set at 70, with a standard deviation of 12, taking
20 points as the difference between pre- and post-training
scores. The result indicated that 18 participants (nine per
group) would be required to attain 90% power. Therefore,
16 patients with Parkinson’s disease and 11 healthy elderly
people were recruited, allowing for potential losses during
the study period. All participants completed the study and
were included in the analysis.
The patients with Parkinson’s disease (two at Stage 1 and
14 at Stage 2 on the Hoehn and Yahr staging scale), undergoing treatment with levodopa, were recruited from Parkinson’s
associations and assigned to the experimental group. The
healthy elderly people, matched for age and gender, were
recruited from third age associations and assigned to the control group. Inclusion criteria for the study were absence of
neurological disease (excluding Parkinson’s disease for the
experimental group) or detectable orthopaedic problems, a
minimum score of 24 on the Mini-Mental State Examination [28], a maximum score of 5 on the Geriatric Depression
Scale-15 items [29], normal or corrected visual acuity, and
good auditory acuity. Participants had no prior experience
with the Wii Fit games and were not participating in any
other rehabilitation programmes. All participants signed an
informed consent form prior to study commencement. The
study was approved by the Research Ethics Committee of
São Camilo University.
Procedures
Prior to commencing training, the participants performed a
right-side functional reach test [30]. This test enables assessment of the limits of stability in the standing position by
measuring the maximum distance that a participant can reach
laterally with their right arm, without moving or lifting their
feet from the floor.
Please cite this article in press as: Mendes FAdS, et al. Motor learning, retention and transfer after virtual-reality-based training in
Parkinson’s disease – effect of motor and cognitive demands of games: a longitudinal, controlled clinical study. Physiotherapy (2012),
http://dx.doi.org/10.1016/j.physio.2012.06.001
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3
Table 1
Games training schedule, and their main motor and cognitive demands.
Sessions 1, 3, 5,
7, 9, 11 and 13
Main motor demands
Main cognitive
demands
Sessions 2, 4, 6, 8,
10, 12 and 14
Main motor demands
Main cognitive
demands
Table Tilt
Shift centre of gravity
slowly in all directions
with feet in a fixed
position
Plan movements in
order to hit targets
Basic Run Plusa
Perform stationary
walk as fast as
possible on soles
Obstacle Course
Perform stationary walk
as fast as possible, halt
and resume walking
Decide on best walking
speed, when to halt and
resume, response
inhibition
Basic Step
Rhythm Parade
Perform stationary walk
to auditory and visual
rhythm provided by
game, while performing
flexo-extension of
elbows in different
rhythm to walk
Shift centre of gravity
sideways keeping feet
still while moving arms
Divide attention
between gait and task of
hitting random targets
with one or both arms
Torso Twists
Alternate steps
mounting and
dismounting Wii
Balance Board,
according to rhythm
determined by game
Perform torso twists,
moving arms and
keeping feet still
while remaining
stable
Divide attention
between gait and task
to memorise greatest
number of items of
information about
course to answer
questions posed at end
of each trial
Sustain attention to
follow visual and
auditory cues which
direct foot movements
Identify colour of
stimulus and plan arm
and hip movements to
direct targets to point
with corresponding
colour
Sustain attention to
mimic movements
shown by avatar,
self-awareness
Soccer Heading
Shift centre of gravity
latero-laterally while
keeping feet still
Penguin Slide
Shift centre of gravity
latero-laterally while
keeping feet still
Tilt City
Single Leg
Extension
a
Balance on one leg
while moving arms and
leg contralaterally while
remaining stable
Sustain attention to
mimic movements
shown by avatar,
self-awareness
Identify stimulus and
decide quickly on
direction of
movements to hit or
dodge target, response
inhibition
Plan movements of
avatar towards targets
Not played on Wii Balance Board.
The functional reach test was repeated 1 week and 60
days after the end of training (Fig. A, see online supplementary material).
Training
Both groups underwent 14 twice-weekly individual training sessions, overseen by a physiotherapist. Sessions were
run on the same days each week and at the same time.
Prior to embarking on the first training session, the games
were demonstrated by the physiotherapist, who explained the
objectives of each game. Subsequently, in order to familiarise
patients with the task and device, participants were allowed
two practice trials per game.
Sessions began with a 30-minute warm-up consisting of
global mobility exercises. This was followed by training on
Wii Fit games as shown in Table 1.
Two attempts were made per game: the first was considered as training and the second was considered as evaluatory.
During the first attempt at each game, participants were
assisted verbally and proprioceptively (by means of manual
contact of the trainer with the patient’s body) to achieve the
best way of moving to meet the game’s objectives. On the second attempt, the participant played without any assistance,
except for constant verbal encouragement; the final score
from the second attempt was recorded for later analysis of
the intersession learning curve. Participants were allowed to
rest between each exercise and/or game according to individual needs. Sixty days after the last training session, an
additional session was conducted in which participants had
two attempts at each of the 10 games in order to determine
learning retention.
The 10 Wii Fit games were selected based on their motor
and cognitive requirements. After analysis of the whole repertoire of games available by three physiotherapists, 10 games
were selected. Table 1 shows the training schedule for the
games, together with their motor and cognitive demands.
In terms of motor demands, four games required multidirectional shifts in the player’s centre of gravity [Table Tilt
(TT), Tilt City (TC), Penguin Slide (PS), Soccer Heading (SH)], four games involved alternating steps [Obstacle
Course (OC), Rhythm Parade (RP), Basic Run Plus (BRP),
Basic Step (BS)], and two games required stationary control of the player’s centre of gravity [Single Leg Extension
(SLE), TTW]. For cognitive demands, all 10 games involved
attention, rapid responses to visual stimuli and performance
assessment by visual and auditory feedback between trials.
Please cite this article in press as: Mendes FAdS, et al. Motor learning, retention and transfer after virtual-reality-based training in
Parkinson’s disease – effect of motor and cognitive demands of games: a longitudinal, controlled clinical study. Physiotherapy (2012),
http://dx.doi.org/10.1016/j.physio.2012.06.001
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Table 2
Participants’ characteristics at baseline.
Age (years)
Disease duration (years)
Mini-Mental State
Examination (score)
Geriatric Depression
Scale (score)
were classified according to the effects on analysis of variance.
Experimental
group (n = 16)
Control group
(n = 11)
P-value
68.6 (8.0)
4.7 (5.4)
27.2 (1.9)
68.7 (4.1)
0.98a
28.3 (1.1)
0.18a
3.6 (1.8)
2.4 (1.6)
0.12 a
Data shown as mean (standard deviation).
a t-test.
Three of the games required planning (TT, PS and TC), two
games involved a dual motor task (RP and TC), one game
required a dual motor and cognitive task (BRP), and two
games entailed decision-making and response inhibition (OC
and SH).
Data analysis
Differences in demographic and clinical characteristics
between the subjects in the two groups at baseline were tested
using Student’s t-test.
Learning curve and retention were rated based on the
scores for the second attempt at each game in the first seven
sessions and the eighth session, respectively, for each of the
10 games. After normality and homogeneity testing, repeated
measurements analysis (2 × 8) was applied to compare each
independent variable (score on each of the 10 games), using
group as the factor (control group and experimental group)
and the sessions (Session 1, Session 2, . . .. . .., Session 7 and
retention) as the repeated measure. Tukey–Kramer’s post hoc
test was applied for effects that reached a 5% level of significance in order to carry out pair-wise, inter- and intragroup
comparisons.
In order to determine the transfer of learning, the effect
of training on the games was tested based on the functional
reach test. Values (in cm) attained by patients with Parkinson’s disease before training, 1 week after training and 60
days after training were compared using one-way repeatedmeasures analysis of variance. All analyses were performed
using Statistica Version10 (StatSoft, Tulsa, OK, USA).
Results
Demographic and clinical characteristics
Table 2 shows the characteristics of subjects in the
experimental and control groups at baseline. No significant
differences were observed between the two groups.
Learning and retention
The scores attained on the games in the training and retention sessions (Table A, see online supplementary material)
Games in which the experimental and control groups had
the same performance and same learning and retention
capacity
For TTW and SLE, repeated-measures analysis of variance only revealed a session effect, with no group effect or
interaction between factors. The post hoc test showed a significant improvement between Session 1 and Session 7, and
between Session 1 and retention for TTW and SLE, respectively (Table A, see online supplementary material).
Therefore, the patients with Parkinson’s disease showed
no performance, learning or retention deficits on these games
compared with healthy elderly people.
Games in which the experimental group had impaired
performance, but the same learning and retention
capacity compared with the control group
For RP, TT, TC, BS and PS, the repeated-measures analysis of variance revealed a group effect and session effect, with
no interaction between factors. The post hoc test showed significant improvements from Session 1 to Session 2 for BS,
from Session 1 to Session 3 for RP and PS, and from Session
1 to Session 6 for TC, and confirmed differences between the
groups for RP, TT, TC, BS and PS (Table A, see online supplementary material).
In summary, the patients with Parkinson’s disease had the
same learning and retention capacity following training as
healthy elderly people, despite having a poorer performance
on these games.
Games in which the experimental group exhibited deficits
in learning and retention capacity
For OC, SH and BRP, repeated-measures analysis of variance revealed interaction between session and group. For OC
(Table A, see online supplementary material), on intragroup
analysis, post hoc test only showed a significant improvement
between Session 1 and Session 7, and Session 1 and retention
for the participants in the control group. Intergroup analysis
showed a significant difference in performance between the
groups at Session 7 which persisted to retention (Fig. 1).
This difference was also observed for SH
(Table A, see online supplementary material). On intragroup
analysis, the post hoc test showed a significant improvement between Session 1 and Session 7, and Session 1
and retention for the participants in the control group.
Intergroup analysis showed a significant difference in performance between the groups at Session 7 which persisted
to retention (Fig. 2). For BRP, intragroup analysis showed
a significant improvement between Session 1 and Session
7, and Session 1 and retention for the participants in the
control group (Table A, see online supplementary material),
while intergroup analysis showed a significant difference
in performance at Session 1 which persisted to retention
(Fig. 3).
Please cite this article in press as: Mendes FAdS, et al. Motor learning, retention and transfer after virtual-reality-based training in
Parkinson’s disease – effect of motor and cognitive demands of games: a longitudinal, controlled clinical study. Physiotherapy (2012),
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400
Experimental Group
350
Control Group
However, for BRP, the impaired performance seen in the first
session worsened after training.
*
Mean Scores
300
*
200
150
50
0
1
2
3
4
5
6
7
Retention
Sessions
Fig. 1. Mean score and standard error for the Obstacle Course game in
Sessions 1 to 7 and at retention in the experimental group and the control
group. *P ≤ 0.05 (group effect, Tukey–Kramer post hoc test).
Experimental Group
140
100
80
Discussion and conclusions
*
*
7
Retention
60
40
20
0
1
2
3
4
5
6
Sessions
Fig. 2. Mean score and standard error for the Soccer Heading game in Sessions 1 to 7 and at retention in the experimental group and the control group.
*P ≤ 0.05 (group effect, Tukey–Kramer post hoc test).
Experimental Group
180
150
Control Group
**
**
**
**
1
2
3
4
**
**
**
**
5
6
7
Retention
120
90
60
30
0
One-way repeated-measures analysis of variance revealed
an assessment effect (F = 7.19, P = 0.003, power = 0.90) for
the test of left functional reach, performed before training,
1 week after training and 60 days after training for patients
with Parkinson’s disease. This was confirmed by the post hoc
test which showed a significant improvement between before
training and 1 week after training (P = 0.003), and before
training and 60 days after training (P = 0.02). Therefore, the
patients with Parkinson’s disease were able to transfer a motor
ability trained on the games to a similar untrained task.
Control Group
120
Mean Scores
Transfer of learning – effect on functional reach test
250
100
Mean Scores
5
Sessions
Fig. 3. Mean score and standard error for the Basic Run Plus game in Sessions 1 to 7 and at retention in the experimental group and the control group.
**P ≤ 0.01 (group effect, Tukey–Kramer post hoc test).
In summary, the patients with Parkinson’s disease exhibited deficits in learning and retention on these games
compared with healthy elderly people; for OC and SH, this
deficit led to impaired performance during later sessions.
This study investigated the ability of patients with Parkinson’s disease to learn, retain and transfer learning on 10
Wii Fit games requiring different motor and cognitive skills
in comparison with healthy elderly people. The authors’
hypothesis was that, depending on the motor and cognitive
requirements of the games, the patients with Parkinson’s disease would exhibit deficits in learning and retention compared
with healthy elderly people.
The results confirmed this initial hypothesis, showing that
patients with Parkinson’s disease had normal learning and
retention on seven games (TTW, SLE, RP, TT, TC, BS and
PS) compared with healthy elderly people, but had worse
performance on five games (RP, TT, TC, BS and PS). The
patients with Parkinson’s disease were unable to improve
their performance on three games following training (OC, SH
and BRP), whereas the healthy elderly people demonstrated
good learning and retention.
Given that the training conditions and number of trials
were the same for all games, the difference in the ability of
patients with Parkinson’s disease to improve performance
may be attributed solely to the different demands of the
games.
Concerning motor requirements, two of the three games
for which patients with Parkinson’s disease displayed no
learning involved stationary gait (OC and BRP), whereas
the third game involved rapid multidirectional shifts in the
player’s centre of gravity (SH), placing similar demands as
five other games (RP, BS, TT, TC and PS) for which the
patients with Parkinson’s disease showed normal learning
compared with healthy elderly people.
For cognitive demands, two of the games for which the
patients with Parkinson’s disease failed to improve required
fast decision-making in hitting or avoiding stimuli displayed
on screen (SH), and in speeding up or halting gait to avoid
visual obstacles presented during a virtual journey (OC).
Although all of the games require several cognitive functions, such as attention, memory and planning, only these
Please cite this article in press as: Mendes FAdS, et al. Motor learning, retention and transfer after virtual-reality-based training in
Parkinson’s disease – effect of motor and cognitive demands of games: a longitudinal, controlled clinical study. Physiotherapy (2012),
http://dx.doi.org/10.1016/j.physio.2012.06.001
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two games required decision-making upon encountering new
stimuli. In the third game for which the patients with Parkinsons’ disease showed learning deficits, players had to answer
three varied questions at the end of a virtual walk about
the visual stimuli displayed along the way. The stimuli
and the questions varied, in order to preclude memorising
the answers between trials. Thus, the game simulated dualtasking conditions where attention is divided between motor
tasks (alternating steps) and cognition, registering several
stimuli presented for later recall – a task which also relies on
working memory. It is noteworthy that, for two other games
requiring divided attention between upper and lower limb
movements (RP and TC), the patients with Parkinson’s disease had no deficits in learning and retention despite having
a poorer performance than healthy elderly people.
Taken together, these results suggest that motor difficulties can impair the performance of patients with Parkinson’s
disease on the majority of games, but they do not affect the
ability to improve performance with practice or to retain
these benefits after training. However, impairment in some
cognitive functions, particularly quick decision-making and
management of attention and/or working memory, may have
hampered learning on some games.
Several studies have reported preserved motor learning
ability in patients with Parkinson’s disease [5,6], especially
under training conditions which present visual, auditory
and/or proprioceptive stimuli that serve to direct performance
[31,32] and/or provide feedback on performance [31,33].
To the authors’ knowledge, this is the first study reporting
this phenomenon on different and complex tasks in the same
group of patients.
However, among those studies that have identified learning deficits in patients with Parkinson’s disease, some
have discussed the mechanisms by which cognitive aspects
can affect results [34]. Several studies have shown that
dopamine depletion in internal circuits of the basal ganglia,
and consequent compromise of the efficacy of communication pathways connecting pre-frontal and cortical pre-motor
areas, can cause the cognitive deficits associated with Parkinson’s disease. Executive functions are particularly affected,
including attention, planning, decision-making, response
inhibition and working memory, and there is a negative effect
on the motor performance of patients [35,36], compromising their functionality [37]. Some studies have shown that
patients with Parkinson’s disease are particularly affected on
tasks requiring decision-making and divided attention [38],
response inhibition [35] and working memory [39].
Moreover, patients with Parkinson’s disease were able to
transfer a motor ability trained on the games to a similar
untrained task. Although some studies have shown deficits
in the ability of patients with Parkinson’s disease to transfer or generalise performance improvement to similar tasks
[40], the present study indicated that patients improved
their ability to shift their centre of gravity, trained on some
of the Wii Fit games. These findings confirmed those of
earlier reports showing that the effects of training with
virtual reality are transferable in patients with Parkinson’s
disease [19,20].
This is an important finding which points to the therapeutic potential of this type of training. Additional studies are
needed to further investigate the transfer of learning between
this type of game and other functional activities.
Based on these results, it can be concluded that the ability
of patients with Parkinson’s disease to learn, retain and transfer performance improvements after extensive training on
Wii Fit games depends largely on the demands, particularly
cognitive, of the specific games involved.
Thus, among the games tested, those in which patients
exhibited no learning deficit (SLE, TTW, RP, TT, TC, BS and
OS) have the greatest indication for therapeutic use, whereas
games for which patients showed no improvement during
training (OC, SH and BR) have low therapeutic potential.
This finding reiterates the importance of game selection
for rehabilitation purposes, and represents the main clinical outcome of this study. Further studies are warranted to
confirm the transfer of learning to activities of daily living,
thereby enabling training in virtual environments to be validated for patients with Parkinson’s disease.
Ethical approval: Research Ethics Committee of the São
Camilo University (Ref. No.: CAAE – 0166.0.166.000-8).
Conflict of interest: None declared.
Acknowledgements
The authors wish to thank the Pro Parkinson Association
(Jundiai) and Brazil Parkinson Association (Sao Paulo).
Appendix A. Supplementary data
Supplementary data associated with this article can be
found, in the online version, at http://dx.doi.org/10.1016/
j.physio.2012.06.001.
References
[1] Krakauer JW. Motor learning: its relevance to stroke recovery and
neurorehabilitation. Curr Opin Neuro 2006;19:84–90.
[2] Rostami HR, Ashayeri H. Effects of motor skill practice on reaction time and learning retention in Parkinson’s disease. Neurol India
2009;57:768–71.
[3] Abbruzzese G, Trompetto C, Marinelli L. The rationale for motor learning in Parkinson’s disease. Eur J Phys Rehabil Med 2009;45:209–14.
[4] Doyon J. Motor sequence learning and movement disorders. Curr Opin
Neurol 2008;21:478–83.
[5] Behrman AL, Cauraugh JH, Light KE. Practice as an intervention to
improve speeded motor performance and motor learning in Parkinson’s
disease. J Neurol Sci 2000;174:127–36.
[6] Pendt L, Reuter I, Muller H. Motor skill learning, retention, and
control deficits in Parkinson’s disease. PLos One 2011;6(7):e21669,
http://dx.doi.org/10.1371/journal.pone.0021669.
Please cite this article in press as: Mendes FAdS, et al. Motor learning, retention and transfer after virtual-reality-based training in
Parkinson’s disease – effect of motor and cognitive demands of games: a longitudinal, controlled clinical study. Physiotherapy (2012),
http://dx.doi.org/10.1016/j.physio.2012.06.001
PHYST-647; No. of Pages 7
ARTICLE IN PRESS
F.A.d.S. Mendes et al. / Physiotherapy xxx (2012) xxx–xxx
[7] Muslimovic D, Post B, Speelman JD, Schmand B. Motor procedural
learning in Parkinson’s disease. Brain 2007;130:2887–97.
[8] Price A, Shin JC. The impact of Parkinson’s disease on sequence learning: perceptual pattern learning and executive function. Brain Cogn
2009;69:252–61.
[9] Cohen H, Pourcher E. Intact encoding, impaired consolidation in procedural learning in Parkinson’s disease. Exp Brain Res 2007;179:
703–8.
[10] Bédard P, Sanes JN. Basal ganglia-dependent processes in recalling learned visual-motor adaptations. Exp Brain Res 2011;209:
385–93.
[11] Nieuwboer A, Rochester L, Müncks L, Swinnen SP. Motor learning in
Parkinson’s disease: limitations and potential for rehabilitation. Parkinsonism Relat Disord 2009;15(Suppl. 3):S53–8.
[12] Rochester L, Baker K, Hetherington V, Jones D, Willems AM, Kwakkel
G, et al. Evidence for motor learning in Parkinson’s disease: acquisition,
automaticity and retention of cued gait performance after training with
external rhythmical cues. Brain Res 2010;1319:103–11.
[13] Michel J, Benninger D, Dietz V, Van Hedel HJA. Obstacle stepping
in patients with Parkinson’s disease: complexity does influence performance. J Neurol 2009;256:457–63.
[14] Stephan MA, Meier B, Zaugg SW, Kaelin-Lang A. Motor sequence
learning performance in Parkinson’s disease patients depends on the
stage of disease. Brain Cogn 2011;75:135–40.
[15] Seo M, Beigi M, Jahanshahi M, Averbeck BB. Effects of dopamine
medication on sequence learning with stochastic feedback in Parkinson’s disease. Front Hum Neurosci 2010;4:1–9.
[16] Levin M. Can virtual reality offer enriched environments for rehabilitation? Exp Rev Neurotherapeut 2011;11:153–5.
[17] Deutsch J, Borbely M, Filler J, Huhn K, Guarrera-Bowlby P. Use of
a low-cost, commercially available gaming console (Wii) for rehabilitation of an adolescent with cerebral palsy. Phys Ther 2008;88:
1196–207.
[18] Fong KNK, Chow KYY, Chan BCH, Lam KCK, Lee JCK, Li THY, et al.
Usability of a virtual reality environment simulating an automated teller
machine for assessing and training persons with acquired brain injury.
J Neuroeng Rehabil 2010;7:19.
[19] Riess TJ. Gait and Parkinson’s disease: a conceptual model for
an augmented-reality based therapeutic device. Stud Health Technol
Inform 1998;58:200–8.
[20] Mirelman A, Maidan I, Herman T, Deutsch JE, Giladi N, Hausdorff JM.
Virtual reality for gait training: can it induce motor learning to enhance
complex walking and reduce fall risk in patients with Parkinson’s disease? J Gerontol A Biol Sci Med Sci 2011;66:234–40.
[21] Saposnik G, Teasell R, Mamdani M, Thorpe KE, Hall J, Cohen LG, et al.
Effectiveness of virtual reality using Wii gaming technology in stroke
rehabilitation: a pilot randomized clinical trial and proof of principle.
Stroke 2010;41:1477–84.
[22] Clark RA, McGough R, Paterson K. Reliability of an inexpensive
and portable dynamic weight bearing asymmetry assessment system incorporating dual Nintendo Wii Balance Boards. Gait Posture
2011;34:288–91.
[23] Gil-Gómez JA, Lloréns R, Alcañiz M, Colomer C. Effectiveness of a
Wii balance board-based system (eBaViR) for balance rehabilitation: a
pilot randomized clinical trial in patients with acquired brain injury. J
Neuroeng Rehabil 2011;8:30.
7
[24] Young W, Ferguson S, Brault S, Craig C. Assessing and training standing balance in older adults: a novel approach using the ‘Nintendo Wii’
balance board. Gait Posture 2011;33:303–5.
[25] Bateni H. Changes in balance in older adults based on use of physical
therapy vs the Wii Fit gaming system: a preliminary study. Physiotherapy 2011, http://dx.doi.org/10.1016/j.physio.2011.02.004.
[26] Williams MA, Soiza RL, Jenkinson AM, Stewart A. EXercising with
Computers in Later Life (EXCELL) – pilot and feasibility study of the
acceptability of the Nintendo® Wii Fit in community-dwelling fallers.
BMC Res Notes 2010;3:238.
[27] Joo LY, Yin TS, Xu D, Thia E, Chia PF, Kuah CWK, et al. A feasibility study using interactive commercial off-the-shelf computer gaming
in upper limb rehabilitation in patients after stroke. J Rehabil Med
2010;42:437–41.
[28] Brucki S, Nitrini R, Caramelli P, Bertolucci PHF, Okamoto IH. Suggestions for utilization of the Mini-Mental State Examination in Brazil.
Arq Neuro-Psiquiatr 2003;61:777–81.
[29] Almeida OP, Almeida SA. Reliability of the Brazilian version of the
abbreviated form of Geriatric Depression Scale (GDS) short form. Arq
Neuro-Psiquiatr 1999;57:421–6.
[30] Newton RA. Validity of the multidirectional reach test. J Gerontol Biol
Sci Med Sci 2001;56:M248–52.
[31] Espay AJ, Baram Y, Dwivedi AK, Shukla R, Gartner M, Gaines L, et al.
At-home training with closed-loop augmented-reality cueing device for
improving gait in patients with Parkinson disease. J Rehabil Res Dev
2010;47:573–81.
[32] Almeida QJ, Bhatt H. A manipulation of visual feedback during
gait training in Parkinson’s disease. Parkinson’s Dis 2011;2012:
1–7.
[33] Werner WG, Gentile AM. Improving gait and promoting retention in individuals with Parkinson’s disease: a pilot study. J Neurol
2010;257:1841–7.
[34] Carbon M, Reetz K, Ghilardi MF, Dhawan V, Eidelberg D. Early Parkinson’s disease: longitudinal changes in brain activity during sequence
learning. Neurobiol Dis 2010;37:455–60.
[35] Wylie SA, Ridderinkhof KR, Bashore TR, van den Wildenberg WPM.
The effect of Parkinson’s disease on the dynamics of online and
proactive cognitive control during action selection. J Cogn Neurosci
2010;22:2058–73.
[36] Wouwe NC, Ridderinkhof KR, van den Wildenberg WPM, Band GPH,
Abisogun A, Elias WJ, et al. Deep brain stimulation of the subthalamic nucleus improves reward-based decision-learning in Parkinson’s
disease. Front HumNeurosci 2011;5:1–13.
[37] Uc EY, Rizzo M, Johnson AM, Emerson JL, Liu D, Mills ED,
et al. Real-life driving outcomes in Parkinson disease. Neurology
2011;76:1894–902.
[38] Perfetti B, Moisello C, Lanzafame S, Varanese S, Landsness E, Onofrj
M, et al. Attention modulation regulates both motor and non-motor
performance: a high-density EEG study in Parkinson’s disease. Arch
Ital Biol 2010;148:279–88.
[39] Harrington DL, Castillo GN, Greenberg PA, Song DD, Lessig S. Neurobehavioral mechanisms of temporal processing deficits in Parkinson’s
disease. PLoS One 2011;6:1–13.
[40] Isaias IU, Moisello C, Marotta G, Schiavella M, Canesi M, Perfetti B,
et al. Dopaminergic striatal innervation predicts interlimb transfer of a
visuomotor skill. J Neurosci 2011;31:14458–62.
Available online at www.sciencedirect.com
Please cite this article in press as: Mendes FAdS, et al. Motor learning, retention and transfer after virtual-reality-based training in
Parkinson’s disease – effect of motor and cognitive demands of games: a longitudinal, controlled clinical study. Physiotherapy (2012),
http://dx.doi.org/10.1016/j.physio.2012.06.001