You are on page 1of 8

558598

research-article2014
NNRXXX10.1177/1545968314558598Neurorehabilitation and Neural RepairHarmsen et al

Original Research Articles


Neurorehabilitation and

A Mirror Therapy–Based Action


Neural Repair
1­–8
© The Author(s) 2014
Observation Protocol to Improve Reprints and permissions:
sagepub.com/journalsPermissions.nav

Motor Learning After Stroke DOI: 10.1177/1545968314558598


nnr.sagepub.com

Wouter J. Harmsen, MSc1,2, Johannes B. J. Bussmann, PhD1, Ruud W.


Selles, PhD1,3, Henri L. P. Hurkmans, PhD1, and Gerard M. Ribbers, MD, PhD1,2

Abstract
Background. Mirror therapy is a priming technique to improve motor function of the affected arm after stroke. Objective.
To investigate whether a mirror therapy–based action observation (AO) protocol contributes to motor learning of the
affected arm after stroke. Methods. A total of 37 participants in the chronic stage after stroke were randomly allocated to
the AO or control observation (CO) group. Participants were instructed to perform an upper-arm reaching task as fast
and as fluently as possible. All participants trained the upper-arm reaching task with their affected arm alternated with
either AO or CO. Participants in the AO group observed mirrored video tapes of reaching movements performed by
their unaffected arm, whereas participants in the CO group observed static photographs of landscapes. The experimental
condition effect was investigated by evaluating the primary outcome measure: movement time (in seconds) of the reaching
movement, measured by accelerometry. Results. Movement time decreased significantly in both groups: 18.3% in the AO
and 9.1% in the CO group. Decrease in movement time was significantly more in the AO compared with the CO group
(mean difference = 0.14 s; 95% confidence interval = 0.02, 0.26; P = .026). Conclusion. The present study showed that a
mirror therapy–based AO protocol contributes to motor learning after stroke.

Keywords
stroke, mirror therapy, action observation, motor learning, upper limbs, rehabilitation

Introduction
More than 50% of stroke survivors suffer from impaired composed and evaluated. Although many studies reported
motor function in the upper extremity.1 Because of the huge on a positive effect of mirror therapy on motor recovery
impact, motor rehabilitation is the focus of clinical work in after stroke,8-10 the exact working mechanisms are not
daily clinical practice as well as of neurorehabilitation fully understood. Selles et al11 examined the effects of
research. The affected limb typically is weak, slow, and unimanual and bimanual mirror therapy protocols on
lacks coordination and dexterity with a loss of the ability to motor learning after stroke. The largest intervention
generate fractionated movements, and spasticity may be effects were found in the condition in which patients only
present. trained the affected arm without a mirror and in the
Treatment paradigms for the affected limb may be condition in which patients moved the unaffected arm in
classified into augmenting techniques, task-specific exer- front of the mirror while observing the mirror reflection.
cises, and priming techniques.2 Priming techniques aim at
increasing the excitability of the involved neural networks
and promoting plastic reorganization. Mirror therapy is an 1
E rasmus MC, Department of Rehabilitation Medicine, Rotterdam, the
example of a priming technique for improving motor Netherlands
2
function after stroke.3,4 In mirror therapy, a mirror is placed Rijndam Rehabilitation Centre, Rotterdam, the Netherlands
3
Erasmus MC, Department of Plastic and Reconstructive Surgery,
in the midsagittal plane, which reflects movements of the Rotterdam, the Netherlands
unaffected limb. The mirror reflection creates the illusion
that the affected side moves with a normal movement Corresponding Author:
Wouter J. Harmsen, MSc, Department of Rehabilitation Medicine,
pattern, creating a form of “virtual feedback.” Erasmus MC–University Medical Center, Room: Ee 1622, Dr
A number of trials on mirror therapy in stroke have Molewaterplein 50, 3015 GE Rotterdam, Netherlands.
been reported,5-7 and various mirror therapy protocols are Email: w.harmsen@erasmusmc.nl

Downloaded from nnr.sagepub.com by guest on May 14, 2015


2 Neurorehabilitation and Neural Repair 

Several authors ascribed the effects of mirror therapy to motion, muscle tone, and the ability to execute proximal
neuronal activations of frontoparietal circuitries in the and distal movements inside and outside movement
brain, involving mirror neurons.12,13 Mirror neurons dis- synergies. The FMA scores range from 0 to 66, with higher
charge during both action execution and action observation scores indicating better motor function.26
(AO) of corresponding movements.14 Previous functional
magnetic resonance imaging studies showed that similar
Randomization
parts of the neuronal network are involved in AO as in
mirror therapy.14,15 Participants were randomly allocated to the AO or control
AO improves motor learning in healthy individuals16-18 observation (CO) group. To minimize possible confounding
and may be a promising tool in regaining motor function effects of motor ability and age, we stratified participants
after stroke.19-21 A recent pilot study showed that into groups based on age (younger than 55 years of age or
self-directed video therapy improves motor recovery after 55 years and older) and motor function (FM score <50 or a
stroke.22 New motor skills become part of the patient’s FM score of ≥50). In this way, we created 4 strata. Stratified
motor repertoire, and observation activates the mirror randomization was achieved by performing a separate
neuron system.23 The beneficial effects of mirror therapy randomization procedure within each stratum. The random-
may, at least partly, be explained by working mechanisms ization was based on a computer-generated random code
similar to that in AO. This study addresses the question of using blocks of 20 patients and using sealed envelopes.
whether a mirror therapy–based AO protocol improves
motor learning in the chronic stage after stroke by studying
a simple upper-arm motor task.
Motor Task
Participants performed a simple upper-arm reaching task.
The task consisted of making a reaching movement
Methods from a starting position located next to the chair, toward a
Study Sample target located in front of them (Figure 1). A light
indicated the start of each trial. After hitting the target,
Participants in the chronic stage after stroke were recruited participants had to move their arm back toward the starting
from the outpatient clinic of Rijndam Rehabilitation Centre position and wait until the light turned on again for the next
in Rotterdam, the Netherlands.. The inclusion criteria were reaching movement. Participants were instructed to make
(1) a Brunnström score for upper-extremity function between the upper-arm reaching movement as fluently and fast as
III and VI, (2) a home dwelling status, and (3) at least 6 possible toward the target end point.
months poststroke. Patients with neglect (indicated by the
star cancellation test and/or reported by the occupational
therapist or psychologist), comorbidities that influence Experimental Procedure
voluntary upper-extremity function, or who suffered from Participants start the experiment with a set of 10 upper-
multiple strokes were excluded. All participants gave arm reaching movements with the affected arm, which
written informed consent, and the study was approved by served as baseline measurement (T0). Hereafter, partici-
the Medical Ethics committee. pants performed a set of 10 trials with their unaffected arm,
which was recorded with a digital camera and used for AO.
Power Analysis After baseline measurements, participants start the training
within the allocated condition. The training contained sets
The sample size was calculated on the data from the study of affected-arm reaching movements, alternated with
of Cirstea and Levin,24 on which our experimental periods of observation (AO or CO). As in mirror therapy,
paradigm was based. We calculated that 12 participants in the video screen was positioned in the midsagittal plane.
each group would be sufficient to have an 80% chance of After training, participants performed another set of
detecting a statistically significant difference of 0.25 s 10 affected-arm reaching movements, which served as
between groups. To increase power, we aimed for a total of follow-up measurement (T1). Figure 2 shows the schematic
20 participants in each group. representation of the experimental procedure.

Clinical Assessment Experimental Conditions: AO and CO


Before starting the experiment, motor ability of the upper In this study, AO is offered in such a way that the
extremity was evaluated using the Fugl-Meyer assessment observation of the upper-arm reaching movements is almost
(FMA).25 The upper-extremity part of the FMA examines similar to what patients would see in the mirror during
voluntary upper-limb movements, tendon reflexes, range of mirror therapy. AO was displayed from a first-person

Downloaded from nnr.sagepub.com by guest on May 14, 2015


Harmsen et al 3

Figure 1.  Side view of the experimental setup: Participants were instructed to move their arm from a position located next to
the chair (A) toward a target located in front of them (B). The distance of the target was adjusted to the body dimensions of each
participant and the participant’s ability to extend the arm, such that at the end of the reaching movement, the fingers would just hit
the target.

Figure 2.  Schematic representation of the experimental setup. Baseline measurement: 10 affected arm movements (T0) followed by
10 unaffected arm movements, which were videotaped with a digital camera. Training: affected arm movements were alternated with
either action observation (AO) or control observation (CO). Follow-up: 10 affected arm movements (T1). The numbers under each
block represent the amount of physical repetitions, whereas the time in minutes indicates the duration of observation.

perspective, so the observed movements correspond to Participants in the CO group observed a slideshow with
the orientation of the participant. To provide participant- static photographs of landscapes as control stimuli. The
specific videos, reaching movements from the unaffected photographs contained no images of humans or animals and
arm were videotaped and mirrored. Thereby, we tried to were selected such that they would not trigger the mirror
create maximal postural familiarity and the illusion that the neuron system; therefore, they were not likely to interfere
affected arm performed the reaching movements in a with the goal in this study.
normal movement pattern. Participants were instructed to
focus on the arm reaching movements, which were
Data Acquisition and Analysis
displayed on the computer monitor (Figure 3). In addition,
participants were instructed to observe the AO with the Accelerometer data measured at the arm and target end
intention to reproduce the reaching task with the affected point were recorded using a TEMEC Vitaport 3 digital
arm because this is proven to be a beneficial strategy in recording system. A switch was used to turn on a light,
observational learning.26,27 which indicated the start of each reaching movement, and

Downloaded from nnr.sagepub.com by guest on May 14, 2015


4 Neurorehabilitation and Neural Repair 

Figure 3.  Side view of the experimental setup during action observation (AO) and control observation (CO): Participants in the AO
group observed mirrored reaching arm movements of the videotaped unaffected arm, as can be seen on the left image. Participants in
the CO group observed a slideshow with static photographs of landscapes, as can be seen on the right image.

simultaneously left a marker signal in the recorded time We evaluated the effect of the following possible
series. Two 2D acceleration sensors (biaxial piezo-resistive confounders on the experimental conditions: age, gender,
accelerosensor, Temec Instruments, Netherlands) were time since stroke, stroke type (hemorrhagic or ischemic),
placed on the ventral side of the wrist, measuring accelera- FM score, affected side (dominant or nondominant), group
tions during the reaching movements in 3 dimensions. (AO or CO), and movement time at baseline measurement
Another 2D acceleration sensor (bi-axial piezoresistive (T0). To do so, first, we individually added each possible
accelerosensor, Temec Instruments, Netherlands) was confounder to a multiple regression model, with experi-
attached at the target end point and measured acceleration mental condition as the other dependent variable using the
in 2 dimensions to indicate the end of each reaching Enter-method, selecting each confounder that changed the β
movement. Accelerations were recorded at a sample of the experimental condition effect by more than 10%. As
frequency of 128 Hz. a second step, we entered each selected confounder in a
Because movement time was found to be a predictive forward regression model, in order of confounding effect
measure in learning a simple upper-arm motor task after size. If the added confounder did not further change the β of
stroke,11,24 it was selected as the primary outcome. the experimental condition effect by more than 10%, it was
Movement time was defined as the time between the start excluded from the final regression model.
signal derived from the marker signal and hitting the target All statistical analyses were 2-tailed and performed
end point, derived from the accelerometer signal on the using IBM SPSS Statistics 20, and a P < .05 was considered
target end point. All data were analyzed using custom-made statistically significant.
Matlab algorithms (7.4.0 r2007 a).
Results
Statistical Analysis A total of 134 participants were eligible for inclusion, of
To evaluate the experimental condition effect on motor whom 37 participated in the present study (Figure 4).
performance, change in movement time between baseline Table 1 shows group characteristics of participants
(T0) and follow-up (T1) was measured and compared allocated to the AO (n = 18) and CO group (n = 19). As can
between groups. For each block of 10 movements, we be seen, the poststroke time period was relatively long in
calculated the median movement time of 9 trials (2-10), both groups; most participants suffered from ischemic
omitting the first reaching movement. Median values for stroke and had a middle cerebral artery lesion. Based on the
movement time were used for group analysis. The assump- FMA, there was no baseline difference in upper-extremity
tion for normality was checked by visual inspections of function between both groups (P = .48).
the histogram and normal curve and by performing a Movement time decreased significantly in both groups:
Shapiro-Wilk test. Independent Student t tests, χ2, or 18.3% in the AO group (P < .001) and 9.1% in the CO
Mann-Whitney U tests were selected to test for differences group (P = .036), with a significant difference in movement
between groups. time decrease between groups (mean difference = 0.14 s;

Downloaded from nnr.sagepub.com by guest on May 14, 2015


Harmsen et al 5

Figure 4.  Flowchart describing the study sample and distribution of participants.

Table 1.  Patient Characteristics.a

Characteristics AO (n = 18) CO (n = 19) P Value


Age (years) 57 (10.4) 60 (8.8) .280
Stroke type (ischemic:hemorrhagic) 13:5 12:7 .401
Time since stroke (months) 46 (37) 38 (25) .753
Sex (male:female) (9:9) (13:6) .254
Affected side (dominant:nondominant) 8:10 9:10 .858
Fugl-Meyer score (ranging from 0 to 66) 54.3 (12.7) 57.1 (10.5) .300
Location artery lesion .476
  Middle cerebral artery 13 16  
  Posterior cerebral artery 1 0  
 Brainstem 3 2  
  Not specified 1 1  
Baseline movement time (s) 1.32 (0.44) 1.11 (0.28) .091

Abbreviations: AO, action observation; CO, control observation


a
Values are presented as mean (SD).

95% confidence interval [CI] = 0.02 to 0.26; P = .026). CI = 0.014 to 0.269) were independent confounding
Although movement time at baseline differed on average variables of the experimental condition effect (AO vs CO).
0.21 s between groups, this was not significant (P = .09). However, the regression model that included these
The extended regression analyses indicated that baseline confounding variables still showed a significant effect of
movement time (β = 0.001; P = .063; 95% CI = −0.009 to the experimental grouping condition on movement time
0.305) and type of stroke (β = 0.141; P = .030; 95% (R = 0.58; β = 0.126; 95% CI = 0.009 to 0.244; P = .036).

Downloaded from nnr.sagepub.com by guest on May 14, 2015


6 Neurorehabilitation and Neural Repair 

Discussion relatively short time periods. It should be noted that


repetitive practice of sequentially simple motor tasks may
To our knowledge, this is the first study ever to specifically lead to motor improvements by adaptation,30 and short-term
investigate a mirror therapy–based AO protocol. Most effects of AO on motor learning may not transfer to more
studies on mirror therapy mainly focus on its effect on complex motor and more clinically meaningful tasks, which
motor learning10 and specific neuronal activations are typically learned more slowly over multiple training ses-
involved.8,13,15,28 Training without a mirror or with a sions, such as hand dexterity or hand function in daily life.31,32
nontransparent screen between both arms are commonly Despite randomized stratification, there were some base-
used control conditions, generally showing that mirror line differences that might explain different intervention
therapy is beneficial for increasing motor learning after effects between groups. For example, patients in the
stroke.8,9,11 The present study specifically investigated the CO group had, on average, a better Fugl-Meyer score
effects of a mirror therapy–based AO protocol on motor and a faster baseline reaching movement. Therefore, we
learning in patients in the chronic stage after stroke. A performed an extended regression analyses to control for
significantly larger decrease in movement time was found possible confounding variables. Although we indeed found
in the AO compared with the CO group. The results indicate that baseline movement time and type of stroke were
that a mirror therapy–based AO protocol contributes to independent confounding variables of the condition effect,
motor learning after stroke and, at least partly, clarifies the the condition effect was still significant after control for
beneficial effects of mirror therapy on motor learning. baseline values, indicating a Group × Time interaction effect.
The primary aim of this study was not to create a Some limitations of the present study should be
clinically meaningful change in arm function that would discussed. First, the mirror therapy–based AO slightly
persist over longer time periods but merely to study the differed from the mirror reflection during mirror therapy.
short-term impact of AO on learning a simple upper-arm In contrast to the mirror reflection, the computer screen has
motor task after stroke. This experimental approach is in limited resolution and depth perception. In addition, to gain
line with previous studies that suggest that simple motor a clear view, the computer screen was positioned close to
tasks can be selected to study the effects of different train- the participant, and therefore differs slightly from the
ing paradigms on motor learning in an efficient way.11,15,28 mirror position during mirror therapy. However, the
Our findings indicate that AO increases motor learning presented AO corresponds to the mirror reflection and
when a simple upper-arm motor task was trained. Previous creates the illusion that the affected arm performed the
studies on AO in stroke evaluated the effects of several reaching movements. Second, the relative heterogeneous
weeks of AO therapy, using functional outcome tests such sample should be mentioned, with participants suffering
as the Frenchay arm test, Wolf motor function test, or the from either hemorrhagic or ischemic stroke. Including only
Box and Block test.22,29 In the study of Ertelt et al,22 patients participants with specific brain lesions was not feasible
in the chronic stage after stroke significantly improved and would have decreased the external validity. A third
motor function following a 4-week video therapy program limitation is that the number of participants in both groups
compared with a control group. Patients entering the AO was relatively small. The power analysis was based on
group observed sequences of daily arm and hand actions findings of Cirstea and Levin,24 who showed a 0.25-s
with increasing complexity, from 3 different perspectives improvement in movement time in the affected no mirror
on a television screen positioned in front of the patient. condition, which was similar to the improvement in the
Beneficial effects of AO on motor learning were also found present study (0.24-s improvement). Therefore, there seems
in the subacute phase after stroke by Franceschini et al,29 to be sufficient power to find a clear significant difference
who studied AO therapy as an add-on treatment to the in the main outcome measure. A fourth possible limitation
standard rehabilitation of arm function. Patients observed 3 of the present study is that we did not further analyze
different motor sequences with increasing complexity from movement trajectory, which may have provided additional
a first-person perspective, based on actions of daily living, information regarding motor learning after stroke. However,
which were performed by young nondisabled men and previous research on motor learning after stroke showed that
women. These studies provide evidence for an additional movement time was a predictive measure when analyzing
positive impact of AO on motor learning after stroke, which a simple goal-directed upper-arm reaching task.11,24
matches the findings of the present study. However, the AO The present study showed that a mirror therapy–based
setup and training paradigms selected in these studies do AO protocol contributes to motor learning in patients in the
not allow transferring the results to the mirror therapy– chronic stage after stroke and, at least partly, clarifies the
based AO paradigm investigated in the present study. beneficial effects of mirror therapy on motor learning.
In this experiment, a simple upper-arm motor task was However, many questions remain. For example, it is still
selected to study the effects of AO on motor learning, which not clear whether early priming techniques, applied in the
allowed us to examine change in motor performance over subacute stage after stroke, may actually promote recovery

Downloaded from nnr.sagepub.com by guest on May 14, 2015


Harmsen et al 7

beyond the level of spontaneous recovery. Additionally, it chronic stroke patients: a phase ii randomized controlled trial.
might be that the effects of mirror therapy or AO on motor Neurorehabil Neural Repair. 2011;25:223-233.
learning can be maximized by combining it with other 9. Yavuzer G, Selles R, Sezer N, et al. Mirror therapy improves
priming techniques, such as transcranial direct current hand function in subacute stroke: a randomized controlled
trial. Arch Phys Med Rehabil. 2008;89:393-398.
stimulation. Answering these types of questions will help in
10. Thieme H, Mehrholz J, Pohl M, Behrens J, Dohle C. Mirror
changing the pragmatic, experience-based orientation of
therapy for improving motor function after stroke. Cochrane
neurorehabilitation to an experimental and theory-based Database Syst Rev. 2012;(3):CD008449.
approach. 11. Selles RW, Michielsen ME, Bussmann JB, et al. Effects

of a mirror-induced visual illusion on a reaching task in
stroke patients: Implications for mirror therapy training.
Conclusion
Neurorehabil Neural Repair. 2014;28:652-659.
The present study showed that a mirror therapy–based 12. Michielsen ME, Smits M, Ribbers GM, et al. The neuronal
AO protocol contributes to motor learning in patients after correlates of mirror therapy: An fmri study on mirror induced
stroke. visual illusions in patients with stroke. J Neurol Neurosurg
Psychiatry. 2011;82:393-398.
13. Bhasin A, Padma Srivastava MV, Kumaran SS, Bhatia R,
Authors’ Note Mohanty S. Neural interface of mirror therapy in chronic
Trial number: ISRCTN40128145. stroke patients: a functional magnetic resonance imaging
study. Neurol India. 2012;60:570-576.
Declaration of Conflicting Interests 14. Buccino G, Binkofski F, Fink GR, et al. Action observa-
tion activates premotor and parietal areas in a somatotopic
The authors declared no potential conflicts of interest with respect manner: an fmri study. Eur J Neurosci. 2001;13:400-404.
to the research, authorship, and/or publication of this article. 15. Hamzei F, Lappchen CH, Glauche V, Mader I, Rijntjes
M, Weiller C. Functional plasticity induced by mirror
Funding training: the mirror as the element connecting both hands
to one hemisphere. Neurorehabil Neural Repair. 2012;26:
The authors received no financial support for the research,
484-496.
authorship, and/or publication of this article.
16. Buccino G, Vogt S, Ritzl A, et al. Neural circuits underly-
ing imitation learning of hand actions: an event-related fmri
References study. Neuron. 2004;42:323-334.
1. Jorgensen HS, Nakayama H, Raaschou HO, Vive-Larsen J, 17. Vogt S, Buccino G, Wohlschlager AM, et al. Pre-

Stoier M, Olsen TS. Outcome and time course of recovery in frontal involvement in imitation learning of hand actions:
stroke: part i. Outcome. The Copenhagen Stroke Study. Arch effects of practice and expertise. Neuroimage. 2007;37:
Phys Med Rehabil. 1995;76:399-405. 1371-1383.
2. Pomeroy V, Aglioti SM, Mark VW, et al. Neurological 18. Larssen BC, Ong NT, Hodges NJ. Watch and learn: seeing
principles and rehabilitation of action disorders: rehabilita- is better than doing when acquiring consecutive motor tasks.
tion interventions. Neurorehabil Neural Repair. 2011;25: PLoS One. 2012;7:e38938.
33S-43S. 19. Buccino G, Solodkin A, Small SL. Functions of the mirror
3. Dohle C, Pullen J, Nakaten A, Kust J, Rietz C, Karbe H. neuron system: implications for neurorehabilitation. Cogn
Mirror therapy promotes recovery from severe hemiparesis: Behav Neurol. 2006;19:55-63.
a randomized controlled trial. Neurorehabil Neural Repair. 20. Garrison KA, Winstein CJ, Aziz-Zadeh L. The mirror neuron
2009;23:209-217. system: a neural substrate for methods in stroke rehabilitation.
4. Altschuler EL, Wisdom SB, Stone L, et al. Rehabilitation Neurorehabil Neural Repair. 2010;24:404-412.
of hemiparesis after stroke with a mirror. Lancet. 1999;353: 21. Pomeroy VM, Clark CA, Miller JS, Baron JC, Markus HS,
2035-2036. Tallis RC. The potential for utilizing the “mirror neurone
5. Michielsen ME, Selles RW, van der Geest JN, et al. Motor system” to enhance recovery of the severely affected upper
recovery and cortical reorganization after mirror therapy in limb early after stroke: a review and hypothesis. Neurorehabil
chronic stroke patients: a phase ii randomized controlled trial. Neural Repair. 2005;19:4-13.
Neurorehabil Neural Repair. 2011;25:223-233. 22. Ertelt D, Small S, Solodkin A, et al. Action observation has a
6. Dohle C, Pullen J, Nakaten A, Kust J, Rietz C, Karbe H. positive impact on rehabilitation of motor deficits after stroke.
Mirror therapy promotes recovery from severe hemiparesis: Neuroimage. 2007;36(suppl 2):T164-T173.
a randomized controlled trial. Neurorehabil Neural Repair. 23. Cross ES, Hamilton AF, Grafton ST. Building a motor

2009;23:209-217. simulation de novo: observation of dance by dancers.
7. Thieme H, Mehrholz J, Pohl M, Behrens J, Dohle C. Mirror Neuroimage. 2006;31:1257-1267.
therapy for improving motor function after stroke. Stroke. 24. Cirstea MC, Levin MF. Improvement of arm movement

2013;44:e1-e2. patterns and endpoint control depends on type of feedback
8. Michielsen ME, Selles RW, van der Geest JN, et al. Motor during practice in stroke survivors. Neurorehabil Neural
recovery and cortical reorganization after mirror therapy in Repair. 2007;21:398-411.

Downloaded from nnr.sagepub.com by guest on May 14, 2015


8 Neurorehabilitation and Neural Repair 

25. Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S,


29. Franceschini M, Ceravolo MG, Agosti M, et al. Clinical

Steglind S. The post-stroke hemiplegic patient: 1. A method relevance of action observation in upper-limb stroke reha-
for evaluation of physical performance. Scand J Rehabil Med. bilitation: a possible role in recovery of functional dexterity.
1975;7:13-31. A randomized clinical trial. Neurorehabil Neural Repair.
26. Badets A, Blandin Y. Feedback and intention during motor- 2012;26:456-462.
skill learning: a connection with prospective memory. Psychol 30. Krakauer JW, Mazzoni P. Human sensorimotor learn-

Res. 2012;76:601-610. ing: adaptation, skill, and beyond. Curr Opin Neurobiol.
27. Badets A, Blandin Y, Shea CH. Intention in motor learn- 2011;21:636-644.
ing through observation. Q J Exp Psychol (Hove). 2006;59: 31. Dayan E, Cohen LG. Neuroplasticity subserving motor skill
377-386. learning. Neuron. 2011;72:443-454.
28. Nojima I, Mima T, Koganemaru S, Thabit MN, Fukuyama 32. Doyon J, Benali H. Reorganization and plasticity in the adult
H, Kawamata T. Human motor plasticity induced by mirror brain during learning of motor skills. Curr Opin Neurobiol.
visual feedback. J Neurosci. 2012;32:1293-1300. 2005;15:161-167.

Downloaded from nnr.sagepub.com by guest on May 14, 2015

You might also like