Neurorehabilitation and Neural

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Randomized Trial of Observation and Execution of Upper Extremity Actions Versus Action Alone in
Children With Unilateral Cerebral Palsy
Giuseppina Sgandurra, Adriano Ferrari, Giuseppe Cossu, Andrea Guzzetta, Leonardo Fogassi and Giovanni Cioni
Neurorehabil Neural Repair 2013 27: 808 originally published online 25 July 2013
DOI: 10.1177/1545968313497101

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NNR27910.1177/1545968313497101Neurorehabilitation and Neural Repair XX(X)Sgandurra et al

Clinical Research Article

Neurorehabilitation and

Randomized Trial of Observation and

Neural Repair
27(9) 808­–815
© The Author(s) 2013
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Versus Action Alone in Children With DOI: 10.1177/1545968313497101

nnr.sagepub.com

Unilateral Cerebral Palsy

Giuseppina Sgandurra, MD, PhD1, Adriano Ferrari, MD2,3,

Giuseppe Cossu, MD4, Andrea Guzzetta, MD, PhD1,
Leonardo Fogassi, PhD4, and Giovanni Cioni, MD1,5

Abstract
Background. The properties of the mirror neuron system suggest a new type of upper limb (UL) rehabilitation in children
with unilateral cerebral palsy (UCP), based on observation of action therapy followed by execution of a variety of observed
movements (AOT). Objective. We tested the effects of AOT in the Upper Limb Children Action Observation Training
(UP-CAT) trial. Methods. In a randomized, evaluator-blinded, block-designed trial, 24 UCP children with mild to moderate
hand impairment were assigned to 2 groups. The experimental group observed, 1 hour per day for 3 consecutive weeks,
video sequences of unimanual or bimanual goal-directed actions and subsequently executed observed actions with the
hemiparetic UL or both ULs. The control group performed the same actions in the same order as the experimental sample,
but had watched computer games. The Assisting Hand Assessment (AHA) scale was the primary outcome measure; the
Melbourne assessment and ABILHAND-Kids were secondary ones. Outcomes were assessed at 1 week (T1), 8 weeks
(T2), and 24 weeks (T3) after the end of the training. Results. The experimental group improved more (P = .008) in score
changes for the AHA at the primary endpoints T1 (P = .008), T2 (P = .019), and T3 (P = .049). No between-group significant
changes were found for ABILHAND-Kids or Melbourne assessment. Conclusions. UP-CAT improved daily UL activities in
UCP children, suggesting a new rehabilitation approach based on a neurophysiological model of motor learning.

Keywords
childhood hemiplegia, upper extremity rehabilitation, mirror neuron system, imitation, randomized controlled trial,
cerebral palsy

Introduction training, constraint-induced movement therapy, hand-arm

bimanual intensive training, and neurodevelopmental treat-
Cerebral palsy (CP), with a prevalence ranging between 2 ment. Unfortunately, randomized controlled trials (RCTs)
and 3 per 1000 live births, is the largest cause of childhood that measure clinical results in children with hemiplegia are
physical disability in the industrialized societies.1 Children scarce.8-11 New interventions strategies, based on solid
with unilateral cerebral palsy (UCP) represent 30% to 40% methodological and scientific grounds are needed.12
of the general population of CP children, their upper limb
(UL) being generally more affected than the lower limb.2,3
Unimanual activities are often preserved, as they are per- 1
IRCCS Fondazione Stella Maris, Calambrone, Pisa, Italy
2
formed by the nonaffected UL; nevertheless, activity and IRCCS S. Maria Nuova Hospital, Reggio Emilia, Italy
3
University of Modena and Reggio Emilia, Modena, Italy
participation of children are severely impaired as most daily 4
University of Parma and Istituto Italiano di Tecnologia (Rete
activities are bimanual.4,5 Tecnologica Multidisciplinare) Parma, Italy
Several models of intervention are currently available, 5
University of Pisa, Calambrone, Pisa, Italy
targeting deficits in UL function and aiming at reducing
Corresponding Author:
activity limitations.6 In a recent systematic review and Giovanni Cioni, IRCCS Fondazione Stella Maris, Viale del Tirreno 331,
meta-analysis,7 4 main interventions have been outlined— 56128, Calambrone, Pisa, Italy.
intramuscular botulinum toxin A combined with UL Email gcioni@inpe.unipi.it

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Sgandurra et al 809
Recent neurophysiological evidences on motor control
and learning have disclosed some interesting opportunities
for rehabilitation. Brain imaging data in humans showed
that both imagery and actual execution of hand actions acti-
vate similar structures of the sensorimotor cortex.13,14
Moreover, it was shown in both monkeys and humans the
existence of a neural system, whose core regions are ventral
premotor and inferior parietal cortex, that is activated both
when individuals perform goal-directed motor acts (eg,
grasping an object) and when they observe someone else
performing the same or a similar motor act.15,16 This system
has been dubbed the mirror neuron system (MNS) and may
play an important role in action understanding, imitation,
and motor learning.17 Functional magnetic resonance imag-
ing studies have shown that action observation, combined
with actual replication of the observed action, induces a
strong activation of the MNS, along with marked improve-
ment in motor learning efficacy.18,19
These results have fostered the development of rehabili-
tation protocols based on the observation of meaningful
actions followed by their execution (Observation to Imitate
[OTI]).20,21 This approach, often labeled Action Observation
Treatment (AOT) and based on the OTI paradigm, has been
used with promising results in pilot studies on adults with
stroke,22,23 Parkinson’s disease,24,25 and during recovery
from orthopedic surgery.26
Knowledge on the ontogeny of the MNS and its role dur-
ing infancy is still scarce and mostly indirect. Many studies
provided evidence that newborns27 and infants28 are able to
imitate others’ individual gestures. Activation of the motor
cortical areas during action observation in infants has been
reported.29,30 In addition, a recent pilot study performed in
children with CP suggests positive effects on UL function
after a rehabilitation program based on AOT.31
We recently proposed32 an original paradigm of UL reha-
bilitation, called Upper Limb Children Action Observation
Training (UP-CAT) and we have designed, according to
CONSORT12 Statement, and registered a RCT based on this
approach.
We first hypothesized that UCP children receiving the
UP-CAT would demonstrate significantly greater improve-
ment than the control group immediately after the training,
and secondly that this effect would be retained at the fol-
low-up 2 and 6 months later. Furthermore, we hypothesized
that, since MNS activity is related to action goals, regard-
less of the movement’s kinematic properties, the observed
improvement would be greater in the goal-relatedness of
UL use, rather than in UL kinematics.
Methods
This randomized, evaluator-blinded, block-designed trial
has been described elsewhere32 and will be briefly summa-
rized. The study was conducted in 2 clinical centers: the
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Department of Developmental Neuroscience of IRCCS
Stella Maris (Pisa, Italy) and the Unit of Children
Rehabilitation of IRCCS S. Maria Nuova Hospital (Reggio
Emilia, Italy). This trial was approved by the Ethical
Committee of both Institutions and was registered at http://
www.clinicaltrials.gov (identifier NCT01016496). All par-
ents provided written informed consent to the treatment.
Study Population and Randomization
Between June 2009 and September 2010, UCP children
between 5 and 15 years were enrolled according to the fol-
lowing inclusion criteria: (a) confirmed diagnosis of spastic
UCP; (b) grade ≤2 on the Modified Ashworth Scale34; (c)
grade between 4 and 8 on the House Functional Classification
System (HFCS),35,36 that is, children whose hand ability
ranged from “fair passive assist” impaired hand, able to
grasp object and hold it weakly (level 4), to a complete
“spontaneous use” of the hand that moves independently of
the other hand (level 8); (d) cognitive level within normal
limits; (e) absence of attentional or sensory impairments; (f)
no history of seizures or seizures well controlled by ther-
apy; and (g) living near 1 of the 2 clinical centers with par-
ents able to commit to an intensive therapy program for 3
weeks. Children who had sustained previous orthopedic
surgery or botulinum toxin A injection in the UL within 6
months prior to study entry were excluded.
After obtaining the informed consent, the participants
were block randomized into pairs according to HFCS activ-
ity level (grades 6-8 vs 4-5), using a computer-generated set
of random numbers. All randomization, sequence genera-
tion, and preparation of group allocation materials were
performed by researchers who had no direct contact with
the clinical aspects of the trial.
Interventions
We planned 15 sets of daily life UL exercises (eg, fill up a
glass of water or pick up a coin and put it in a money box;
Table 1). Each set was composed by 3 sequential UL goal-
related actions of increasing complexity. In order to grade
the activities according to the range of children capabilities,
2 series of sets were conceived in relation to the HFCS level.
The exercises used the same material but differed in type of
movement (ie, range of movement, type of grasp) to guaran-
tee the feasibility of the proposed activity both in terms of
movements and goal. During the rehabilitation sessions,
each child from both groups sat on a chair with both arms
placed on a table in front of a large monitor screen (22 inches)
positioned at 1 m. A staff member sat at the child’s affected
side to prompt attention during task execution. The experi-
mental group performed the UP-CAT protocol, which
required the observation of video sequences showing uni-
manual or bimanual goal-directed actions followed by the
810 Neurorehabilitation and Neural Repair 27(9)

Table 1.  List of Goal-Directed Actions Performed by All Children and First Observed in Video Clips by the Experimental Group
During Action Observation Treatment.

Unimanual  1 Remove large lid from container, take out coloured candy, and place it in glass, pour water in glass
 2 Pick colored card (blue, yellow, red), turn it over, and match it to similar figure to make pairs
 3 Pick up rubber stamp, press it against horizontal and vertical plane to print figure
 4 Pick up coin, put it into money box through slot
 5 Pick up animal-shaped sponge stamp, press it against horizontal and vertical plane to print figure
 6 Pick up spray can and spray
 7 Lift open cap on tube containing shimmery powder and pour some on sheet of paper
 8 Pick up toy fishing rod and catch magnetic animals
Bimanual  9 Use hole punch to make holes in sheet of paper and match holes on studs
10 Wet and wring cloth and insert it in toy washing machine
11 Insert cards in clothespin in horizontal and vertical plane
12 Roll piece of Play-Doh into ball and put it into toy oven
13 Put coin in wallet and put wallet into box
14 Make figure using stencil and toothbrush soaked in tempera paint
15 Decorate frame with pieces of mosaic

execution of the observed actions either with their plegic UL
for unimanual or with both ULs for bimanual actions. Each
video sequence lasted 3 minutes and showed one goal-
directed action that was repeated a number of times, depend-
ing on the duration of the video (minimum 15 times). Then
the child was required to perform the same observed action
for 3 minutes in the exact order and with the same objects as
shown in the video. The therapist encouraged the child by
providing verbal suggestions without performing any dem-
onstration. The child had to continuously repeat the observed
action for 3 minutes. Subsequently, the same video sequence
was replayed a second time. Every day, 3 different goal-
directed actions of increasing complexity were observed and
imitated for a total time of about 60 minutes, including rest-
ing intervals. Children underwent 15 rehabilitation sessions
on 15 consecutive working days for a total of 45 different
goal-directed actions. Children from the control sample
watched computer games and then were verbally instructed
to perform the same UL actions and in the same order as the
experimental group. More details on the rehabilitation proto-
col have been reported elsewhere.32
Outcomes
Trained child therapists blind to group assignment evalu-
ated all enrolled children at baseline (T0, before the train-
ing), and at 1 week (T1), 8 weeks (T2), and 24 weeks (T3)
after the end of the training. As primary outcome we adopted
the Assisting Hand Assessment (AHA)33 test, which evalu-
ates the spontaneous use of the assisting hand during a sem-
istructured play session with specific toys. As secondary
outcome we selected the Melbourne Assessment of
Unilateral Upper Limb Function (MUUL).37 Both these
assessments were videotaped and then scored by observers
who were blind as to the group allocation and assessment
order. Moreover, to evaluate bimanual home and commu-
nity activities, parents filled out the ABILHAND-Kids
questionnaire,38 following the same experimental assess-
ment time schedule. Parents were blinded to the group
assignment.
Statistical Methods
The RCT was designed to evaluate the actual efficiency of
OTI in improving bimanual UL activity performance.
According to CONSORT guidelines, the sample size esti-
mates were based on projected treatment effect on the pri-
mary outcome measure (AHA). The AHA scale
responsiveness to change has been shown in a study in
which Eliasson et al39 used this scale as the outcome mea-
sure in evaluating the effects of a modified model of con-
straint-induced movement therapy. The authors reported a
significant effect size of 1.16. The statistical analysis indi-
cated that, to detect a 1.16 effect size at a significant level of
.05 and 80% power, a minimum sample size of 12 subjects
per group was required. Clinical data were analyzed by
means of the Statistical Package for Social Sciences (SPSS,
version 20.0). Means and standard deviation of the rehabili-
tation scores for both groups were calculated to identify
potential baseline differences between groups. As a first
step, between-group differences for all selected outcome
measures were evaluated at T0, by means of Mann–Whitney
U independent sample test, to verify that the 2 groups had
the same baseline.
To test our first hypothesis the between-group differ-
ences for the primary and secondary outcome measures
were evaluated at the primary endpoint (T1), compared
with T0, by means of Mann–Whitney U independent sam-
ple test. This same test was performed for the differences
between T2 and T3 and baseline (T0), to test the secondary

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Sgandurra et al 811
Figure 1.  Flow diagram of Upper Limb Children Action
Observation Training (UP-CAT) study aimed to compare the
results of observation of upper limb goal-directed actions
followed by execution (action observation therapy) to
observation of no relevant computer games followed by the
execution of the same actions (control group). No children
enrolled missed any follow-up sessions.
hypothesis, that is, whether an effect was retained at follow-
ing checks. This last hypothesis was also examined by
Wilcoxon matched-pairs signed rank test between T0 and
the subsequent assessments (T1, T2, and T3) for each group
in the primary outcome measure. Bonferroni corrections
were used, resulting in a significance level of P < .0166, to
account for multiple comparisons. To detect if significant
changes were correlated to the level of HFCS, we performed
a correlation analysis between the change scores of primary
endpoint time (T1) and baseline versus HFCS for the pri-
mary outcome measure.
Results
Recruitment and Study Population
As indicated in Figure 1, 24 children were enrolled out of
66 assessed for eligibility at the 2 centers. A total of 42 chil-
dren were excluded because either they did not meet the
inclusion criteria or parents declined participation.
Thereafter, no subjects missed any follow-up sessions; chil-
dren and parents maintained their interest on the trial and no
adverse events were detected. The experimental and control
groups had similar demographic and clinical baseline char-
acteristics (see Table 2). No differences in baseline scores
for AHA (P = .31), MUUL (P = .40), and ABILHAND-Kids
(P = .56) between groups were found.
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Table 3 shows between-group results for the primary and
secondary outcome measures.
Primary Outcome
Assisting Hand Assessment.  At the primary endpoint (T1)
between-group difference in the changes was significant
(P = .008) and this difference tended to remain at T2 and
T3, although at the limits of statistical significance (T2 −
T0, P = .019; T3 − T0, P = .049; Table 3).
Within-group differences were significant at all follow-
up assessments (T1, T2, and T3) versus T0 (P = .005, .016,
and .007, respectively) in the experimental group but not in
the control group (P = .09, .44, and .37, respectively).
Moreover, the changes observed in the experimental
group were greater than the recommended smallest detect-
able difference (SDD; >.76 logits)40 in contrast to the con-
trol group.
Finally, no correlation was found between the changes
scores of T1 and T0 versus level of HFCS (Pearson .526,
P = .079).
Secondary Outcomes
Melbourne Assessment of Unilateral Upper Limb Func-
tion.  Between-group differences in the changes were sig-
nificant neither at T1 (P = .93) nor at T2 and T3 (T2 − T0,
P = .84, T3 − T0, P = .79).
However, the SDD for both groups was smaller than the
clinically significant level of 8.9%41 at all time points.
ABILHAND-Kids. At T1 between-group differences in the
changes were not significant (P = .15) and so also at T2 and
T3 (T2 − T0, P = .14, T3 − T0, P = .12).
Discussion
In this RCT study, we proposed a 3-week paradigm of
intensive UL action observation training in a group of chil-
dren with hemiplegia. Our results indicate that this new
rehabilitation approach is effective in improving UL activ-
ity performance in daily activities and that these effects tend
to persist over time. In fact, immediately at the end of the
planned training, between-group changes were statistically
significant at AHA, the primary outcome measure.
Moreover, within-group analysis indicates a significant
improvement of the experimental group that continued in
the follow-up assessments, whereas the control group
remained unchanged. At ABILHAND-Kids no between-
group differences were found. MUUL scores did not statis-
tically change at between-group analysis and the
within-group score changes did not reach the SDD, that is,
the minimum change for a clinically significant change.
Similar findings, that is, significant changes at MUUL
812 Neurorehabilitation and Neural Repair 27(9)

Table 2.  Main clinical characteristics of experimental and control cases.

Experimental Group (n = 12) Control Group (n = 12)

Age (years)  
 Mean ± SD 9.48 ± 2.12 9.94 ± 2.77
 Range 6.48-12.69 6.12-14.39
Gender (males) 8 8
Side of hemiplegia (right) 10 7
Type of cerebral lesion at MRI  
  Brain malformation 1 2
  Abnormalities of PVWM 4 3
  Cortical/subcortical infarct 7 7
Hand ability level at HFCS  
 Mean ± SD 5.58 ± 1.31 5.75 ± 1.36

Abbreviations: SD, standard deviation; MRI, magnetic resonance imaging; PVWM: periventricular white matter; HFCS, House Functional Classification
System.

Table 3.  Between-Group Differences.

Experimental Group (n = 12) Control Group (n = 12) Pa

Primary outcome measure  
AHA (logits), mean ± SD  
  Baseline (T0) 2.04 ± 1.50 2.63 ± 1.69  
 T1 2.94 ± 1.69 2.78 ± 1.67 .008b
 T2 2.90 ± 1.81 2.78 ± 1.58 .019c
 T3 3.06 ± 2.25 2.83 ± 1.70 .049d
Secondary outcome measures  
MUUL (%), mean ± SD  
  Baseline (T0) 75.44 ± 10.65 78.91 ± 12.67  
 T1 79.90 ± 10.87 82.98 ± 10.35 .931b
 T2 81.28 ± 11.30 84.57 ± 9.80 .840c
 T3 78.05 ± 14.50 81.89 ± 14.00 .795d
ABILHAND-Kids (logits), mean ± SD  
  Baseline (T0) 0.65 ± 1.42 0.93 ± 2.28  
 T1 1.41 ± 0.87 1.21 ± 2.85 .149b
 T2 2.05 ± 1.19 1.22 ± 2.40 .043c
 T3 2.07 ± 1.34 1.27 ± 2.54 .118d

Abbreviations: SD, standard deviation; AHA, Assisting Hand Assessment; MUUL, Melbourne Assessment of Unilateral Upper Limb Function.
a
Asymptotic significance (two-tailed), significant level P < .0166.
b
Comparison between groups by Mann–Whitney U test for T1 − T0.
c
Comparison between groups by Mann–Whitney U test for T2 − T0.
d
Comparison between groups by Mann–Whitney U test for T3 − T0.

scores, but below clinical significance, were recently
reported in children with CP after a rehabilitation program
based on AOT.31
The main thrust for the UP-CAT was to detect the func-
tional modifications induced by the OTI in motor-impaired
children. OTI does make a real difference between the
experimental and the control group, since both groups exe-
cuted the same actions, but only the former was allowed to
observe the actions before being required to perform them.
The idea that this approach should elicit an improvement in
children with motor impairments stems from the properties
of the MNS, which has been shown to be very active during
the imitation of previously observed actions.18,42 Based on
this hypothesis, AOT rehabilitation programs have been
tested in adult patients affected by various types of brain
pathologies with results better than those obtained by a con-
trol intervention.22,23,25,43,44 The challenge of UP-CAT was
to apply this new model as an option in children rehabilita-
tion. Our intervention design was different from those pro-
posed in adults.22,44 Our intervention included unimanual
and bimanual actions to foster the use of the affected UL in
a range of daily activities requiring both types of

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Sgandurra et al 813
performances. Each video presented to the subjects lasted 3
minutes, a time sufficient to engage and maintain child’s
attention. In addition, the actions were presented only from
a first-person perspective to allow an immediate motor
identification with the observed UL.32 In fact, the presenta-
tion of actions from third person perspective would have
required the children to perform an additional mental rota-
tion, a skill that may not have been acquired yet45 or may be
impaired.46,47 Finally, videos showed actions belonging to
the UL motor repertoire of the enrolled children, that is, the
actions were graded according to the child’s baseline motor
impairment, as indicated by the HFCS. The setting of all
proposed exercises was the same for all children, but the
type of required movement (ie, range of motion, reach tra-
jectory, hand orientation, and opening, etc) was simplified
for the more severely impaired participants.
The results obtained, as assessed with the AHA, show a
change in the use of UL in daily activity but not in action
kinematics, as measured by the MUUL, as found in the
action observation programs in adults.22,23,44 This raises the
issue of whether motor learning is more kinematic or goal-
oriented in UCP children. A closer inspection of the video
recordings taken during the exercise sessions seems to indi-
cate that observation elicits in children a marked propensity
to preserve the task proficiency, by selecting movements
that guarantee the outcome goals, regardless of the kine-
matic resemblance with the observed model. We might
speculate that children exploit the property of the MNS to
activate goal representation15,48-50 rather than its capacity to
provide direct and detailed instructions on each movement
subcomponent, thus emphasizing the execution of the
action as a whole.
Interestingly, the AHA and ABILHAND-Kids measures
provide different types of results. The AHA evaluates the
spontaneous use of the assisting hand in semistructured
play, whereas ABILHAND-KIDS provides a raw score for
manual daily activities, not taking into account the involve-
ment of a single hand (be it the affected one or not) or of
both hands. A child could obtain the same score while exe-
cuting an activity with one hand (healthy hand) or with both
hands. In addition, AHA and not ABILHAND-KIDS scores
reveal that a child improves the efficiency of his affected
hand in bimanual activities, by enhancing the use of the
assisting hand.
So far, there are no standard intervention protocols for
UL management in children with CP. Rehabilitation pro-
grams vary in terms of duration, intensity of training and
frequency. Furthermore, they are mostly based on changes
induced by physiotherapy, orthotics, or medications, for
example, for spasticity, aimed at modifying the expression
of centrally generated motor schemas (“bottom-up”
approach). None of these protocols has been proven to have
an advantage over the others, besides often being time con-
suming and costly.
Downloaded from nnr.sagepub.com at National Dong Hwa University on March 20, 2014
In this study we approached the issue of motor rehabili-
tation in children from a completely different perspective,
as we aimed at directly inducing a functional modification
of the cortical components underpinning the action organi-
zation, exploiting the peculiar features of the MNS. Among
the major advantages of using this “top-down” model is the
possibility of recruiting a very early ability of children,
namely that of imitating by observation.51
To the best of our knowledge there is only one study,
recently published, that deals with AOT treatment, applied
to a small group of children with various types of CP.31 The
results of MUUL showed a rapid gain immediately subse-
quent to the intervention, with a statistically significant dif-
ference between the experimental and control groups, but
with a score gain that, as in our study, was much lower than
the recommended SDD for this test, that is, 8.9%.41 A gain
lower than SDD value may not reflect a true change in func-
tion but rather a “chance” occurrence or an error in mea-
surement and therefore, even if statistically significant, it
does not meet the requirement for a real improvement.41
Unfortunately, no other outcome measures or any longer
term follow-up checks were provided.31
A limitation of the present study is the small number of
children enrolled, which was, however, adequate according
to power analysis for our primary outcome. Moreover, the
homogeneity of the sample, owing to the stringent inclusion
criteria, besides a careful statistical treatment of the data
provides a high reliability of the obtained results. Moreover,
the type of intervention, tailored according to the severity of
hand motor impairment, is clearly described in terms of
video presentation, setting, object sequences, and therapist
behavior.32 The effectiveness of exercise tailoring is con-
firmed by the lack of significant correlation between func-
tional changes and HFCS levels. It should also be noted that
the task proposed to the children sustained their attention
across all sessions. A further important implication of this
study is the constant involvement of the families to prevent
interruption of the rehabilitation program.
Conclusions
Action observation training appears to be effective in
improving affected UL daily actions with effects that persist
at 6 months. Our therapeutic protocol was inexpensive and
time efficient and should be an easily reproducible rehabili-
tation program.
Acknowledgments
We acknowledge the contribution of physical therapists Elisa Sicola,
Roberta Di Pietro, and Maria Cristina Filippi for the arrangement of
exercises and of Valentina Burzi, Caterina Di Gioia, Francesca Foti,
and Eliana Parente (all MDs) for videos collection and medical
checks. We also thank Vincent Corsentino for reviewing the English
of the article and Giuseppe Rossi for statistical advice.
814 Neurorehabilitation and Neural Repair 27(9)
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with
12. Weller C, McNeil J. CONSORT 2010 statement: updated
respect to the research, authorship, and/or publication of this
article.
13. Lacourse MG, Orr EL, Cramer SC, Cohen MJ. Brain
Funding
The author(s) disclosed receipt of the following financial support
for the research, authorship, and/or publication of this article:
Grants for this trial have been obtained from Emilia Romagna
Region (Regional Research Project “New perspectives on reha-
bilitation in adults and children with motor disorders, autistic
spectrum disorders, and in disorders of empathic communication:
the role of mirror-neuron system”) and the Italian Ministry of
Health (RC 2010-2011).
References
1. Krägeloh-Mann I, Cans C. Cerebral palsy update. Brain Dev.
2009;31:537-544.
2. Uvebrant P. Hemiplegic cerebral palsy: aetiology and out-
come. Acta Paediatr Scand. 1988;345:1-100.
3. Cioni G, Sgandurra G, Muzzini S, Paolicelli PB, Ferrari A.
Forms of hemiplegia. In: Ferrari A, Cioni G, eds. The Spastic
Forms of Cerebral Palsy. A Guide to the Assessment of
Adaptive Functions. Milan, Italy: Springer-Verlag; 2009:331-
353.
4. Sköld A, Josephsson S, Eliasson AC. Performing biman-
ual activities—the experiences of young persons with
hemiplegic cerebral palsy. Am J Occup Ther. 2004;58:
416-425.
5. Sakzewski L, Ziviani J, Boyd R. The relationship between uni-
manual capacity and bimanual performance in children with
congenital hemiplegia. Dev Med Child Neurol. 2010;52:811-
816.
6. Boyd RN, Morris ME, Graham HK. Management of upper
limb dysfunction in children with cerebral palsy: a systematic
review. Eur J Neurol. 2001;8(suppl 5):150-166.
7. Sakzewski L, Ziviani J, Boyd R. Systematic review and
meta-analysis of therapeutic management of upper limb dys-
function in children with congenital hemiplegia. Pediatrics.
2009;123:E1111-E1122.
8. Aarts PB, Jongerius PH, Geerdink YA, van Limbeek J, Geurts
AC. Effectiveness of modified constraint-induced movement
therapy in children with unilateral spastic cerebral palsy: a
randomized controlled trial. Neurorehabil Neural Repair.
2010;24:509-518.
9. Sakzewski L, Ziviani J, Abbott DF, Macdonell RA, Jackson
GD, Boyd RN. Equivalent retention of gains at 1 year after
training with constraint-induced or bimanual therapy in chil-
dren with unilateral cerebral palsy. Neurorehabil Neural
Repair. 2011;25:664-671.
10. Gordon AM, Hung YC, Brandao M, et al. Bimanual training
and constraint-induced movement therapy in children with
hemiplegic cerebral palsy: a randomized trial. Neurorehabil
Neural Repair. 2011;25:692-702.
11. Koman LA, Smith BP, Williams R, et al. Upper extrem-
ity spasticity in children with cerebral palsy: a randomized,
double-blind, placebo-controlled study of the short-term
Downloaded from nnr.sagepub.com at National Dong Hwa University on March 20, 2014
outcomes of treatment with botulinum A toxin. J Hand Surg
Am. 2013;38:435-446.
guidelines can improve wound care. J Wound Care.
2010;19:347-353.
activation during execution and motor imagery of novel
and skilled sequential hand movements. Neuroimage.
2005;27:505-519.
14. Munzert J, Lorey B, Zentgraf K. Cognitive motor processes:
the role of motor imagery in the study of motor representa-
tions. Brain Res Rev. 2009;60:306-326.
15. Gallese V, Fadiga L, Fogassi L, Rizzolatti G. Action recogni-
tion in the premotor cortex. Brain. 1996;119:593-609.
16. Fabbri-Destro M, Rizzolatti G. Mirror neurons and mirror
systems in monkey and humans. Physiology. 2008;23:171-
179.
17. Rizzolatti G, Fogassi L, Gallese V. The mirror neuron system:
a motor-based mechanism for action and intention under-
standing. In: Gazzaniga M, ed. The Cognitive Neuroscience
IV. Cambridge, MA: MIT Press; 2009:625-640.
18. Buccino G, Vogt S, Ritzl A, et al. Neural circuits underly-
ing imitation learning of hand actions: an event-related fMRI
study. Neuron. 2004;42:323-334.
19. Cross ES, Hamilton AF, Grafton ST. Building a motor simu-
lation de novo: observation of dance by dancers. Neuroimage.
2006;31:1257-1267.
20. Pomeroy VM, Clark CA, Miller JS, Baron JC, Markus HS,
Tallis RC. The potential for utilizing the “mirror neurone
system” to enhance recovery of the severely affected upper
limb early after stroke: a review and hypothesis. Neurorehabil
Neural Repair. 2005;19:4-13.
21. Garrison KA, Winstein CJ, Aziz-Zadeh L. The mirror neuron
system: a neural substrate for methods in stroke rehabilitation.
Neurorehabil Neural Repair. 2010;24:404-412.
22. Ertelt D, Small S, Solodkin A, et al. Action observation has a
positive impact on rehabilitation of motor deficits after stroke.
Neuroimage. 2007;36(suppl 2):T164-T173.
23. Franceschini M, Agosti M, Cantagallo A, Sale P, Mancuso
M, Buccino G. Mirror neurons: action observation treatment
as a tool in stroke rehabilitation. Eur J Phys Rehabil Med.
2010;46:1-7.
24. Alegre M, Rodríguez-Oroz MC, Valencia M, et al. Changes
in subthalamic activity during movement observation in
Parkinson’s disease: is the mirror system mirrored in the basal
ganglia? Clin Neurophysiol. 2010;121:414-425.
25. Pelosin E, Bove M, Ruggeri P, Avanzino L, Abbruzzese
G. Reduction of bradykinesia of finger movements by a
single session of action observation in Parkinson disease.
Neurorehabil Neural Repair. 2013;27:552-560.
26. Bellelli G, Buccino G, Bernardini B, Padovani A, Trabucchi
M. Action observation treatment improves recovery of post-
surgical orthopedic patients: evidence for a top-down effect?
Arch Phys Med Rehabil. 2010;91:1489-1494.
27. Meltzoff AN, Moore MK. Imitation of facial and manual ges-
tures by human neonates. Science. 1977;198:74-78.
28. Paulus M, Hunnius S, Vissers M, Bekkering H. Imitation in
infancy: rational or motor resonance? Child Dev. 2011;82:
1047-1057.
Sgandurra et al 815
29. Shimada S, Hiraki K. Infant’s brain responses to live and tele-
vised actions. Neuroimage. 2006;32:930-939.
30. Nyström P. The infant mirror neuron system studied with high
density EEG. Soc Neurosci. 2008;3:334-347.
31. Buccino G, Arisi D, Gough P, et al. Improving upper limb
motor functions through action observation treatment: a pilot
study in children with cerebral palsy. Dev Med Child Neurol.
2012;54:822-828.
32. Sgandurra G, Ferrari A, Cossu G, et al. Upper limb chil-
dren action-observation training (UP-CAT): a randomised
controlled trial in hemiplegic cerebral palsy. BMC Neurol.
2011;11:80.
33. Krumlinde-Sundholm L, Holmefur M, Kottorp A, Eliasson,
AC. The Assisting Hand Assessment: current evidence of
validity, reliability, and responsiveness to change. Dev Med
Child Neurol. 2007;49:259-264.
34. Bohannon RW, Smith MB. Interrater reliability of a modified
Ashworth scale of muscle spasticity. Phys Ther. 1987;67:206-
207.
35. House JH, Gwathmey FW, Fidler MO. A dynamic approach
to the thumb-in-palm deformity in cerebral palsy: evalua-
tion and results in fifty-six patients. J Bone Joint Surg Am.
1981;63:216-225.
36. Koman LA, Williams RM, Evans PJ, et al. Quantification of
upper extremity function and range of motion in children with
cerebral palsy. Dev Med Child Neurol. 2008;50:910-917.
37. Randall M, Carlin JB, Chondros P, Reddihough D. Reliability
of the Melbourne Assessment of Unilateral Upper Limb
Function. Dev Med Child Neurol. 2001;43:761-767.
38. Arnould C, Penta M, Renders A, Thonnard JL. ABILHAND-
Kids: a measure of manual ability in children with cerebral
palsy. Neurology. 2004;63:1045-1052.
39. Eliasson AC, Krumlinde-Sundholm L, Shaw K, Wang C.
Effects of constraint-induced movement therapy in young
children with hemiplegic cerebral palsy: an adapted model.
Dev Med Child Neurol. 2005;47:266-275.
40. Holmefur M, Aarts P, Hoare B, Krumlinde-Sundholm L.
Test-retest and alternate forms reliability of the assisting hand
assessment. J Rehabil Med. 2009;41:886-891.
41. Klingels K, De Cock P, Desloovere K, et al. Comparison
of the Melbourne Assessment of Unilateral Upper Limb
Downloaded from nnr.sagepub.com at National Dong Hwa University on March 20, 2014
Function and the Quality of Upper Extremity Skills Test
in hemiplegic CP. Dev Med Child Neurol. 2008;50:
904-909.
42. Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta
JC, Rizzolatti G. Cortical mechanisms of human imitation.
Science. 1999;286:2526-2528.
43. da Silva Cameirão M, Bermúdez I, Badia S, Duarte E,
Verschure PF. Virtual reality based rehabilitation speeds
up functional recovery of the upper extremities after stroke:
a randomized controlled pilot study in the acute phase of
stroke using the rehabilitation gaming system. Restor Neurol
Neurosci. 2011;29:287-298.
44. Franceschini M, Ceravolo MG, Agosti M, et al. Clinical
relevance of action observation in upper-limb stroke reha-
bilitation: a possible role in recovery of functional dexterity.
A randomized clinical trial. Neurorehabil Neural Repair.
2012;26:456-462.
45. Molina M, Tijus C, Jouen F. The emergence of motor imagery
in children. J Exp Child Psychol. 2008;99:196-209.
46. Mutsaarts M, Steenbergen B, Bekkering H. Impaired motor
imagery in right hemiparetic cerebral palsy. Neuropsychologia.
2007;45:853-859.
47. Crajé C, van Elk M, Beeren M, van Schie HT, Bekkering H,
Steenbergen B. Compromised motor planning and motor
imagery in right hemiparetic cerebral palsy. Res Dev Disabil.
2010;31:1313-1322.
48. Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F,
Rizzolatti G. Parietal lobe: from action organization to inten-
tion understanding. Science. 2005;308:662-667.
49. Gazzola V, van der Worp H, Mulder T, Wicker B, Rizzolatti
G, Keysers C. Aplasics born without hands mirror the goal
of hand actions with their feet. Curr Biol. 2007;17:1235-
1240.
50. Jastorff J, Begliomini C, Fabbri-Destro M, Rizzolatti G,
Orban GA. Coding observed motor acts: different organi-
zational principles in the parietal and premotor cortex of
humans. J Neurophysiol. 2010;104:128-140.
51. Meltzoff AN. Elements of a developmental theory of imita-
tion. In: Meltzoff AN, Prinz W, eds. The Imitative Mind.
Development, Evolution and Brain Bases. Cambridge,
England: Cambridge University Press; 2002:19-41.