Exp Brain Res DOI 10.1007/s00221-016-4554-3

RESEARCH ARTICLE

Motor imagery training promotes motor learning in adolescents with cerebral palsy: comparison between left and right hemiparesis Audrey Sartori Cabral‑Sequeira1,2 · Daniel Boari Coelho1 · Luis Augusto Teixeira1 

Received: 13 October 2015 / Accepted: 4 January 2016 © Springer-Verlag Berlin Heidelberg 2016

Abstract  This experiment was designed to evaluate the effects of pure motor imagery training (MIT) and its combination with physical practice on learning an aiming task with the more affected arm in adolescents suffering from cerebral palsy. Effect of MIT was evaluated as a function of side of hemiparesis. The experiment was accomplished by 11- to 16-year-old participants (M = 13.58 years), who suffered left (n = 16) or right (n = 15) mild hemiparesis. They were exposed to pure MIT (day 1) followed by physical practice (day 2) on an aiming task demanding movement accuracy and speed. Posttraining movement kinematics of the group receiving MIT were compared with movement kinematics of the control group after receiving recreational activities (day 1) and physical practice (day 2). Kinematic analysis showed that MIT led to decreased movement time and straighter hand displacements to the target. Performance achievements from MIT were increased with further physical practice, leading to enhanced effects on motor learning. Retention evaluation indicated that performance improvement from pure MIT and its combination with physical practice were stable over time. Performance achievements were equivalent between adolescents with either right or left hemiparesis, suggesting similar capacity between these groups to achieve performance improvement from pure imagery training and from its association with physical practice. Our results suggest that motor imagery

* Luis Augusto Teixeira [email protected] 1

Human Motor Systems Lab, School of Physical Education and Sport, University of São Paulo, Av. Prof. Mello Moraes, 65. Cidade Universitária, São Paulo, SP 05508‑030, Brazil

2

Association for Assistance to Deficient Children, Av. Professor Ascendino Reis, 724, São Paulo, SP, Brazil





training is a procedure potentially useful to increase motor learning achievements in individuals suffering from cerebral palsy. Keywords  Mental practice · Motor learning · Training techniques · Hemiparesis · Adolescence

Introduction Unilateral cerebral palsy is a lesion affecting motor control centers of one of the cerebral hemispheres of the developing brain, leading to major motor disabilities in the body side contralateral to the lesion. Some of the main deficits in the control of the more affected arm have been shown in children’s performance of reaching and aiming tasks, with slower (Chang et al. 2005; Coluccini et al. 2007; Rönnqvist and Rösblad 2007), and more segmented (Rönnqvist and Rösblad 2007) movements as compared to typically developing children. Additionally, reduced range of motion of the shoulder on the frontal plane has been reported in children suffering from cerebral palsy (Coluccini et al. 2007). Similar kinematic characteristics have been found in movements of adults affected by cerebral palsy (Ricken et al. 2005). Deficits in motor behavior from cerebral palsy have been shown to be associated with deficient planning of motor actions (Steenbergen et al. 2007b). Reduced capacity of movement planning seems to be particularly severe in cases of lesions to the left cerebral hemisphere (Crajé et al. 2009), a finding consistent with results of neuroimaging studies suggesting left hemisphere dominance for action planning (Schluter et al. 2001; Johnson-Frey et al. 2005; Tomasino et al. 2011). By assessing motor planning through object manipulation and assessing motor imagery by means of chronometry of mental rotation, Crajé et al.

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(2010) further evidenced that compromised motor planning from lesions to the left cerebral hemisphere is associated with a decreased capacity to mentally simulate body movements (see also van Elk et al. 2010). Lesion to the right cerebral hemisphere, on the other hand, has been reported to do not affect motor imagery capacity (Mutsaarts et al. 2007). In a recent study in children and adolescents with cerebral palsy, Chinier et al. (2014) evidenced that left cerebral hemisphere damage leads to decreased brain activation associated with motor imagery of manual movements while right cerebral hemisphere damage is characterized by a pattern of bilateral activation of the frontoparietal brain network, similar to that observed in typically developing individuals. These findings converge to indicate dominance of the left cerebral hemisphere for generating mental movement simulation, suggesting that motor imagery training (MIT) might be useful only for neurological patients having the left cerebral hemisphere spared by the lesion. Research has shown that MIT induces important effects on learning and associated functional cerebral reorganization. In neurologically healthy individuals, Bernardi et al. (2013) showed that MIT leads to improved speed and accuracy of manual movements in difficult music sequences at the piano keyboard. In further research, Gentili et al. (2006, 2010) showed that MIT of a sequential multiple-target pointing task induced performance gains in movement straightness and speed, with performance improvements persisting over time (Gentili et al. 2010). Further results by Allami et al. (2008) showed that for certain motor tasks MIT can lead to performance gains even higher than those observed as a result of physical practice (see also Zhang et al. 2011). Neurophysiological studies have revealed that behavioral gains from MIT are associated with functional reorganization of neural maps activated with the imagined movements, inducing similar brain plasticity to that observed from physical practice (Pascual-Leone et al. 1995; Jackson et al. 2003; Zhang et al. 2011; Allami et al. 2014). Allami et al. (2014), in particular, showed that MIT followed by a limited amount of physical trials on a manual task led to similar performance gains in comparison with exclusive physical practice. Additionally, MIT was shown to induce the same increment of cortical excitability over the premotor regions as that observed after physical practice. These findings suggest that MIT modulates activity in the neural network associated with execution of the imagined movement, increasing the potential of physical practice to induce higher levels of motor performance. Evidence for the effect of MIT on motor learning in individuals with cerebral lesions has been provided by clinical studies in individuals affected by stroke (Liu et al. 2004, 2014; Page et al. 2005, 2009; Hwang et al. 2010; Cho et al. 2013). In those studies, rehabilitation protocols combining MIT and physical practice have been compared

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against exclusive physical practice of functional tasks. Consistent with experimental results showing advantage of combination of imagery and physical practice (Allami et al. 2008, 2014; Zhang et al. 2011), those clinical studies have reported the benefit of associating MIT with physical practice protocols to achieve improved movement control of the affected limbs (see Ietswaart et al. 2011, for divergent results). Additionally, at the neural level Page et al. (2009) showed that MIT of wrist movements of the affected hand led to increased activation of motor and premotor areas in both cerebral hemispheres (see also Liu et al. 2014). From these findings, MIT seems to be an effective tool to induce neural plasticity and the corresponding improvement of motor performance in individuals who suffered a cerebral insult. Steenbergen et al. (2009) have suggested that MIT might be a potential tool for improvement of motor performance of individuals suffering not only from stroke but also from cerebral palsy. However, our review indicated that no study scrutinizing the possible effect of MIT on motor learning in individuals with cerebral palsy is available thus far in the literature. The present study was designed to evaluate the effect of MIT on motor learning in adolescents suffering from cerebral palsy, comparing individuals with right versus left hemiparesis. Previous results have documented the imagery capacity in typically developing adolescents (Choudhury et al. 2007a), with correlated speed-accuracy tradeoff between executed and imagined aiming movements (Choudhury et al. 2007b). These results suggest that adolescents might benefit from their imagery capacity to promote motor learning if submitted to MIT. Based on results of deficient capacity of motor imagery in individuals with lesions to the left cerebral hemisphere (Crajé et al. 2009), we hypothesized that MIT leads to performance gains only in adolescents with left hemiparesis. To test this hypothesis, we provided experimental groups with right or left hemiparesis initially with pure motor imagery training and then supplemented imagery training with physical practice, having as reference for the effects on motor learning equivalent control groups receiving no practice and then physical practice.

Methods Participants Adolescents suffering from mild cerebral palsy participated of this experiment. They had been treated in their childhood in an institution specialized for children’s neurological diseases. Inclusion criteria were level 1 in the gross motor function classification system (Palisano et al. 1997), no dystonia or athetosis (as diagnosed by the institutional

Exp Brain Res

Fig. 1  Image of a participant with right hemiparesis touching the target with the pointer after an inward motion clearing the obstacle (white cube). Markers at the pointer tip and on the arm were used for kinematic analysis

neurologist), and no neuromuscular blockade in the more affected arm by means of injection of alcohol, phenol, or botulinum toxin type A within the period of 2 months before data collection. From these criteria, we selected initially 49 participants. Exclusion criteria were manifestation of incapacity to follow simple verbal instructions (n = 8), incapacity to perform the experimental task (n  = 4), and participant’s declaration of incapacity to mentally simulate self-performance of the experimental task (n  = 4). Two other participants dropped out after the first day of the experiment. The experiment was accomplished by 11to 16-year-old participants (M = 13.58 years, SD = 1.74), who suffered left (n = 16, 8 of each sex) or right (n = 15, 8 males/7 females) mild hemiparesis. Procedures were approved by the institutional ethics committee, with participants and parents providing written informed consent, in accordance with the standards established in the Declaration of Helsinki. Task and equipment Motor learning as a result of mental and/or physical practice was measured in the more affected arm on manual aiming at a spatial target. The task was performed with the participant in a seating position on a height adjustable chair. The task consisted of aiming as fast and accurately as possible at a circular 2-cm-diameter target set-up on a frame in front of the participant. To make contact with the target, participants used a custom-built light (20 g) 10-cmlong pointer attached to a handle, which was manipulated through palmar grasping in a pronated position with the more affected hand (Fig. 1). Initial position to perform the task was lightly touching the tip of the pointer at a

2-cm-diameter spot, approximately aligned with the shoulder of the more affected arm. The target was positioned 30 cm from the initial position in parallel with participants’ frontal plane. Movements were initiated ipsilaterally to the more affected arm and then performed through an inward arm displacement crossing the egocentric mid sagittal plane into the contralateral hemispace to hit the target. To increase task difficulty, a 3-cm sided cube was used as an obstacle positioned on the frame midway between the initial and the target position. The pointer was to be moved over that obstacle in the displacement toward the target. Participants were positioned with their body midline aligned with the obstacle, approximately 20 cm from the proximal frame border. Motor performance was evaluated through movement kinematics. For that purpose, 1-cmdiameter reflective passive markers were attached to the following points: distal end of the pointer, second metacarpophalangeal joint, internal portion of the wrist, lateral epicondyle, acromions of both body sides, and manubrium sterni. The markers were tracked by means of four optoelectronic cameras surrounding the action space (Vicon, MX3+). Experimental design and procedures The experiment was conducted over two sessions of practice, with each one followed by an immediate and a delayed (retention) evaluation. In the first session, we evaluated the effect of pure MIT. The second session had the purpose of assessing the effect of supplementing MIT with physical practice. Participants suffering from hemiparesis either to the right or to the left body side were randomly assigned to an experimental or control condition, balancing the numbers of male and female participants within group. The experimental design was composed by four groups: right hemiparesis, motor imagery training and control; and the same composition for left hemiparesis. Groups were gender-matched and consisted of eight participants each, except controls for left hemiparesis (n = 7). Sessions of practice were provided over 2 days. On day 1, MIT groups had two sets of 50 mental rehearsals, with each set divided into five blocks of ten rehearsals. Participants were instructed to mentally rehearse the aiming movement from a first person proprioceptive perspective, trying to simulate the physical sensations of rapidly moving the more affected arm over the obstacle and finishing the movement by touching the target. They were instructed to refrain from making any arm movements during mental rehearsal. Instruction was immediately followed by demonstration of the movement by the experimenter sitting in front of the participant. In the sequence, participants performed a single physical trial for familiarization. Immediately before starting each mental rehearsal during imagery

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Exp Brain Res

Fig. 2  Summary of the experimental design. Activities performed by each group (MIT motor imagery training, Con control, R right hemiparesis, L left hemiparesis) on days 1 and 2, indicating the mode of practice and periods of testing

training, participants observed the action space. Then, they closed their eyes to rehearse movement execution, preventing attention deviation to objects in the laboratory and favoring concentration on the mental task. During mental rehearsals, participants maintained both hands relaxed and supported on the table, which was visually monitored by the experimenter. In the intervals between rehearsals, the experimenter reminded the participant to rehearse the movements of the more affected arm, trying to increase speed of the imagined movement over trials. Initiation and end of trials were signaled by the participant by tapping their index finger of the resting (less affected) arm on the supporting table. Rehearsals within a block were spaced by approximately 5 s, and rest intervals of 1 min were provided between blocks of 10 rehearsals, with 10 min of rest between sets of 50 rehearsals. Each set of 50 rehearsals was performed in the interval of approximately 12 min, with the whole session taking approximately 34 min to be concluded. On day 1, the control groups manipulated the keyboard of a personal computer with the less affected hand to play a game called “tetris” (accessed through www.freetetris.org). That game requires stacking different geometric virtual pieces to make horizontal lines with the purpose of earning points. They practiced the game during 12 min, then had a rest interval of 10 min, and concluded the session with additional 12-min playing the same game. The subsequent phase of the experiment took place following an interval of 24–48 h after the first day of practice. In this phase, all groups were provided with physical practice of the experimental aiming task. Consequently, results from this phase indicate the effect of pure physical practice in the control groups and the effect of combining imagery (day 1) and physical (day 2) training in the MIT groups. At practice onset, participants were instructed to try to make fast and accurate movements in aiming at the target and were verbally encouraged about every three trials to improve performance. Physical movements were the same as instructed for imagery training, with initial position ipsilateral to the more affected arm, and aiming at the target in the opposite hemifield on the action space by passing the pointer over the obstacle. Practice schedule

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was the same as for imagery training, with intertrial intervals of approximately 5 s, intervals of 1 min every 10 trials, and an interval of 10 min between blocks of 50 trials. The task was performed under full vision, without provision of extrinsic feedback. This experimental design, thus, differs from previous ones maintaining the summation of imagery and physical trials constant across groups while manipulating the ratio between them (e.g., Allami et al. 2008). In the present design, we maintained the number of physical trials constant across the groups, manipulating previous imagery training. From this design, one can conclude about performance achievements from pure MIT and its potential role in magnifying the effect of subsequent physical practice. Performance evaluation was made by means of three trials performed with the more affected arm, with the same instructions as those given for physical practice, emphasizing the importance of both movement speed and accuracy. Kinematic signals were sampled at a frequency of 200 Hz. Evaluation of the effects of practice was made as described next. Day 1: Posttest 1, performed 1 min following the end of the respective activities of the MIT and control groups, indicating the immediate effects of MIT. Day 2: Retention 1, performed immediately before physical practice, indicating retention of the effect of MIT in the first session on day 1. Posttest 2, performed 1 min following the end of the physical trials, indicating the immediate effects of physical practice preceded by imagery training (MIT groups) in comparison with pure physical practice (control groups). Retention 2, performed 30 min after the end of physical practice, indicating retention of performance achievements in the second session. The experimental design is summarized in Fig. 2. Analysis Kinematic data were first digitalized through the Vicon Nexus software (Vicon, Oxford, UK). Following visual inspection, analysis was performed through custom-made MATLAB (Mathworks, Inc, Natick, MA) routines. Raw data were filtered through a dual-pass fourth-order Butterworth filter with cutoff frequency set at 10 Hz. Analyses

Exp Brain Res Table 1  Mean values of kinematic analysis for the right and left hemiparesis MIT groups across tests

Right

Movement time (s) Movement straightness Peak height (mm) Sub-movements (n) Shoulder velocity (°/s) Elbow velocity (°/s) Radial error (mm)

Left

PT1

R1

PT2

R2

PT1

R1

PT2

R2

1.10 (.04) .91 (.05) 120.40 (37.69) 2.25 (1.16) 14.96 (7.80) 13.26 (6.91)

1.03 (.48) .89 (.06) 126.94 (29.54) 2.83 (1.15) 15.99 (9.67) 8.99 (6.74)

1.01 (.49) .93 (.04) 90.05 (15.07) 1.56 (.78) 23.00 (7.82) 9.81 (8.72)

.88 (.11) .93 (.03) 99.84 (25.04) 1.73 (.69) 18.58 (5.22) 6.43 (4.50)

.90 (.33) .94 (.03) 109.70 (27.42) 3.00 (1.84) 19.20 (8.95) 8.79 (6.27)

.85 (.16) .92 (.04) 112.63 (27.01) 2.38 (1.12) 18.83 (5.98) 9.47 (7,21)

.73 (.08) .93 (.04) 91.54 (30.79) 1.94 (1.15) 22.15 (5.52) 11.14 (7.20)

.72 (.12) .94 (.06) 90.20 (28.51) 2.23 (1.62) 22.40 (6.41) 9.57 (7.43)

14.58

6.98

9.50

7.51

11.62

15.78

10.97

9.60

(5.12)

(3.79)

(4.64)

(4.68)

(10.65)

(12.91)

(6.71)

(4.44)

were based on 3-D movement reconstruction. The following dependent variables were analyzed: Movement time, considering movement initiation/end as the time at which the pointer marker achieved the velocity of 20 mm/s with increasing/decreasing subsequent values. This variable is considered as one of the main global indexes of performance in aiming tasks. Movement straightness, given by the ratio of the distance between the initial marker position and the target by the length of hand displacement in the longitudinal-transversal (xy) plane. This variable indicates the ability to control dynamically joint torques to produce straight hand displacements toward the target. Frequency of sub-movements, given by the number of peaks sided by valleys in the velocity curve for differences in instantaneous velocities greater than 1 cm/s. Reduced frequency of submovements indicates less numerous adjustments through feedback mechanisms, characteristic of more skilled movements controlled in a predominant feedforward mode. Peak height, given by the maximum height achieved by the hand during the movement. Reduced peak height in hand displacement indicates a narrow safety margin to pass over the obstacle, favoring short movement times. Average joint angular velocity was calculated for the motion at the shoulder and elbow. These variables indicate velocity at specific segmental movement components. Radial error, distance between the pointer marker and the target position at movement end, indicating spatial accuracy at the end of movement. Trials for each test were averaged within participant for statistical analysis. Assumptions of parametric statistics were verified through the Shapiro–Wilk test. Significant differences are reported, accompanied by the respective effect sizes given by partial eta squared (η2). Post

hoc comparisons were made by means of Newman–Keuls procedures.

Results Statistical analysis was divided into two steps. First, we looked at the effect of MIT on motor performance as a function of side of hemiparesis. To evaluate the possible differential effect of MIT on motor learning between right and left hemiparesis, the two experimental groups were compared over tests. In this analysis, we evaluated whether side of hemiparesis affected the results of pure MIT and its association with physical practice, comparing between the two experimental groups immediate effects on motor performance and its retention over time. This analysis was made through two-way 2 (side: right × left hemiparesis) × 4 (test: posttest 1 × retention 1 × posttest 2 × retention 2) ANOVAs with repeated measures on the second factor. Results showed no significant main or interaction effects related to side of hemiparesis across the variables analyzed (P values >.1). Descriptive average results (standard errors in parenthesis) for the MIT groups with right versus left hemiparesis over tests are presented in Table 1. These results indicate that pure MIT or its association with physical practice did not affect differently performance of individuals with right or left hemiparesis. To assess the effect of MIT on motor learning, in the ensuing step of analysis we collapsed data of both the right and left hemiparesis MIT groups (n  = 16) to compare against the collapsed data from the right and left hemiparesis control groups (n  = 15). Some of the performance characteristics achieved from MIT and its association with

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physical practice are represented in Fig. 3. That figure presents kinematic profiles of single trials of left-to-right hand displacements (left hemiparesis) in the longitudinaltransversal plane, representing the group effect of imagery

Fig. 3  Single-trial kinematic profiles of left hand displacements (left to right) in the longitudinal (x) by transversal (y) plane, representing the increased movement straightness following pure imagery training in the posttest 1 (MIT-PT1) and following the combination of MIT with physical practice in posttest 2 (MIT-PT2), having as reference a participant of the control group evaluated in posttest 1 (Con-PT1)

Fig. 4  Mean values of kinematic analysis (standard errors represented by vertical bars), showing results of motor imagery training (MIT) in comparison with controls (Con) across tests (PT1 posttest 1, R1 retention 1, PT2 posttest 2, R2 retention 2) for the following vari-

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training on movement straightness in the posttest 1 (pure MIT effect) and posttest 2 (combination of MIT with physical practice) in comparison with a participant of the control group evaluated in the posttest 1. Statistical analysis was made through two-way 2 (practice: MIT × control) × 4 (test: posttest 1 × retention 1 × posttest 2 × retention 2) ANOVAs with repeated measures on the second factor. Analysis of movement time (Fig. 4a) showed significant main effects of practice, F(1, 29) = 6.47, P  = .02, η2  = .21, and test, F(3, 87) = 6.94, P  = .0003, η2  = .22. The effect of practice was due to lower values for MIT (M  = .71 s, SE = .10) in comparison with controls (M  = 1.10 s, SE = .10). Post hoc comparisons for the effect of test indicated that in posttest 2 (M  = .90 s, SE  = .05) and retention 2 (M  = .90 s, SE = .04) movement times were shorter than values achieved in the previous tests, posttest 1 (M = 1.07 s, SE = .07) and retention 1 (M = 1.04 s, SE = .06). Results for movement straightness (Fig.  4b) indicated a significant main effect of practice,

ables: a movement time (s), b movement straightness (normalized), c peak height (mm), d absolute frequency of sub-movements (n), and average angular velocity (°/s) for the e shoulder and f elbow motions

Exp Brain Res

F(1, 29) = 7.26, P = .01, η2 = .22. That effect was due to higher scores for MIT (M = .92, SE = .01) in comparison with controls (M = .88, SE = .03). Results for peak height (Fig.  4c) showed a significant main effect of test, F(3, 87)  = 6.63, P  = .0005, η2  = .21. Post hoc comparisons indicated that in posttest 2 (M = 101.87 mm, SE = 6.72) and retention 2 (M  = 99.07 mm, SE = 6.68) hand peak height was lower than in the posttest 1 (M = 120.13 mm, SE = 7.02) and retention 1(M = 116.04 mm, SE = 6.30). Analysis of frequency of sub-movements (Fig. 4d) showed a significant main effect of test, F(3, 87) = 3.21, P = .03, η2  = .11. Post hoc comparisons indicated lower values in the posttest 2 (M  = 2.42, SE = .28) in comparison with posttest 1 (M = 2.69, SE = .29) and retention 1 (M = 2.92, SE = .30). Analysis of angular velocity at the shoulder (Fig. 4e) showed a marginally significant main effect of practice, F(1, 29) = 3.48, P = .07, η2 = .13, and a significant main effect of test, F(3, 87) = 3.76, P  = .0004, η2  = .22. The effect of practice was due to higher shoulder velocity for MIT (M = 19.34°/s, SE = 1.87) in comparison with controls (M  = 14.80°/s, SE = 2.16). Post hoc comparisons for the effect of test indicated that values in posttest 2 (M = 19.88°/s, SE = 1.59) and retention 2 (M = 19.02°/s, SE  = 1.67) were higher than those observed in posttest 1 (M = 15.27°/s, SE = 1.43) and retention 1 (M = 15.40°/s, SE  = 1.39). Analysis of angular velocity at the elbow (Fig.  4f) indicated higher descriptive values for MIT than for controls, but no significant effects were found (F values .1). No significant main effects or interactions were found in the analysis of spatial error, with averages across phases of 10.96 mm (SE = 1.90) for MIT and of 9.11 mm (SE = 1.52) for the control groups, F values .08.

Discussion In this study, we assessed for the first time the effect of motor imagery training on motor learning in adolescents with cerebral palsy, testing the hypothesis that learning by imagery training is effective only for adolescents with left hemiparesis. Analysis indicated no effect associated with side of hemiparesis, suggesting that adolescents with right or left hemiparesis achieved equivalent motor performance from motor imagery training and its further association with physical practice. We found that imagery training induced faster and straighter movements, as revealed by the general advantage in those variables for the groups receiving imagery training in comparison with controls. The higher speed following motor imagery training seems to have been due particularly to faster proximal movements at the shoulder. These results indicate that imagery training

led to better results across tests, including the first posttest and retention evaluations, epochs indicating the effect of pure imagery training. The absence of practice by phase interactions indicates that the performance achieved as a result of imagery training persisted after the physical practice. This result suggests that gains from physical practice were additive to the previous achievements from imagery training, leading to higher levels of performance at the end of physical practice. Persistence of higher performance of the MIT group in the retention tests indicates that performance achievements from motor imagery training were stable over time, characterizing a motor learning effect. One of the main motivations of this research was to compare the effect of imagery training between adolescents suffering from right versus left hemiparesis. Since limited capacity of motor planning (Crajé et al. 2009, 2010) and imagery (Crajé et al. 2010; van Elk et al. 2010) has been reported to be characteristic of left but not right hemisphere lesions (Mutsaarts et al. 2007), we expected to find an effect of imagery training in adolescents with left hemiparesis only. However, our results showed that adolescents with either left or right hemiparesis benefited from imagery training, achieving equivalent performance from pure imagery training and from its association with physical practice. A possible interpretation of these results is that previous studies of imagery capacity in neurological patients have been made with relatively complex cognitive operations requiring mental rotation of a figure (Mutsaarts et al. 2007; Crajé et al. 2010; van Elk et al. 2010). The aiming task used in our experiment can be considered to be relatively simple in terms of mental simulation, requiring displacement of the more affected arm between two points from the participant’s personal perspective. In addition, participants were instructed to imagine the kinesthetic sensations from the movement, which does not occur in the task of mental image rotation (cf. Steenbergen et al. 2007a). These characteristics of the imagery training in our experiment may have favored simulation of movements with the more affected limb by adolescents with either right or left cerebral hemisphere lesions. Some support for this viewpoint has been provided recently (Spruijt et al. 2013). In the Spruijt et al.’s study, adolescents with left, right, or bilateral paresis due to cerebral palsy had their imagery capacity evaluated by means of chronometry of imagined and physically executed walking across paths combining different lengths and widths. Results showed that durations of the walking tasks were similar between physical and imagery trials. As most participants had unilateral right or combined right–left hemiparesis, it is apparent that left cerebral hemisphere lesion did not inhibit the capacity of mentally simulating the whole body displacement. Extending this interpretation to our results, it seems that individuals with right or left hemiparesis could improve manual movements from

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motor imagery training. However, as the numbers of participants in the MIT groups for right and left hemiparesis were relatively small, further research is required to support this conclusion. Lack of a learning effect for movement accuracy in our results diverges from previous results in neurologically healthy individuals showing improvement of accuracy from motor imagery training (Bernardi et al. 2013). That result may be due to emphasis on movement speed during practice. Although a similar emphasis on movement accuracy and speed was made in the initial instructions, participants were encouraged to increase speed in the imagined and physically performed movements during practice. This procedure may have biased participants’ attention to improve only movement speed during imagery and physical trials. Emphasis on movement speed in aiming movements has been shown to induce less accurate movements in healthy individuals (Elliott et al. 1991), and so may have hindered the improvement of this movement component during acquisition of the experimental task. We found absence of a significant effect of imagery training for peak movement height and frequency of sub-movements, with a general gain across groups following physical practice. From these results, it becomes apparent that imagery training did not affect those movement components, with requirement of physical practice for improvement. However, if one observes the descriptive values shown in the panels C and D of Fig. 4 an interesting (although nonsignificant) trend can be seen. Even though the groups in general presented lower averages in posttest and retention 2 as compared to posttest and retention 1, comparison of averages between practice conditions suggests lower values for imagery training than for the respective control groups for both peak height and sub-movements following physical practice. This descriptive relationship suggests that physical practice may have induced higher performance gains following motor imagery training. We consider the possibility that high movement variability, characteristic of individuals with cerebral palsy, may have masked an interaction between imagery and physical practice. If this is the case, we speculate about the possibility that performance improvement from imagery training is manifested only after its supplementation with physical practice, leading to better results in comparison with pure physical practice. Decreased movement time from imagery training in our results is consistent with previous findings of faster movements following imagery training in neurologically healthy individuals (Gentili et al. 2006, 2010; Allami et al. 2008, 2014; Bernardi et al. 2013) and in those affected by stroke (Stevens and Stoykov 2003). Moreover, enhanced movement straightness from pure imagery training has been previously found in healthy individuals (Gentili et al. 2010). Thus, our results indicating analogous performance

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achievements from imagery training in adolescents with cerebral palsy extend previous findings, showing the effectiveness of imagery training to promote performance improvement (for improvement of other components in neurological patients, see Liu et al. 2004, 2014; Page et al. 2005, 2009; Hwang et al. 2010; Cho et al. 2013). We also showed that faster aiming movements from MIT were due particularly to higher angular velocity at the shoulder. Increased adaptability has been shown at this joint in children with cerebral palsy to deal with task demands in reaching (Domellöf et al. 2009). From these observations, it is apparent that one important locus of higher movement speed from imagery training is at the proximal portion of limb control, contributing to attenuate one of the movement malfunctions induced by cerebral palsy represented by limited shoulder movements (Coluccini et al. 2007). Findings of faster and straighter movements following imagery training suggest that the altered movement dynamics of movement control provoked by cerebral palsy was successfully modeled in the mental space. Wolpert has proposed that action representation is a component of an internal forward model generated by the neural system, simulating the interplay between intrinsic and extrinsic forces in the dynamics of body movement control (Wolpert 1997; Flanagan et al. 2003). Based on this perspective, it is conceptualized that an efferent copy of the motor commands is produced when a movement is imagined, which is used to make predictions about sensory consequences of its physical execution. This proposition implies that to simulate a movement in the mental space deficits in movement control are taken into consideration, obeying the same neuromotor and biomechanical constraints (cf. Papaxanthis et al. 2003; Courtine et al. 2004). Consistent with this notion, previous research has shown that slower movements due to neurological disease are associated with longer times to complete a mental simulation of movements produced with the affected limbs (Dominey et al. 1995; Sabaté et al. 2004; Spruijt et al. 2013). Our results suggest that the adolescents evaluated in our experiment were able to generate accurate mental predictions of muscular and extrinsic forces acting on their more affected limb during movement execution, simulating the constraints imposed by the deficits in neuromotor control provoked by cerebral palsy. From the simulated consequences of imagined movements with the more affected limb, it seems that mental representations of that action are changed across practice trials to produce more skilled performance in a persistent way. Previous neurophysiological data support this conceptualization by showing that imagined and physically performed movements share partially overlapping neural substrates (Sirigu et al. 1996; Jeannerod 2001; Ehrsson et al. 2003; Papaxanthis et al. 2003) and networks (Sharma and Baron 2013), in addition to inducing similar brain plasticity as a result

Exp Brain Res

of training (Pascual-Leone et al. 1995; Jackson et al. 2003; Page et al. 2009; Zhang et al. 2011; Allami et al. 2014; Liu et al. 2014). Beyond the positive effect of pure imagery training on motor learning, we found that physical practice following motor imagery training led to higher performance in movement time and straightness in comparison with pure physical practice. Even though the imagery training group initiated the physical practice at a higher level of performance regarding the control group, their performance continued increasing following motor imagery training with further physical trials, maintaining the advantage in performance regarding the control group. This result is convergent with the descriptive trend toward better results for both peak height and number of sub-movements of the imagery training groups following physical practice. These findings are consistent with previous results showing that motor imagery training augments the gains achieved by ensuing physical practice (Allami et al. 2008, 2014). From the present and previous results, then, it is plausible that imagery training not only induces higher performance by itself but also leads to higher performance improvement in subsequent physical trials. A possible explanation for this secondary effect is that motor imagery training increases the excitability of different cerebral areas associated with movement planning and control (Pascual-Leone et al. 1995; Jackson et al. 2003; Zhang et al. 2011; Allami et al. 2014), which might enlarge the potential of learning from physical trials in the ensuing period. Enlargement of motor learning effects from physical practice by means of previous motor imagery training may underlie the superior results of rehabilitation protocols combining imagery and physical practice in comparison with protocols based on pure physical practice (Liu et al. 2004, 2014; Page et al. 2005, 2009; Hwang et al. 2010; Cho et al. 2013). From these results, we provided support for Steenbergen et al.’s (2009) assumption that motor imagery training is a valid procedure for promoting motor rehabilitation of individuals with cerebral palsy. As final remarks, it should be noted that use of control groups, rather than a pretest, to assess the effects of pure motor imagery training on motor learning prevented contamination of that evaluation by prior physical experience during testing. On the other hand, lack of a pretest prevented a direct measurement of performance gains due to motor imagery training. Additionally, results presented here should be generalized to adolescents presenting mild hemiparesis. This recommendation is made from the perspective that our participants were not strongly affected by cerebral palsy, and this condition may have favored the positive effect of motor imagery training. Individuals who suffered more extensive brain damages, leading to moderate or strong hemiparesis, might have different

performance achievements from imagery training because of the more extensive damage to cerebral structures and associated movement disorders. Considering that our results correspond to the first evidence for the effect motor imagery training on motor learning in individuals with cerebral palsy, and that the effect sizes were small, further research in applied settings testing more complex motor tasks is required to confirm the effectiveness of this procedure as an intervention tool. Based on our finding that gains from physical practice were additive to the previous performance achievements from imagery training, we suggest that physical practice of functional motor skills be preceded by motor imagery training as a regular procedure in clinical practice to individuals suffering from mild cerebral palsy. Acknowledgments  This study was supported by the Foundation for Research Support of the State of São Paulo, Brazil (FAPESP, Grant Number 2011/09601-1), and Brazilian Council of Science and Technology (CNPq, Grant Number 302628/2013-4) provided to LAT.

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