Motor imagery difficulties in children with Cerebral Palsy: A specific or general deficit?

Research in Developmental Disabilities 57 (2016) 102–111

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Research in Developmental Disabilities

Motor imagery difficulties in children with Cerebral Palsy: A specific or general deficit? Jessica M. Lust a,∗ , Peter H. Wilson b , Bert Steenbergen a,b a b

Radboud University Nijmegen, Behavioural Science Institute, P.O. Box 9104, 6500 HE Nijmegen, The Netherlands Australian Catholic University, School of Psychology, Melbourne 3065, VIC, Australia

a r t i c l e

i n f o

Article history: Received 22 July 2015 Received in revised form 10 June 2016 Accepted 13 June 2016 Keywords: Cerebral Palsy Explicit motor imagery Implicit motor imagery Hand laterality judgment task Hand rotation Praxis imagery questionnaire

a b s t r a c t Aim: The aim of this study was to examine the specificity of motor imagery (MI) difficulties in children with CP. Method: Performance of 22 children with CP was compared to a gender and age matched control group. MI ability was measured with the Hand Laterality Judgment (HLJ) task, examining specifically the direction of rotation (DOR) effect, and the Praxis Imagery Questionnaire (PIQ). Results: In the back view condition of the HLJ task both groups used MI, as evidenced by longer response times for lateral compared with medial rotational angles. In the palm view condition children with CP did not show an effect of DOR, unlike controls. Error scores did not differ between groups. Both groups performed well on the PIQ, with no significant difference between them in response pattern. Conclusion and implication: The present study suggests that children with CP show deficits on tasks that trigger implicit use of MI, whereas explicit MI ability was relatively preserved, as assessed using the PIQ. These results suggest that employing more explicit methods of MI training may well be more suitable for children with CP in rehabilitation of motor function. © 2016 Elsevier Ltd. All rights reserved.

What this paper adds 1. This paper presents the first study to compare explicit and implicit MI ability in the same group of children with CP. 2. Deficits in MI that are specific to the implicit mode of control are highlighted in children with CP. 3. Results suggest that children with CP may benefit from rehabilitation techniques that utilize the explicit forms of MI. 1. Introduction Cerebral Palsy (CP) is the most common cause of childhood disability (Cans, 2000) with a prevalence of approximately 2/1000 live births (e.g. Blair & Watson, 2006; Johnson, 2002; Stanley, Blair, & Alberman, 2000). The underlying disorder of movement and posture is attributed to non-progressive disturbances in the development of the neuromotor system during the foetal or infant period (Rosenbaum et al., 2007). The impact of CP on activities of daily living is profound, with much debate still on the nature of the motor control and cognitive deficits that contribute to impaired function. In the present paper

∗ Corresponding author. E-mail address: [email protected] (J.M. Lust). http://dx.doi.org/10.1016/j.ridd.2016.06.010 0891-4222/© 2016 Elsevier Ltd. All rights reserved.

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we examined the issue of motor imagery (MI) in CP, reflecting the ability to represent movement parameters internally. To advance our knowledge of those aspects of MI that are impaired in children with CP, we used both a hand laterality judgment task enlisting implicit MI and a subjective MI questionnaire enlisting explicit MI. To address the movement problems of CP, children regularly participate in rehabilitative activities aimed at improving the execution of motor actions (Koman, Smith, & Shilt, 2004; Sakzewski, Ziviani, & Boyd, 2014). There is moderate to strong evidence for the effectiveness of several intensive physical therapy interventions in CP (reviewed in Anttila, Autti-Rämö, Suoranta, Mäkelä, & Malmivaara, 2008; Sakzewski et al., 2014). However, there is converging evidence that the motor deficits in these children are not related solely to problems in the (overt) motor execution of movement but may also derive from problems in cognitive processes that precede action, e.g., MI, a core aspect of motor simulation (Steenbergen, JongbloedPereboom, Spruijt, & Gordon, 2013). MI is regarded as an internal (multimodal) representation of a prospective action, performed under varying levels of conscious control (Vogt, Di Rienzo, Collet, Collins, & Guillot, 2013). MI is experienced as an embodied phenomenon, with visuospatial, somatic, timing and force parameters that are normally associated with overt movement also preserved (Vogt et al., 2013). MI can be generated purely in an imaginary context or with reference to the immediate environment; as such, it serves both motor planning and decision making over various timescales. In neurocomputational terms, MI is thought to be a function of internal modelling (e.g. Jeannerod & Decety, 1995; Steenbergen, Crajé, Nilsen, & Gordon, 2009; Steenbergen & Gordon, 2006; Van Elk et al., 2010). Internal forward models of movement are necessary for skilled actions. This is particularly true of those movements performed under tight temporal and spatial constraints as neural transmission times through sensory feedback loops are inherently slow (Flanagan, Vetter, Johansson, & Wolpert, 2003; Kawato, 1999). Forward models are a core part of the motor system, generated as a corollary of motor commands emanating from premotor regions. More precisely, efference copy signals are used as an input for (forward) model estimation. Forward models are processed along fast visuomotor channels and act as a template against which real-time feedback can be compared and limb adjustments can be made should unexpected perturbations occur, whether they be visual, kinaesthetic or other (Flanagan et al., 2003; Kawato, 1999). Structures underpinning this intricate system of control have been confirmed in neuroimaging, neurophysiological and neuropsychological investigations, and involve reciprocal connections between prefrontal, posterior parietal and cerebellar cortices (Shadmehr & Krakauer, 2008). A deficit of internal modelling may interfere with the ability to adequately prepare and control a movement and is hypothesized to underlie motor execution problems in children with other neurodevelopmental disorders like Developmental Coordination Disorder (DCD; see the internal modelling deficit (IMD) hypothesis, Adams, Lust, Wilson, & Steenbergen, 2014; Wilson & Butson, 2007; Wilson, Ruddock, Smits-Engelsman, Polatajko, & Blank, 2013). Like DCD, evidence for an internal modelling deficit in CP comes from studies of MI, specifically those on anticipatory planning and mental rotation (reviewed in Steenbergen & Gordon, 2006; Steenbergen et al., 2013). MI is an embodied process that involves the ability to mentally simulate movements from a first person perspective (Jeannerod, 1994, 1995). MI is both pervasive and important, used when watching somebody else’s actions with the intention to imitate, mentally rehearsing a to-be-performed skill, anticipating the effect of a motor action or preparing a movement (Jeannerod, 1995; Toussaint, Tahej, Thibaut, Possamai, & Badets, 2013; Fuelscher, Williams, Enitcott, & Hyde, 2015; Noten, Wilson, Ruddock, & Steenbergen, 2014). Studies on anticipatory planning in CP (Steenbergen & Gordon, 2006; Steenbergen et al., 2013) have been particularly instructive. Prospective judgment tasks, for example, show that when executing a grasp-to-turn movement, children with CP do not always adjust their initial grip type prospectively in order to prevent an uncomfortable posture at the end of the movement, i.e. these children do not generally show the end-state comfort effect as described by Rosenbaum and Jorgenson (Rosenbaum & Jorgensen, 1992). Prospective judgment tasks are a strong marker of forward modelling – they enlist a process of action simulation before response initiation (Adams et al., 2014). Impaired MI in CP is also shown in mental rotation tasks (Crajé et al., 2010). In these tasks, the ability to accurately represent movement internally is inferred by the ability to imagine movements or postures that conform to the biomechanical constraints of an action performed overtly (Jeannerod, 1995). An often used paradigm to measure (implicit) MI ability is Parson’s Hand Laterality Judgment task (HLJ task, e.g. Parsons, 2001). Here subjects are asked to judge the laterality of pictures of rotated hands displayed on a computer screen; judgments can be made without explicit reference to the use of imagery. For typically developing children differences in response time are observed between stimuli that require biomechanically efficient/ easy (medial) hand rotations and those requiring more awkward (lateral) rotations (e.g. De Lange, Hagoort, & Toni, 2005; Parsons & Fox, 1998; Parsons, 1987, 1994; Ter Horst, Van Lier, & Steenbergen, 2010). Absence of this difference (or direction of rotation, i.e. DOR) effect in CP indicates that participants do not use an MI strategy to solve the hand laterality task (Steenbergen et al., 2013; Williams et al., 2011). Whereas there is good evidence of impaired MI in CP, we know little about the specificity of this deficit—i.e., is it a general deficit or is it confined to actions generated implicitly by limb-related stimuli? This is an important question as MI training has been reported as a tool for rehabilitation of movement in adults (Munzert, Lorey, & Zentgraf, 2009; Schuster et al., 2011) and for children with motor execution problems (Steenbergen et al., 2009; Wilson et al., 2013; Wilson, Thomas, & Maruff, 2002). Knowledge of those aspects of MI most affected in CP could inform both theoretical models of (atypical) motor control and how imagery training might be optimized in this population. In the study presented here we addressed three questions about the nature and specificity of the imagery deficit in CP: First, we examined the DOR effect to test for difficulties in the implicit use of MI in the present sample of children with CP. Second, we examined whether implicit MI difficulties in CP extend to explicit forms of MI. The latter requires that

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Table 1 Participant information of the children with Cerebral Palsy (CP), per CP type. Age (years)

GMFCS

MACS

Box and Blocks

CP type

n (girls, boys)

M(SD), min-max

Classification (n)

Classification (n)

Preferred hand (M (SD))

Nonpreferred hand (M (SD))

Unilateral left spastic hemiplegia

10 (6,4)

6.3(1.1), 5–8 6.8(1.5), 5–9 7.0(1.4), 6–9

I (7), II (3)

I (3), II (7)

37.5 (7.8)

18.4 (6.5)

I (7), II (1)

I (2), II (6)

40.6 (8.4)

18.8 (7.3)

Unilateral right spastic hemiplegia 8 (3,5) Spastic diplegia

4 (2,2)

I (1), III (1), IV (2) I (1), II (1), III (1), IV (1) 32.8 (9.7)

23.5 (11.1)

Note: GMFCS = Gross Motor Function Classification System, MACS = Manual Ability Classification System.

the child enlists conscious control when performing MI, as when, for example, someone is asked “explicitly” to imagine a particular grasping movement (like picking up a hammer) and then report on the relative position of the digits in relation to the object. Third, if deficits in explicit MI exist, we were interested in whether these were generalized across different aspects of motor image representation—specific end-state postures, dynamic kinaesthetic flow, or object-related sensation, for instance (Ochipa et al., 1997) – or were specific. To answer these questions we administered the HLJ-task (e.g. Ter Horst et al., 2010) and the Praxis Imagery Questionnaire (PIQ, Ochipa et al., 1997; Wilson, Maruff, Ives, & Currie, 2001). In line with earlier work (reviewed also by Steenbergen et al., 2013), we predicted that children with CP would have difficulties adjusting their performance as a function of the differing biomechanical constraints depicted by stimuli in the HLJ task. As used successfully in the study of apraxia (Ochipa et al., 1997) and DCD (Wilson et al., 2001), we used the PIQ to evaluate different facets of imagery ability in the performance of daily life actions. General (object) imagery and MI as well as different levels of kinaesthetic detail in MI are assessed and dissected by four subtests (McAvinue & Robertson, 2008; Ochipa et al., 1997). The “object” subtest involves imagining the object used as part of the action; “kinaesthetic” subtest addresses joint movement; “position” assesses imagery of the spatial position of the hand in relation to either the object or other body parts, while “action” involves imagining the general motion of the limb used to complete an action. These subtests thus enable measurement of the ability to retrieve different visual, tactile and kinaesthetic features of the internal representation of the movements (Ochipa et al., 1997), a separation supported in recent psychometric evaluations (Malouin et al., 2007). Given the profound motor difficulties in CP, we predicted a generalized impairment of MI on the PIQ. 2. Methods 2.1. Participants Initially 25 children (14 girls) with CP aged 5–9 years (M = 6.6, SD = 1.3) were recruited via the Dutch society of parents of physically disabled children (“BOSK”) and the Sint MaartensKliniek Nijmegen. Inclusion criteria were the ability to handle the response device used in the task, IQ > 70 as indicated by the brief version of the Wechsler Nonverbal scale of ability (WNV, Wechsler & Naglieri, 2006) or attendance of a main stream primary school. IQ data was available for all children involved in the study and based on the short version of the Wechsler Nonverbal scale of ability the mean IQ was 94 (SD = 18). Asymmetry in hand function was measured using the Box and Block test (Jongbloed-Pereboom, Nijhuis-van der Sanden, & Steenbergen, 2013; Mathiowetz, Volland, Kashman, & Weber, 1985). Motor skill in everyday functioning was measured by the Gross Motor Function Classification System (GMFCS, Gorter, Van Tol, Van Schie, & Ketelaar, 2009) score and the Manual Ability Classification System (MACS, Eliasson et al., 2006) score. Three children were excluded: One boy with severe attention problems, and two girls, one who could not follow task instructions and one with severe visual problems. Participant information on the remaining 22 children with CP is shown in Table 1. The CP group was compared to a gender- and age-matched (5–9 years old, M = 6.6, SD = 1.2) control group from mainstream Dutch primary schools. Controls had no reported motor problems, confirmed by their performance on the Box and Block test that was within the normal range (Jongbloed-Pereboom et al., 2013). The study was approved by the Ethics Committee Faculty of Social Sciences (ECSS; ECG2012-2402-018) at Radboud University Nijmegen and the Central Committee on Research Involving Human Subjects (MREC; NL 40355.091.12). Informed consent was obtained from the children’s parent/guardian. 2.2. Measures 2.2.1. Hand laterality judgment task Single hand stimuli (measuring 10 by 4 cm) were presented on the centre of the screen of a laptop using Presentation software (Neurobehavioral Systems, Inc., Version 16.5 Build 08.15.13). Children in the control group were asked to indicate whether the presented hand was a left or a right hand by pressing the corresponding large custom made button (10 cm in diameter) with their preferred hand. For children with CP this button was not used as we anticipated that they may be at a disadvantage using this button that necessitates a ‘push-movement’. With this set-up we obviate the possibility that

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Fig. 1. Response device with two rectangular touch pads one central circular touch pad.

differences in motor function of the less-affected hand in children with CP would have confounded the results. Children with CP used a custom made response device, measuring 28 × 30 cm with three brass touch pads: one central (circle of 4 cm diameter) and two peripheral (rectangular, measuring 7 × 10 cm, spaced 7.5 cm apart) (Fig. 1). The next trial did not start until the child indicated he/she was ready by touching the central touch pad. Responses were made solely with the less-affected hand. The children were asked to indicate whether the presented hand was a left or a right hand as quickly and as accurately as possible by pressing the corresponding (left or right) rectangular touch pad. The stimulus remained visible until a response was registered. Each trial started with the presentation of a fixation cross presented centrally on the laptop screen 1 s after touching the central pad. The fixation cross was replaced by a hand stimulus after a random interval of 1000–1500 ms. Right and left hands were presented at rotation angles of 0◦ (fingers pointing upward), 60◦ , 120◦ , 180◦ , 240◦ , and 300◦ with each angle occurring three times per hand. Two task conditions were administered, a back view condition and a palm view condition. Each condition consisted of 36 experimental trials presented in random order, preceded by six practice trials. 2.2.2. Praxis imagery questionnaire We used ten motor actions from the modified Florida Praxis Imagery Questionnaire reported by Wilson et al. (2001, based on Ochipa et al., 1997). Prior to testing we verified that each child was familiar with the terms fingers, thump, index finger, little finger, wrist, elbow, shoulder, throat/neck and palm of the hand. During the PIQ the child sat facing the researcher who ensured that he/she did not physically perform any of the motor actions. For each item, the child was asked to imagine him/herself performing the action. The child was then asked to answer one question from each of the four subtests (kinaesthetic: which joint moves more; position: spatial position of hands or body parts in relation to either the object or other body parts; action: direction of limb motion; object: imagining the object in use). Each response was later scored for correctness (0 or 1). Hence, the maximum score for each subtest was 10, giving a total score of 40 for the questionnaire. An answer was regarded as invalid if the child physically performed the movement before giving an answer or if the child failed to answer. Only five item responses (0.3%) were excluded from the analyses. Total scores were converted to a proportion of correct responses. 2.3. Procedure Each child was seen on a one-on-one basis. All children in the control group were tested at their school. Thirteen children with CP were tested in their own home, four at a university test room, one at the Sint MaartensKliniek and four at in their school. At the start of testing, children were seated at a table and chair of appropriate height. The tasks were embedded in a larger test battery addressing the cognitive motor development of children. The children were allowed to have breaks whenever needed.

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Fig. 2. Mean response times (ms) per angle and direction of rotation (DOR) in the back view condition of the hand rotation task. Error bars represent the 95% confidence intervals.

2.4. Data analysis For the HLJ task, only those children with 50% or more correct responses within each condition were included in the analysis. This excluded data from three children with CP in the back view condition and data from two in the palm view condition. In addition, data from three children were excluded in one or two condition due to an inability to complete the task without hand movements. The remaining children with CP (17 in each condition) were matched (age and sex) to control children. Anticipatory responses (<250 ms) and RTs showing an abnormal delay (SD > 3.0 or >15 s) were removed prior to analysis. In the CP group, 3.2% of trials in the back view and 0.04% in the palm view condition were removed. In the controls, 1.5% of trials in the back view and 1.7% in the palm view condition were removed. To infer the use of MI, response time and accuracy for laterally- and medially-rotated stimuli were contrasted (Parsons, 1987, 1994; Ter Horst et al., 2010). Laterally rotated stimuli consisted of 60◦ and 120◦ rotated right hand stimuli and 300◦ and 240◦ rotated left hand stimuli. Medially rotated stimuli consisted of 300◦ and 240◦ rotated right hand stimuli and 60◦ and 120◦ rotated left hand stimuli. The within-subject effect of direction of rotation (DOR: lateral/medial) on RT was analyzed in separate repeated measures ANOVAs for back view and palm view stimuli. Measures of effect size were also reported to temper reliance on significance tests and the probability of Type I and II errors. The number of errors were analyzed with a Mann Whitney U test. Scores on the PIQ were compared between groups using a Mann-Whitney U test. Within groups differences in performance between the four subscales were analyzed using Friedman’s 2-way ANOVA by ranks. All analyses were performed using SPSS version 19. The significance level was set at 0.05. 3. Results 3.1. Hand rotation task: back view A mixed 2 (group: CP and Control) × 2 (angle: 60◦ and 120◦ ) × 2 (DOR: lateral and medial) ANOVA on response time showed a main effect of group (F(1,32) = 5.73, p = 0.02, ␩p 2 = 0.15), but no interactions (p > 0.05). On average children with CP show longer response times (M = 3657, SE = 292 ms) than controls (M = 2668, SE = 292 ms). There were significant main effects of angle (F(1,32) = 8.32, p < 0.007, ␩p 2 = 0.21) and DOR (F(1,32) = 19.83, p < 0.0005, ␩p 2 = 0.38). As presented in Fig. 2, response time increased with rotation angle and were increased for laterally compared to medially rotated hand stimuli. There was no difference between groups on the total number of errors (Median CP group = 4.0, Median control group = 2.0, U = 99.50, p = 0.12, r = −0.27). 3.2. Hand rotation task: palm view A mixed 2 (group: CP and Control) × 2 (angle: 60◦ and 120◦ ) × 2 (DOR: lateral and medial) ANOVA on response time showed a main effect of group (F(1,32) = 5.64, p = 0.02, ␩p 2 = 0.15). On average children with CP showed longer response times (M = 3953, SE 234 ms) than controls (M = 3166, SE = 234 ms). Importantly, there was a significant DOR*group interaction effect (F(1,32) = 6.49, p = 0.02, ␩p 2 = 0.17). An analysis of simple effects within each group showed a significant effect of DOR

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Fig. 3. Mean response times (ms) per angle and direction of rotation (DOR) in the palm view condition of the hand rotation task in control group (left graph) and in the CP group (right graph). Error bars represent the 95% confidence intervals.

for controls (F(1,16) = 10.19, p = 0.006, ␩p 2 = 0.39), not CP (F(1,16) = 0.05, p = 0.82, ␩p 2 = 0.003) (Fig. 3). No other significant effects were found (p > 0.05). There was no difference between groups in total number of errors (Median CP group = 5.0, Median control group = 5.0, U = 143.00, p = 0.96, r = −0.01). 3.3. Praxis imagery questionnaire (PIQ) No significant group differences on PIQ scores were found (Table 2) were found. There was a trend for controls to perform better on the Object subscale than children with CP, but the effect size was very small (Table 2). Median scores on PIQ subscales are shown in Fig. 4. Friedman’s 2-way ANOVA showed a difference between subscales for the control group only (p < 0.0005). Fig. 4 shows that this is attributable to better performance by controls on the Object subscale, while no such trend was evident for the CP group. 4. Discussion In the study presented here, we examined the specificity of the putative MI deficit (e.g. Steenbergen et al., 2013) in a group of children with CP and matched controls. In line with earlier studies using a HLJ task paradigm (reviewed in Steenbergen et al., 2013), the present results suggest that children with CP had selective deficits in using MI in solving the hand laterality judgment task. In the back view condition, the performance of both groups suggested use of MI by longer response times for lateral compared with medial rotational angles (DOR effect). However, children with CP were significantly slower than controls, consistent with earlier studies (e.g. Williams et al., 2011). For the palm view condition, results were also consistent with earlier studies in adults with CP (e.g. Crajé et al., 2010): our response time data revealed no DOR effect in children with CP, unlike controls. No group difference was shown on laterality judgment errors suggesting no issues with task engagement per se. The absence of the DOR effect in the palm view condition indicates that children with CP did not use a MI strategy to Table 2 Mann-Whitney U test results.

Kinaesthetic Position Action Object Total *

Group

n

Mean Rank

U

Z

p

Effect Size*

Controls CP Controls CP Controls CP Controls CP Controls CP

22 22 22 22 22 22 22 22 22 22

19.82 25.18 23.00 22.00 23.32 21.68 26.16 18.84 23.82 21.18

183.0

−1.41

0.159

−0.21

231.0

−0.26

0.792

−0.04

224.0

−0.43

0.667

−0.06

161.5

−1.93

0.053

−0.29

213.0

−0.68

0.495

−0.10

√ Calculated as Z/ N (Fritz, Morris, & Richler, 2012; p. 12).

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Fig. 4. Median proportion scores (±95% CI) on the Praxis Imagery Questionnaire (PIQ, subscales and total) for the CP and control group.

solve the task, a hypothesis also supported by a recent neurophysiological study (Ter Horst, van Lier, & Steenbergen, 2013; Zapparoli et al., 2014). Generally speaking, back view stimuli are recognised more quickly than palm view (e.g. Funk, Brugger, & Wilkening, 2005). This differential pattern of results may reflect how commonly back versus palm views are observed in the course of natural action. Our first-person viewpoint encounters back view images more commonly than palm view (as evidenced in graphomotor activities, relaxed sitting, most object grasp and placement actions, and so on); and, with repeated exposure this is likely to build a more refined representation of the effector, in this posture. For children with CP, the issue in motor representation (and action simulation) is expressed for hand postures that are less commonly experienced. In addition, the DOR effect reflects the biomechanical constraints involved in moving body parts (or simulated their movement) into an awkward posture. The simulation is synonymous with MI but the strength of the effect may not necessarily correlate with imagery ability per se. Indeed, some studies suggest that the effect may decline after the childhood period (see Funk et al., 2005). Clearly, the exact functional significance of the DOR and its absence in children with CP warrants further study. Although the order in which the back and the palm view condition were presented was not counterbalanced across participants, and differences between the back and the palm view condition have to be interpreted cautiously, the present results confirm findings that children with CP have difficulties using implicit MI in the HLJ task. Further EEG or functional neuroimaging data are required to isolate the neural mechanisms that support (or do not support) the DOR effect in children with CP, and how this changes with age (see for example Jongsma et al., 2015). To study the specificity of the MI deficit we also administered an adapted version of the PIQ consisting of ten different motor actions from daily life that had to be imagined. Contrary to our hypothesis, both groups performed equally well on this task, with no appreciable difference in response pattern across subscales. This result parallels that seen in DCD by Wilson et al. (2001). Whereas children with DCD showed a clear MI deficit, as measured by a mental chronometry task, their performance on the PIQ was very similar to that of controls (but differed only marginally on the kinaesthetic subscale, with a small effect size and an average of 1 less correct answer out of 12 compared with controls). Studies in children with CP have shown repeatedly a reduced level of MI ability which has been interpreted as a for deficit in the forward modelling of movements (e.g. Steenbergen et al., 2013). The children in our group of children with CP showed an impaired ability to resolve biomechanical constraints while performing the HLJ task, but this MI deficit did not generalize to the ability to generate and reflect on motor images of daily motor skills. The distinction may reflect the degree to which each task involves conscious use of motor representations (Jeannerod & Frak, 1999). While the HLJ task triggers implicit use of MI (e.g. Parsons et al., 1995), the PIQ requires that children generate and perform an imagined motor action in response to verbal instructions (e.g. McAvinue & Robertson, 2008). While we would expect this task to demand a degree of executive function (EF) and memory, children with CP seemed able to consciously generate and manipulate motor images as accurately as controls. What we do not know, however, is whether the process of (explicit) image generation is more protracted in CP; this is an issue for future investigation. Clearly, while EF deficits are evident in CP (e.g. Bodimeade, Whittingham, Lloyd, & Boyd, 2013; Weierink, Vermeulen, & Boyd, 2013), this does not appear to be a limiting factor in the explicit use of MI on the PIQ. It is important to note that implicit and explicit MI tasks have been employed to test the integrity of the body schema (reviewed in (Vignemont de, 2010)). While our study originated from the theoretical perspective of the internal model deficit

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in order to understand MI in children with CP, a recent systematic review on the impact of several forms of acquired brain damage on MI performance (Di Rienzo, Collet, Hoyek, & Guillot, 2014) showed that disturbances of body schema primarily affect implicit MI. Interestingly, the pattern of MI deficits we observed may be interpreted as a problem of body schema as opposed to a forward modelling impairment (Di Rienzo et al., 2014). Our study was, however, not set up to disentangle body schema and specific internal forward modelling deficits. Moreover, comparison between brain damage acquired at a later age and congenital brain damage is fraught given the inherent plasticity of the nervous system. In a recent study, Iosa et al. (2014) specifically focussed on disentangling body schema deficits from internal forward modelling deficits in children with CP via a comparison of imagery performance with and without vision. It was argued that without the support of vision, internal modelling relied more on the representation of body schema (Iosa et al., 2014). It was found that MI performance was better when vision was occluded, supporting the hypothesis that the process of internal forward modelling is more impaired in CP than the body schema. As utilizing internal models of movement is important when adequately preparing and controlling a movement, our finding has some important implications for the use of MI in rehabilitation. First, as children with CP do not show a reduced ability to mentally represent daily life motor actions (accurately) when explicitly instructed to do so, MI can be used when training such actions. Second, the ability to assess the mental representation of daily actions allows the therapist to detect and address representational errors during training. Third, the findings suggest that children with CP do not automatically enlist MI, even when cued appropriately by the stimulus environment. Explicitly addressing and training the use of this ability may well confer advantages when required to use MI automatically in real life situations − e.g. crossing the street (see also Te Velde, Van der Kamp, Becher, Van Bennekom, & Savelsbergh, 2005) or judging whether stove top workspace affords safe reaching for a saucepan. While the PIQ was shown to have good discriminant validity in adult apraxia (Ochipa et al., 1997) and DCD (Wilson et al., 2001), its broader psychometric properties are not yet known (McAvinue & Robertson, 2008). Also evaluation of MI was subjective. Notwithstanding these limitations, our study points to the potential use of the PIQ as a screening tool for children in movement rehabilitation. Test items involve simple and varied movements that are engaging and suitable for young children. Moreover, responses can be scored clearly (correct or incorrect) unlike the Kinesthetic and Visual Imagery Questionnaire (KVIQ, Malouin et al., 2007). Taken together, we recommend further development of this questionnaire as a useful assessment tool for individual differences in explicit MI ability. In summary, the present study suggests that children with CP show deficits in tasks that trigger implicit use of MI. However, explicit MI ability seems comparable to that of children without CP. As the use of internal models of movement is necessary for skilled motor behaviour (Flanagan et al., 2003; Kawato, 1999), the present study suggests that employing explicit MI as a training tool in rehabilitation supports the development of skilled movement. Acknowledgements We gratefully acknowledge the participating children and their parents. 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