Research in Developmental Disabilities 37 (2015) 95–101
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Research in Developmental Disabilities
Motor imagery for walking: A comparison between cerebral palsy adolescents with hemiplegia and diplegia Miche`le Molina a,*, Cyril Kudlinski a, Jessica Guilbert a, Steffie Spruijt b, Bert Steenbergen b,c, Franc¸ois Jouen d a
Laboratoire Psychologie des Actions Langagie`res et Motrices, Universite´ de Caen, France Radboud University Nijmegen, Behavioural Science Institute, The Netherlands c Australian Catholic University, School of Psychology, Melbourne, Australia d Laboratoire Cognitions Humaine et Artificielle, Ecole Pratique des Hautes Etudes, France b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 October 2014 Accepted 29 October 2014 Available online
The goal of the study was to investigate whether motor imagery (MI) could be observed in cerebral palsy (CP) participants presenting a bilateral affected body side (diplegia) as it has been previously revealed in participants presenting a unilateral body affected sided (hemiplegia). MI capacity for walking was investigated in CP adolescents diagnosed with hemiplegia (n = 10) or diplegia (n = 10) and in adolescents with typical motor development (n = 10). Participants were explicitly asked to imagine walking before and after actually walking toward a target located at 4 m and 8 m. Movement durations for executed and imagined trials were recorded. ANOVA and Pearson’s correlation analyses revealed the existence of time invariance between executed and imagined movement durations for the control group and both groups of CP participants. However, results revealed that MI capacity in CP participants was observed for the short distance (4 m) but not for the long distance (8 m). Moreover, even for short distance, CP participants performed worse than typical adolescents. These results are discussed inline of recent researches suggesting that MI in CP participants may not depend on the side of the lesion. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Motor imagery Mental chronometry CP Walking
1. Introduction Motor disorders in individuals with cerebral palsy (CP) are kwown to induce deficit in motor anticipatory planning (Craje´ et al., 2010; Mutsaarts, Steenbergen, & Meulenbroek, 2004; Mutsaarts, Steenbergen, & Bekkering, 2005, 2006) which, in turn, has been be related to impaired ability to use motor imagery (i.e. Mutsaarts et al., 2006). Motor imagery (MI) is the mental simulation of a motor act, without any overt motor execution and thus refers to the capacity to produce kinesthetic representations of motor actions (Decety, Jeannerod, & Prablanc, 1989). MI would be used to predict the proprioceptive consequences of an action and then contribute to movement planning (Grush, 2004; Papaxanthis, Pozzo, Skoura, & Schieppati, 2002).
* Corresponding author at: Laboratoire Psychologie des Actions Langagie`res et Motrices, Universite´ de Caen, esplanade de la paix, 14032 Cedex 5, France. Tel.: +33 23128566263. E-mail address: [email protected] (M. Molina). http://dx.doi.org/10.1016/j.ridd.2014.10.053 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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Various studies conducted in adult participants without brain damaged (Schluter, Krams, Rushworth, & Passingham, 2001) and with left hemispheric stroke (Rushworth, Nixon, Wade, Renowden, & Passingham, 1998) have corroborated a left cerebral dominance for movement planning. In line with these studies, MI capacity in CP participants has been mainly investigated in hemiplegic cerebral palsy (HCP) with the idea that right HCP with left brain damage would be impaired in MI (Mutsaarts, Steenbergen, & Bekkering, 2007). Most of these studies have used a hand laterality task that addresses implicit MI: a judgment on the laterality of a displayed hand stimulus has to be made as quickly as possible. In this kind of tasks, participants are not explicitly instructed to imagine the rotation of their own hand to judge the laterality of the hand stimulus presented. MI is deduced from the recorded reaction times profiles: reaction times are expected to vary according to the rotation angle and to biomechanical constraints of the hand stimuli (Horst, Van Lier, & Steenbergen, 2010). Studies have led to non-converging conclusions concerning the capacity of individuals with hemiplegia on the left or the right body side to perform MI implicit tasks. For instance, Mustaarts et al. (2007) reported a linear increase in reaction time as a function of angle rotation of the hand in left hemiparetic individuals (right brain-damaged) but not in right hemiparetic individuals (left brain-damaged). In contrast, Steenbergen, van Nimwegen, and Craje´ (2007) failed to find differences in reaction times in individuals with hemiplegia on the left body side or on the right body side. Increasing biomechanical constraints modify reaction time in CP children with both left- and right-side affected (Williams, Anderson, et al., 2011; Williams, Reid, Reddihough, & Anderson, 2011) but yet another study indicated that reaction time was not affected in CP adolescents with right-sided hemiplegia (Craje´ et al., 2010). Studies using explicit MI tasks have led to more convergent results. Explicit MI tasks are supposed to increase body awareness, and consequently help participants to use MI (Spruijt et al., 2013). These tasks are based on the mental chronometry paradigm: participants are asked to move and to imagine moving themselves (or a body part), from a first person perspective, toward targets located at different distances. The durations of both, the actual and imagined movements are then compared. When participants use MI, they preserve the temporal unfolding of displacement when asked to imagine acting: a temporal invariance between executed and imagined movement durations is consequently observed. The results obtained with typical participants commonly revealed the existence of a temporal invariance between overt and covert movement whatever the distance to be performed. The mental chronometry paradigm has also been used in a fingerpointing task to targets varying in size with typically developing children (Caeyenberghs, Wilson, van Roon, Swinnen, & Smits-Engelsman, 2009) and in children with hemiplegic cerebral palsy (Williams, Anderson, Reid, & Reddihough, 2012). These studies have revealed that the duration of performed and imagined movements is congruent with Fitts’ law (Fitts, 1954): The time required to rapidly move or imagine moving to a target area is a function of the distance to the target and the size of the target both, in typically developing children (Caeyenberghs et al., 2009) and in right-sided HCP children, but not in HCP children with left-sided hemiplegia (Williams et al., 2012). According to Williams et al. (2012), this last result which is in sharp contrast with implicit hand task studies reporting compromised MI ability in right-sided but not in left-sided hemiplegic participants (Mustaarts et al., 2007), reveals that the side of hemiplegia alone is not an indicator of MI performance. This important conclusion has received some additional support from a recent study conducted by Spruijt et al. (2013), in which walking was used as the experimental motor task. Left and right hemiplegic adolescents were explicitly required to walk or to imagine walking on paths varying in length and width that defines various indexes of difficulty according to Fitts’ law (1954). Results revealed that task difficulty had similar effects on movement duration for both actual walking and imagined walking revealing MI capacity in CP adolescents with left and right hemiplegia. These results are thus inline with Williams et al. (2012), who stated that MI performance in the HCP may not be related to the affected side of hemiplegia. A direct implication of the conclusion of Williams et al. (2012) is that MI in a walking task should be also observed in other clinical subtypes of cerebral palsy. The main goal of the present research was to evaluate MI in a walking task in two clinical subtypes of CP: diplegia and hemiplegia. Contrary to hemiplegia, which most frequently involves a unilateral lesion, diplegia involves in most cases bilateral injury (Okumura, Kato, Kuno, Hayakawa, & Watanabe, 1997). CP subtypes differ according to the topography of the motor impairment with both lower limbs more affected than upper limbs in participants with diplegia and one side of the body affected in HCP participants (Dabney, Lipton, & Miller, 1997). We hypothesized that, inline with the conclusion of Williams et al. (2012), according to which MI is not related to the affected body side in CP children, MI would be observed as well in CP adolescents with diplegia as with hemiplegia. A second goal was to assess the general impairment in MI for motor task in both groups of CP participants. In order to reach this goal, MI performance of each group of participants was compared to MI performance of adolescents with a typical motor development.
2. Methods 2.1. Participants The CP participants were recruited at two schools for special education in France. Participants contributed on a voluntary basis. In accordance with the Helsinki Declaration and approved by the Regional Ethical Committee, participants took part in the study after their own written consent was obtained. Consent was also obtained from parents and/or caregivers. Inclusion criteria described participants with CP, related to identified-brain damage that occurred during the first six months of life. Information about the diagnoses and additional disabilities was obtained from participant’s medical records.
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Thirty participants were included. The age of the participants ranged from 12 to 19 years. Ten participants (mean age: 15.9 2.02) were affected by right spastic hemiplegia (HCP). Ten participants (mean age: 15.5 2.55) were affected by spastic diplegia (DCP). Participants with hemiplegia and diplegia were all able to independently walk over a distance of 8 m, without the use of an assistive mobility device. At the time of testing, all participants received physical therapy aimed at pain relief and preventing contractures. The adapted French version of the Gross Motor Function Measure (MFM) was used to evaluate the motor capacity of the participants with CP (Be´rard, Girardot, Hodgkinson, & Payan, 2006). HCP participants had MFM scores greater than 85%, and DCP participants had MFM scores ranging from 75% to 85%. Ten participants from mainstream high school (mean age: 16.3 2.01) were also recruited as control group: they all were free of any physical or neurological condition affecting motor development. 2.2. Materials and procedures The walking task was based on the classical mental chronometry paradigm initially designed by Decety et al. (1989) with typical participants. In this well-known experimental context, MI is investigated by varying the distance participants will have to walk or to imagine walking. Experiments took place in the physical therapy room. The executed and imagined conditions started by asking participants to stand behind a 1 m line representing the starting point. At the level of this starting line a visual red mark was presented. A second visual red mark was presented at a distance of 4 m or 8 m from the starting line. This second visual mark represented the arrival point. Participants were required to walk straight from the starting point to the arrival point. In the executed movement condition, the experimenter instructed the participant as follows: ‘‘You are going to walk at a comfortable pace from here (the experimenter pointed to the starting point) to the next visual target that you see over there (the experimenter pointed to the arrival point).’’ No time limitation was provided to the participant. Once the experimenter made sure that the participant understood the task, the experiment began. In the imagined motion condition, participants received the following instruction: ‘‘You are going to imagine walking from this point (the experimenter pointed to the starting point) to this one (the experimenter pointed to the arrival point). You must imagine walking at a comfortable speed. However, you will not actually walk. You just have to think of walking toward the visual target. Once you start walking, tell me, ‘‘go’’. Once you stop moving, tell me, ‘‘stop’’. Participants performed the imagined trials with the eyes open. An electronic stopwatch with milliseconds precision recorded durations of performed and imagined movements. During the executed and imagined movements, the experimenter started the stopwatch when the participant indicated the start of the movement (whether in real or imagined movement) and stopped it when the participant indicated the stop of the movement (real or imagined). All participants were instructed to walk or to imagine walking at the same speed during the trials in the executed and the imagined conditions. For the imagined conditions, all participants remained at the starting point without walking to the arrival point. In each group, half of the participants performed first the 4 m distance and then the 8 m distance condition. Reverse order was used for the other participants. Participants were randomly assigned to one of two distance-order conditions (4 m and 8 m vs. 8 m and 4 m). These distance-order conditions were aimed at disentangling motor imagery capacity from motor memory capacity (Papaxanthis et al., 2002). If motor imagery capacity is present, whatever the distance to be performed (4 m or 8 m), the time correspondence between actual and imagined displacement should be observed independently of the order of presentation of the imagined trial (after or before the executed trial). On the contrary, if time invariance is exclusively observed when imagined movement is measured after actual movement, the effect will be related to motor memory (Papaxanthis et al., 2002). For each distance, each participant successively performed three tasks: imagined before executed (IBE), executed (EXE) and imagined after executed (IAE). Each block of IBE, EXE and IAE tasks was thus repeated for each distance whatever the distance-order condition. 2.3. Data analyses First for each participant, individual movement durations for executed and imagined tasks were analyzed in order to detect outliers (movement duration > group mean 3SD). No data were identified as outliers and all measures were kept for analyses. Second, the normality (Shapiro–Wilk test) and the equivalence of variance (Levene test) of the distributions of movement durations were tested in order to control that parametric analysis could be used to evaluate motor imagery capacity of the participants. Since the tests confirmed the Gaussian nature of data, a two-way ANOVA was performed to control that for each group of participants (typical, hemiplegia, diplegia) actual walking time depended on the distance to be performed (4 m vs. 8 m). Then, tasks were analyzed with a 3 2 2 3 mixed-model ANOVA with Group (control, hemiplegia, diplegia) and distanceorder (4–8 m vs. 8–4 m) as between subjects factors and with distance (4 m vs. 8 m) and task (imagined before executed, executed, imagined after executed) as a within subjects factor. This analysis was aimed at controlling that MI did not depend on the order of presentation of the imagined trial (after or before the executed trial). Since no distance-order effect was observed, a second 3 2 3 mixed-model ANOVA with Group (typical, hemiplegia, diplegia) as between subjects factors and with distance (4 m vs. 8 m) and task (IBE, EXE, IAE) as a within subjects factor, was used to study MI across groups of participants. Non-expected interactions were analyzed using Tukey post hoc tests. To determine the relation between the movement durations of executing and imagining task, Pearson correlations were calculated. Finally, Fisher’s Z was then used to test whether the size of correlations between executed and imagined walking differed between groups of participants.
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3. Results As revealed in Table 1, executed walking durations varied across participant groups. As expected and demonstrated by the two-way ANOVA real walking times increased with the distance for each participant, F(1, 27) = 125.12, p < .00001, a = 1. Importantly, CP participants with hemiplegia (M = 7.15, SD = 1.47) and with diplegia (M = 7.21, SD = 2.46) were not significantly slower than typical individuals (M = 6.01, SD = 1.66), as no effect of group, F(2, 27) = 1.26, p = 29, a = 25, was found. This indicated that in participants with gait disturbance as well as in typical participants, actual walking duration increased with the distance to be covered. No other effects were observed. The question remains whether this effect of distance observed for walking times also exists for imagined walking times in each group of participants. This was tested by the second ANOVA with group as between-subjects factor, distance and task as within-subjects factors (Fig. 1). This ANOVA confirmed that for each group of participants and for both actual and imagined movements, a significant effect of distance was observed, F(1, 27) = 76.94, p < .00001, a = 1, such that the movement duration was longer for 8 m (M = 7.53, SD 2.27) than for 4 m (M = 4.84, SD = 1.89). This analysis also revealed a significant effect of the task, F(2, 54) = 8.71, p < .0005, a = 0.96, according to which movement duration was shorter during the last task (IAE, M = 5.65, SD = 2.08) compared to the first (IBE, M = 6.10, SD = 2.29) and the second task (EXE, M = 6.79, SD = 1.93). This main effect could be related to a general effect of fatigue occurring for each group and for both distances. However, as can be seen in Fig. 1, a significant interaction between distance and task was also observed, F(2, 54) = 3.18, p = .049, a = 58, revealing dissimilarities between the duration of executed and imagined walking as a function of the distance to be covered (Fig. 1). This non-expected result was more specifically considered by Tukey post hoc analysis that revealed that the durations of actual (M = 5.17, SD = 1.83) and imagined walking (M = 4.67, SD = 2.04) were not significantly different for the 4 m distance. On the contrary, for the 8 m distance, the movement duration of the actual walking (M = 8.41, SD = 2.30) was longer than the duration of imagined walking (M = 7.09, SD = 2.62). This difference between overt and covert movement duration was observed when the imagined displacement was performed both before (p = .0018) and after (p = .00026) the real displacement. However as illustrated by Fig. 1, this effect seems mainly observed in both clinical subtypes. In order to assess this phenomenon, values of duration for executed and imagined tasks were plotted against each other for each group of participants. For each group of participants, Pearson’s product-moment correlations (Table 2) were then calculated between EXE and IBE durations and between EXE and IAE durations for both distances of 4 m and 8 m. In typical participants, whatever the distance (4 m vs. 8 m) to be completed and whatever the trial (imagined walking before vs. after the real movement), durations of imagined walking were related to the durations of real walking. This relation between executed and imagined walking duration was also observed in CP participants, but only for the shortest distance to walk. When the distance was increased to 8 m, this linear relation was never observed in both CP participants with hemiplegia and diplegia. Since durations between executed and imagined walking for the shortest 4 m distance correlated in all groups of participants, Fisher’s Z were calculated to test whether the size of correlations between executed and imagined walking time computed for 4 m significantly differed across groups (Table 3). As can be seen in Table 3, no significant differences were observed when comparing correlations between covert and overt movement between CP participants with hemiplegia and CP participants with diplegia: correlations between imagined movement duration performed before (IBE) or after (IAE) executed movement did not differ between CP subtypes. On the contrary, correlations between covert and overt movements were significantly higher in typical participants when compared to CP participants with hemiplegia and CP participants with diplegia. 4. Discussion In the present study we used a mental chronometry paradigm to examine the motor imagery capacity of individuals with CP compared to typical individuals. We investigated MI with the walking task initially designed by Decety et al. (1989), which is nowadays a standard paradigm to investigate MI in typical participants. Based on previous results clearly demonstrating MI in participants with hemiplegia (Spruijt et al., 2013), and in line with the conclusion of Williams et al. (2012), suggesting that in CP children, MI is not related to the body affected-side, we hypothesized that MI should be also observed in CP participants with diplegia.
Table 1 Mean, standard deviation and range for actual walking times according to group of participants.
4m 8m
Mean (SD) Range Mean (SD) Range
Typical
Hemiplegia
Diplegia
4.37 (1.23) 2.80–6.00 7.64 (2.22) 5.30–12.00
5.44 (1.28) 3.5–8.0 8.85 (2.08) 6.00–12.53
5.69 (2.57) 2.79–12.00 8.73 (2.59) 5.47–13.00
[(Fig._1)TD$IG]
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Fig. 1. Movement duration in seconds (mean and standard deviation) for each group of participants and for each task (IBE, EXE, IAE) according to distance (4 m: black squares and 8 m: gray square).
Our results indicate that MI capacity observed in CP participants with hemiplegia can be extended to CP participants with diplegia. Participants with hemiplegia and diplegia demonstrate temporal invariance between executed and imagined walking. Moreover, significant correlations between real and imagined movements (IBE and IAE trials) were observed for each group of CP participants: temporal invariance between overt and covert walking duration was observed independently
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Table 2 Pearson’s product-moment correlations (r values and probabilities) between real and imagined walking. Significant correlations are in bold face.
EXE IBE 4 m EXE IAE 4 m EXE IBE 8 m EXE IAE 8 m
Typical
Hemiplegia
Diplegia
r = .97 p = .0001 r = 91 p = .001 r = .87 p = .002 r = .84 p = .005
r = .70 p = .025 r = .87 p = .001 r = .07 p = .85 r = .26 p = .47
r = .88 p = .001 r = .77 p = .002 r = .53 p = .115 r = .59 p = .07
of the order of presentation of the imagined displacement (after or before the executed walking). This indicates that the observed performance was not just related to a reminiscence involving motor memory, but to the effective use of motor imagery as demonstrated by Papaxanthis et al. (2002), in typical adolescents without brain damage. However, when compared to control participants enrolled in the present research, both hemiplegic and diplegic CP participants exhibit compromised MI. As expected, when the distance was increased from 4 m to 8 m, the linear relation between overt and covert walking was maintained in typical participants. This was not observed in CP participants. Even if CP participants were able to increase the duration of imagined walking as a function of distance, the augmentation of duration for imagined waking was unrelated to the duration of actual travel. In fact, correlations between overt and covert movement duration were not significant in CP participants when they had to imagine walking over 8 m. This result seems contradictory to the results reported by Spruijt et al. (2013) who demonstrated that increasing task difficulty, by manipulating the length and the width of the path to walk, has similar effects on movement durations for both actual and imagined walking. However the maximal distance used by Spruijt et al. (2013) was equal to 5 m, which is very close to the shortest distance we used in the present experiment. As demonstrated in Section 3, CP participants exhibit temporal invariance between overt and covert walking when they had to imagine or to walk for 4 m but not for 8 m. A possible explanation could be related to the mechanical cost of walking which is significantly higher in children with hemiplegia (Feng, Pierce, Do, & Aiona, 2014) and diplegia than in typical children (Van de Walle et al., 2012). It is well probable that increasing the distance to be covered to 8 m had a significant effect on the mechanical cost of actual walking, but no effect on imagined walking. This interpretation is coherent with the results demonstrating that the durations of actual and imagined walking were not significantly different, in CP participants, for the 4 m distance, but significantly longer for the actual walking when the distance was increased to 8 m. As underlined, the main result of the present study is that CP participants with hemiplegia or diplegia can use explicit MI when they are asked to voluntarily simulate action such as moving toward a target located at a short distance. Nevertheless, this ability is impaired in comparison to the ability observed in typical participants when the distance is increased. These results are coherent with the suggestions of Craje´ et al. (2010) reporting that MI is not an ‘all-or-nothing phenomenon’. A major interest of the study was to use the well-documented paradigm of walking task initially designed by Decety et al. (1989) in order to compare MI performance in CP and typical participants with the same task. This is successful since we documented significant differences between CP and typical participants in MI performance when the distance to be walked was increased. However, this paradigm may certainly not be sufficient to reveal subtle differences in MI performance across subtypes of CP participants. As a matter of fact, Williams et al. (2012) reported that children with congenital left and right hemiplegia do not differ from typically developing pairs when observed in simple grip hand task whereas they differ when observed in more complex pointing task involving higher spatial constraints. In future research, participants with hemiplegia and diplegia CP should be compared in a more complex walking task involving, for instance, a speed accuracy trade-off. Such a comparison should be very informative about MI in CP children since many studies provided objective evidence of the distinct differences between children with diplegia and hemiplegia in various aspects of motor functioning (Damiano et al., 2006). These studies have evidenced that CP children, within the same mobility classification level in GMFCS, show consistent pattern of differences such that hemiplegic participants exhibit better lower extremity mobility scores and better gait compared with diplegic participants. The literature also indicates that children with cerebral palsy present a lower postural balance ability compared with typically developing children (Rodda & Graham, 2001). Recent study (Rojas et al., 2013)
Table 3 P values for comparison of correlation size across groups. Significant values are in bold face.
Typical vs. hemiplegia Typical vs. diplegia Hemiplegia vs. diplegia
Correlation between EXE and IBE trials
Correlation between EXE and IAE trials
.0005 .0219 .0735
.0166 .0018 .1840
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Research in Developmental Disabilities
Motor imagery for walking: A comparison between cerebral palsy adolescents with hemiplegia and diplegia Miche`le Molina a,*, Cyril Kudlinski a, Jessica Guilbert a, Steffie Spruijt b, Bert Steenbergen b,c, Franc¸ois Jouen d a
Laboratoire Psychologie des Actions Langagie`res et Motrices, Universite´ de Caen, France Radboud University Nijmegen, Behavioural Science Institute, The Netherlands c Australian Catholic University, School of Psychology, Melbourne, Australia d Laboratoire Cognitions Humaine et Artificielle, Ecole Pratique des Hautes Etudes, France b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 October 2014 Accepted 29 October 2014 Available online
The goal of the study was to investigate whether motor imagery (MI) could be observed in cerebral palsy (CP) participants presenting a bilateral affected body side (diplegia) as it has been previously revealed in participants presenting a unilateral body affected sided (hemiplegia). MI capacity for walking was investigated in CP adolescents diagnosed with hemiplegia (n = 10) or diplegia (n = 10) and in adolescents with typical motor development (n = 10). Participants were explicitly asked to imagine walking before and after actually walking toward a target located at 4 m and 8 m. Movement durations for executed and imagined trials were recorded. ANOVA and Pearson’s correlation analyses revealed the existence of time invariance between executed and imagined movement durations for the control group and both groups of CP participants. However, results revealed that MI capacity in CP participants was observed for the short distance (4 m) but not for the long distance (8 m). Moreover, even for short distance, CP participants performed worse than typical adolescents. These results are discussed inline of recent researches suggesting that MI in CP participants may not depend on the side of the lesion. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Motor imagery Mental chronometry CP Walking
1. Introduction Motor disorders in individuals with cerebral palsy (CP) are kwown to induce deficit in motor anticipatory planning (Craje´ et al., 2010; Mutsaarts, Steenbergen, & Meulenbroek, 2004; Mutsaarts, Steenbergen, & Bekkering, 2005, 2006) which, in turn, has been be related to impaired ability to use motor imagery (i.e. Mutsaarts et al., 2006). Motor imagery (MI) is the mental simulation of a motor act, without any overt motor execution and thus refers to the capacity to produce kinesthetic representations of motor actions (Decety, Jeannerod, & Prablanc, 1989). MI would be used to predict the proprioceptive consequences of an action and then contribute to movement planning (Grush, 2004; Papaxanthis, Pozzo, Skoura, & Schieppati, 2002).
* Corresponding author at: Laboratoire Psychologie des Actions Langagie`res et Motrices, Universite´ de Caen, esplanade de la paix, 14032 Cedex 5, France. Tel.: +33 23128566263. E-mail address: [email protected] (M. Molina). http://dx.doi.org/10.1016/j.ridd.2014.10.053 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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Various studies conducted in adult participants without brain damaged (Schluter, Krams, Rushworth, & Passingham, 2001) and with left hemispheric stroke (Rushworth, Nixon, Wade, Renowden, & Passingham, 1998) have corroborated a left cerebral dominance for movement planning. In line with these studies, MI capacity in CP participants has been mainly investigated in hemiplegic cerebral palsy (HCP) with the idea that right HCP with left brain damage would be impaired in MI (Mutsaarts, Steenbergen, & Bekkering, 2007). Most of these studies have used a hand laterality task that addresses implicit MI: a judgment on the laterality of a displayed hand stimulus has to be made as quickly as possible. In this kind of tasks, participants are not explicitly instructed to imagine the rotation of their own hand to judge the laterality of the hand stimulus presented. MI is deduced from the recorded reaction times profiles: reaction times are expected to vary according to the rotation angle and to biomechanical constraints of the hand stimuli (Horst, Van Lier, & Steenbergen, 2010). Studies have led to non-converging conclusions concerning the capacity of individuals with hemiplegia on the left or the right body side to perform MI implicit tasks. For instance, Mustaarts et al. (2007) reported a linear increase in reaction time as a function of angle rotation of the hand in left hemiparetic individuals (right brain-damaged) but not in right hemiparetic individuals (left brain-damaged). In contrast, Steenbergen, van Nimwegen, and Craje´ (2007) failed to find differences in reaction times in individuals with hemiplegia on the left body side or on the right body side. Increasing biomechanical constraints modify reaction time in CP children with both left- and right-side affected (Williams, Anderson, et al., 2011; Williams, Reid, Reddihough, & Anderson, 2011) but yet another study indicated that reaction time was not affected in CP adolescents with right-sided hemiplegia (Craje´ et al., 2010). Studies using explicit MI tasks have led to more convergent results. Explicit MI tasks are supposed to increase body awareness, and consequently help participants to use MI (Spruijt et al., 2013). These tasks are based on the mental chronometry paradigm: participants are asked to move and to imagine moving themselves (or a body part), from a first person perspective, toward targets located at different distances. The durations of both, the actual and imagined movements are then compared. When participants use MI, they preserve the temporal unfolding of displacement when asked to imagine acting: a temporal invariance between executed and imagined movement durations is consequently observed. The results obtained with typical participants commonly revealed the existence of a temporal invariance between overt and covert movement whatever the distance to be performed. The mental chronometry paradigm has also been used in a fingerpointing task to targets varying in size with typically developing children (Caeyenberghs, Wilson, van Roon, Swinnen, & Smits-Engelsman, 2009) and in children with hemiplegic cerebral palsy (Williams, Anderson, Reid, & Reddihough, 2012). These studies have revealed that the duration of performed and imagined movements is congruent with Fitts’ law (Fitts, 1954): The time required to rapidly move or imagine moving to a target area is a function of the distance to the target and the size of the target both, in typically developing children (Caeyenberghs et al., 2009) and in right-sided HCP children, but not in HCP children with left-sided hemiplegia (Williams et al., 2012). According to Williams et al. (2012), this last result which is in sharp contrast with implicit hand task studies reporting compromised MI ability in right-sided but not in left-sided hemiplegic participants (Mustaarts et al., 2007), reveals that the side of hemiplegia alone is not an indicator of MI performance. This important conclusion has received some additional support from a recent study conducted by Spruijt et al. (2013), in which walking was used as the experimental motor task. Left and right hemiplegic adolescents were explicitly required to walk or to imagine walking on paths varying in length and width that defines various indexes of difficulty according to Fitts’ law (1954). Results revealed that task difficulty had similar effects on movement duration for both actual walking and imagined walking revealing MI capacity in CP adolescents with left and right hemiplegia. These results are thus inline with Williams et al. (2012), who stated that MI performance in the HCP may not be related to the affected side of hemiplegia. A direct implication of the conclusion of Williams et al. (2012) is that MI in a walking task should be also observed in other clinical subtypes of cerebral palsy. The main goal of the present research was to evaluate MI in a walking task in two clinical subtypes of CP: diplegia and hemiplegia. Contrary to hemiplegia, which most frequently involves a unilateral lesion, diplegia involves in most cases bilateral injury (Okumura, Kato, Kuno, Hayakawa, & Watanabe, 1997). CP subtypes differ according to the topography of the motor impairment with both lower limbs more affected than upper limbs in participants with diplegia and one side of the body affected in HCP participants (Dabney, Lipton, & Miller, 1997). We hypothesized that, inline with the conclusion of Williams et al. (2012), according to which MI is not related to the affected body side in CP children, MI would be observed as well in CP adolescents with diplegia as with hemiplegia. A second goal was to assess the general impairment in MI for motor task in both groups of CP participants. In order to reach this goal, MI performance of each group of participants was compared to MI performance of adolescents with a typical motor development.
2. Methods 2.1. Participants The CP participants were recruited at two schools for special education in France. Participants contributed on a voluntary basis. In accordance with the Helsinki Declaration and approved by the Regional Ethical Committee, participants took part in the study after their own written consent was obtained. Consent was also obtained from parents and/or caregivers. Inclusion criteria described participants with CP, related to identified-brain damage that occurred during the first six months of life. Information about the diagnoses and additional disabilities was obtained from participant’s medical records.
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Thirty participants were included. The age of the participants ranged from 12 to 19 years. Ten participants (mean age: 15.9 2.02) were affected by right spastic hemiplegia (HCP). Ten participants (mean age: 15.5 2.55) were affected by spastic diplegia (DCP). Participants with hemiplegia and diplegia were all able to independently walk over a distance of 8 m, without the use of an assistive mobility device. At the time of testing, all participants received physical therapy aimed at pain relief and preventing contractures. The adapted French version of the Gross Motor Function Measure (MFM) was used to evaluate the motor capacity of the participants with CP (Be´rard, Girardot, Hodgkinson, & Payan, 2006). HCP participants had MFM scores greater than 85%, and DCP participants had MFM scores ranging from 75% to 85%. Ten participants from mainstream high school (mean age: 16.3 2.01) were also recruited as control group: they all were free of any physical or neurological condition affecting motor development. 2.2. Materials and procedures The walking task was based on the classical mental chronometry paradigm initially designed by Decety et al. (1989) with typical participants. In this well-known experimental context, MI is investigated by varying the distance participants will have to walk or to imagine walking. Experiments took place in the physical therapy room. The executed and imagined conditions started by asking participants to stand behind a 1 m line representing the starting point. At the level of this starting line a visual red mark was presented. A second visual red mark was presented at a distance of 4 m or 8 m from the starting line. This second visual mark represented the arrival point. Participants were required to walk straight from the starting point to the arrival point. In the executed movement condition, the experimenter instructed the participant as follows: ‘‘You are going to walk at a comfortable pace from here (the experimenter pointed to the starting point) to the next visual target that you see over there (the experimenter pointed to the arrival point).’’ No time limitation was provided to the participant. Once the experimenter made sure that the participant understood the task, the experiment began. In the imagined motion condition, participants received the following instruction: ‘‘You are going to imagine walking from this point (the experimenter pointed to the starting point) to this one (the experimenter pointed to the arrival point). You must imagine walking at a comfortable speed. However, you will not actually walk. You just have to think of walking toward the visual target. Once you start walking, tell me, ‘‘go’’. Once you stop moving, tell me, ‘‘stop’’. Participants performed the imagined trials with the eyes open. An electronic stopwatch with milliseconds precision recorded durations of performed and imagined movements. During the executed and imagined movements, the experimenter started the stopwatch when the participant indicated the start of the movement (whether in real or imagined movement) and stopped it when the participant indicated the stop of the movement (real or imagined). All participants were instructed to walk or to imagine walking at the same speed during the trials in the executed and the imagined conditions. For the imagined conditions, all participants remained at the starting point without walking to the arrival point. In each group, half of the participants performed first the 4 m distance and then the 8 m distance condition. Reverse order was used for the other participants. Participants were randomly assigned to one of two distance-order conditions (4 m and 8 m vs. 8 m and 4 m). These distance-order conditions were aimed at disentangling motor imagery capacity from motor memory capacity (Papaxanthis et al., 2002). If motor imagery capacity is present, whatever the distance to be performed (4 m or 8 m), the time correspondence between actual and imagined displacement should be observed independently of the order of presentation of the imagined trial (after or before the executed trial). On the contrary, if time invariance is exclusively observed when imagined movement is measured after actual movement, the effect will be related to motor memory (Papaxanthis et al., 2002). For each distance, each participant successively performed three tasks: imagined before executed (IBE), executed (EXE) and imagined after executed (IAE). Each block of IBE, EXE and IAE tasks was thus repeated for each distance whatever the distance-order condition. 2.3. Data analyses First for each participant, individual movement durations for executed and imagined tasks were analyzed in order to detect outliers (movement duration > group mean 3SD). No data were identified as outliers and all measures were kept for analyses. Second, the normality (Shapiro–Wilk test) and the equivalence of variance (Levene test) of the distributions of movement durations were tested in order to control that parametric analysis could be used to evaluate motor imagery capacity of the participants. Since the tests confirmed the Gaussian nature of data, a two-way ANOVA was performed to control that for each group of participants (typical, hemiplegia, diplegia) actual walking time depended on the distance to be performed (4 m vs. 8 m). Then, tasks were analyzed with a 3 2 2 3 mixed-model ANOVA with Group (control, hemiplegia, diplegia) and distanceorder (4–8 m vs. 8–4 m) as between subjects factors and with distance (4 m vs. 8 m) and task (imagined before executed, executed, imagined after executed) as a within subjects factor. This analysis was aimed at controlling that MI did not depend on the order of presentation of the imagined trial (after or before the executed trial). Since no distance-order effect was observed, a second 3 2 3 mixed-model ANOVA with Group (typical, hemiplegia, diplegia) as between subjects factors and with distance (4 m vs. 8 m) and task (IBE, EXE, IAE) as a within subjects factor, was used to study MI across groups of participants. Non-expected interactions were analyzed using Tukey post hoc tests. To determine the relation between the movement durations of executing and imagining task, Pearson correlations were calculated. Finally, Fisher’s Z was then used to test whether the size of correlations between executed and imagined walking differed between groups of participants.
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3. Results As revealed in Table 1, executed walking durations varied across participant groups. As expected and demonstrated by the two-way ANOVA real walking times increased with the distance for each participant, F(1, 27) = 125.12, p < .00001, a = 1. Importantly, CP participants with hemiplegia (M = 7.15, SD = 1.47) and with diplegia (M = 7.21, SD = 2.46) were not significantly slower than typical individuals (M = 6.01, SD = 1.66), as no effect of group, F(2, 27) = 1.26, p = 29, a = 25, was found. This indicated that in participants with gait disturbance as well as in typical participants, actual walking duration increased with the distance to be covered. No other effects were observed. The question remains whether this effect of distance observed for walking times also exists for imagined walking times in each group of participants. This was tested by the second ANOVA with group as between-subjects factor, distance and task as within-subjects factors (Fig. 1). This ANOVA confirmed that for each group of participants and for both actual and imagined movements, a significant effect of distance was observed, F(1, 27) = 76.94, p < .00001, a = 1, such that the movement duration was longer for 8 m (M = 7.53, SD 2.27) than for 4 m (M = 4.84, SD = 1.89). This analysis also revealed a significant effect of the task, F(2, 54) = 8.71, p < .0005, a = 0.96, according to which movement duration was shorter during the last task (IAE, M = 5.65, SD = 2.08) compared to the first (IBE, M = 6.10, SD = 2.29) and the second task (EXE, M = 6.79, SD = 1.93). This main effect could be related to a general effect of fatigue occurring for each group and for both distances. However, as can be seen in Fig. 1, a significant interaction between distance and task was also observed, F(2, 54) = 3.18, p = .049, a = 58, revealing dissimilarities between the duration of executed and imagined walking as a function of the distance to be covered (Fig. 1). This non-expected result was more specifically considered by Tukey post hoc analysis that revealed that the durations of actual (M = 5.17, SD = 1.83) and imagined walking (M = 4.67, SD = 2.04) were not significantly different for the 4 m distance. On the contrary, for the 8 m distance, the movement duration of the actual walking (M = 8.41, SD = 2.30) was longer than the duration of imagined walking (M = 7.09, SD = 2.62). This difference between overt and covert movement duration was observed when the imagined displacement was performed both before (p = .0018) and after (p = .00026) the real displacement. However as illustrated by Fig. 1, this effect seems mainly observed in both clinical subtypes. In order to assess this phenomenon, values of duration for executed and imagined tasks were plotted against each other for each group of participants. For each group of participants, Pearson’s product-moment correlations (Table 2) were then calculated between EXE and IBE durations and between EXE and IAE durations for both distances of 4 m and 8 m. In typical participants, whatever the distance (4 m vs. 8 m) to be completed and whatever the trial (imagined walking before vs. after the real movement), durations of imagined walking were related to the durations of real walking. This relation between executed and imagined walking duration was also observed in CP participants, but only for the shortest distance to walk. When the distance was increased to 8 m, this linear relation was never observed in both CP participants with hemiplegia and diplegia. Since durations between executed and imagined walking for the shortest 4 m distance correlated in all groups of participants, Fisher’s Z were calculated to test whether the size of correlations between executed and imagined walking time computed for 4 m significantly differed across groups (Table 3). As can be seen in Table 3, no significant differences were observed when comparing correlations between covert and overt movement between CP participants with hemiplegia and CP participants with diplegia: correlations between imagined movement duration performed before (IBE) or after (IAE) executed movement did not differ between CP subtypes. On the contrary, correlations between covert and overt movements were significantly higher in typical participants when compared to CP participants with hemiplegia and CP participants with diplegia. 4. Discussion In the present study we used a mental chronometry paradigm to examine the motor imagery capacity of individuals with CP compared to typical individuals. We investigated MI with the walking task initially designed by Decety et al. (1989), which is nowadays a standard paradigm to investigate MI in typical participants. Based on previous results clearly demonstrating MI in participants with hemiplegia (Spruijt et al., 2013), and in line with the conclusion of Williams et al. (2012), suggesting that in CP children, MI is not related to the body affected-side, we hypothesized that MI should be also observed in CP participants with diplegia.
Table 1 Mean, standard deviation and range for actual walking times according to group of participants.
4m 8m
Mean (SD) Range Mean (SD) Range
Typical
Hemiplegia
Diplegia
4.37 (1.23) 2.80–6.00 7.64 (2.22) 5.30–12.00
5.44 (1.28) 3.5–8.0 8.85 (2.08) 6.00–12.53
5.69 (2.57) 2.79–12.00 8.73 (2.59) 5.47–13.00
[(Fig._1)TD$IG]
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Fig. 1. Movement duration in seconds (mean and standard deviation) for each group of participants and for each task (IBE, EXE, IAE) according to distance (4 m: black squares and 8 m: gray square).
Our results indicate that MI capacity observed in CP participants with hemiplegia can be extended to CP participants with diplegia. Participants with hemiplegia and diplegia demonstrate temporal invariance between executed and imagined walking. Moreover, significant correlations between real and imagined movements (IBE and IAE trials) were observed for each group of CP participants: temporal invariance between overt and covert walking duration was observed independently
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Table 2 Pearson’s product-moment correlations (r values and probabilities) between real and imagined walking. Significant correlations are in bold face.
EXE IBE 4 m EXE IAE 4 m EXE IBE 8 m EXE IAE 8 m
Typical
Hemiplegia
Diplegia
r = .97 p = .0001 r = 91 p = .001 r = .87 p = .002 r = .84 p = .005
r = .70 p = .025 r = .87 p = .001 r = .07 p = .85 r = .26 p = .47
r = .88 p = .001 r = .77 p = .002 r = .53 p = .115 r = .59 p = .07
of the order of presentation of the imagined displacement (after or before the executed walking). This indicates that the observed performance was not just related to a reminiscence involving motor memory, but to the effective use of motor imagery as demonstrated by Papaxanthis et al. (2002), in typical adolescents without brain damage. However, when compared to control participants enrolled in the present research, both hemiplegic and diplegic CP participants exhibit compromised MI. As expected, when the distance was increased from 4 m to 8 m, the linear relation between overt and covert walking was maintained in typical participants. This was not observed in CP participants. Even if CP participants were able to increase the duration of imagined walking as a function of distance, the augmentation of duration for imagined waking was unrelated to the duration of actual travel. In fact, correlations between overt and covert movement duration were not significant in CP participants when they had to imagine walking over 8 m. This result seems contradictory to the results reported by Spruijt et al. (2013) who demonstrated that increasing task difficulty, by manipulating the length and the width of the path to walk, has similar effects on movement durations for both actual and imagined walking. However the maximal distance used by Spruijt et al. (2013) was equal to 5 m, which is very close to the shortest distance we used in the present experiment. As demonstrated in Section 3, CP participants exhibit temporal invariance between overt and covert walking when they had to imagine or to walk for 4 m but not for 8 m. A possible explanation could be related to the mechanical cost of walking which is significantly higher in children with hemiplegia (Feng, Pierce, Do, & Aiona, 2014) and diplegia than in typical children (Van de Walle et al., 2012). It is well probable that increasing the distance to be covered to 8 m had a significant effect on the mechanical cost of actual walking, but no effect on imagined walking. This interpretation is coherent with the results demonstrating that the durations of actual and imagined walking were not significantly different, in CP participants, for the 4 m distance, but significantly longer for the actual walking when the distance was increased to 8 m. As underlined, the main result of the present study is that CP participants with hemiplegia or diplegia can use explicit MI when they are asked to voluntarily simulate action such as moving toward a target located at a short distance. Nevertheless, this ability is impaired in comparison to the ability observed in typical participants when the distance is increased. These results are coherent with the suggestions of Craje´ et al. (2010) reporting that MI is not an ‘all-or-nothing phenomenon’. A major interest of the study was to use the well-documented paradigm of walking task initially designed by Decety et al. (1989) in order to compare MI performance in CP and typical participants with the same task. This is successful since we documented significant differences between CP and typical participants in MI performance when the distance to be walked was increased. However, this paradigm may certainly not be sufficient to reveal subtle differences in MI performance across subtypes of CP participants. As a matter of fact, Williams et al. (2012) reported that children with congenital left and right hemiplegia do not differ from typically developing pairs when observed in simple grip hand task whereas they differ when observed in more complex pointing task involving higher spatial constraints. In future research, participants with hemiplegia and diplegia CP should be compared in a more complex walking task involving, for instance, a speed accuracy trade-off. Such a comparison should be very informative about MI in CP children since many studies provided objective evidence of the distinct differences between children with diplegia and hemiplegia in various aspects of motor functioning (Damiano et al., 2006). These studies have evidenced that CP children, within the same mobility classification level in GMFCS, show consistent pattern of differences such that hemiplegic participants exhibit better lower extremity mobility scores and better gait compared with diplegic participants. The literature also indicates that children with cerebral palsy present a lower postural balance ability compared with typically developing children (Rodda & Graham, 2001). Recent study (Rojas et al., 2013)
Table 3 P values for comparison of correlation size across groups. Significant values are in bold face.
Typical vs. hemiplegia Typical vs. diplegia Hemiplegia vs. diplegia
Correlation between EXE and IBE trials
Correlation between EXE and IAE trials
.0005 .0219 .0735
.0166 .0018 .1840
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