Kinematic parameters of hand movement during a disparate bimanual movement task in children with unilateral Cerebral Palsy

Human Movement Science 46 (2016) 239–250

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Kinematic parameters of hand movement during a disparate bimanual movement task in children with unilateral Cerebral Palsy Julian Rudisch a,⇑, Jenny Butler a, Hooshang Izadi b, Ingar Marie Zielinski c, Pauline Aarts d, Deirdre Birtles e, Dido Green a a

Department of Sport and Health Sciences, Oxford Brookes University, Oxford, United Kingdom Department of Mechanical Engineering and Mathematical Sciences, Oxford Brookes University, Oxford, United Kingdom Behavioural Science Institute, Radboud University, Nijmegen, The Netherlands d Sint Maartenskliniek, Nijmegen, The Netherlands e School of Psychology, University of East London, London, United Kingdom b c

a r t i c l e

i n f o

Article history: Received 9 June 2015 Revised 11 January 2016 Accepted 12 January 2016

Keywords: Unilateral Cerebral Palsy Bimanual coordination Kinematics Mirror movements Bimanual interference

a b s t r a c t Children with unilateral Cerebral Palsy (uCP) experience problems performing tasks requiring the coordinated use of both hands (bimanual coordination; BC). Additionally, some children with uCP display involuntary symmetrical activation of the opposing hand (mirrored movements). Measures, used to investigate therapy-related improvements focus on the functionality of the affected hand during unimanual or bimanual tasks. None however specifically address spatiotemporal integration of both hands. We explored the kinematics of hand movements during a bimanual task to identify parameters of BC. Thirty-seven children (aged 10.9 ± 2.6 years, 20 male) diagnosed with uCP participated. 3D kinematic motion analysis was performed during the task requiring opening of a box with their affected- (AH) or less-affected hand (LAH), and pressing a button inside with the opposite hand. Temporal and spatial components of data were extracted and related to measures of hand function and level of impairment. Total task duration was correlated with the Jebsen–Taylor Test of Hand Function in both conditions (either hand leading with the lid-opening). Spatial accuracy of the LAH when the box was opened with their AH was correlated with outcomes on the Children’s Hand Use Experience Questionnaire. Additionally, we found a subgroup of children displaying non-symmetrical movement interference associated with greater movement overlap when their affected hand opened the box. This subgroup also demonstrated decreased use of the affected hand during bimanual tasks. Further investigation of bimanual interference, which goes beyond small scaled symmetrical mirrored movements, is needed to consider its impact on bimanual task performance following early unilateral brain injury. Ó 2016 Elsevier B.V. All rights reserved.

1. Introduction Many tasks in everyday life require the coordinated and simultaneous use of both hands, i.e. bimanual coordination (BC). Adequate temporal and spatial integration of each hand, with limited interference between hands, usually develops with age and is often crucial for successful execution of these tasks (Birtles et al., 2011; de Boer, Peper, & Beek, 2012). Differences in ⇑ Corresponding author at: Department of Sport and Health Sciences, Oxford Brookes University, Jack Straws Lane, Oxford OX3 0FL, United Kingdom. E-mail address: [email protected] (J. Rudisch). http://dx.doi.org/10.1016/j.humov.2016.01.010 0167-9457/Ó 2016 Elsevier B.V. All rights reserved.

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the difficulty between various bimanual movement tasks can be substantial and partly determined by the similarity or divergence of movement characteristics between both hands. On a model level, symmetrical so called in-phase movements during which homologous muscles are activated at the same time, have been shown to be preferred over their asymmetrical counterpart, anti-phase movements (Haken, Kelso, & Bunz, 1985; Kelso & Schoner, 1988; Swinnen, 2002). Phase-modes that are neither in- nor anti-phase are generally the least stable within the intrinsic dynamics of a system but can be improved with practice (Kostrubiec & Zanone, 2002; Kostrubiec, Zanone, Fuchs, & Kelso, 2012). Bimanual tasks in daily life are however neither purely in-phase (e.g. clapping) nor anti phase (e.g. a drum roll), but rather characterised by completely disparate movements of both hands that have to be aligned while not interfering with each other (e.g. using cutlery). In adults, the differentiation of hand function in bimanual tasks typically shows the non-dominant hand to take on the more stabilising role (Birtles et al., 2011). Based on the model of a kinematic chain, where the proximal segment acts as the reference frame for the motion of the distal segment, Guiard (1987) proposes that the holding or stabilizing action (often carried out by the non-dominant hand) during a bimanual movement task acts as a spatial frame of reference to which the manipulating action (carried out by the dominant hand) adjusts. Apart from characteristics of the task itself, the structural integrity of central nervous system areas associated with motor control has a significant impact on the capability of inter-limb movement execution (Gooijers & Swinnen, 2014; Liuzzi, Horniss, Zimerman, Gerloff, & Hummel, 2011; Swinnen, 2002; Weinstein et al., 2013). With an incidence of 2–3 per 1000 life-births (Cans et al., 2000), Cerebral Palsy (CP) incorporates a wide range of non-progressive brain disorders affecting areas related to motor control. Causal factors are disturbances in brain development during infancy or early childhood (Rosenbaum et al., 2007) which affect motor output and sensory feedback of the affected limbs (Rosenbaum et al., 2007). Approximately one third of the concerned group have lesions that are located predominantly in one hemisphere, causing unilateral motor impairments (Arnfield, Guzzetta, & Boyd, 2013; Krageloh-Mann & Cans, 2009). Individuals who suffer from unilateral CP (uCP) generally use their less affected hand during unimanual tasks, with similar (or slightly worse) skills than their healthy peers. Bimanual activities, however, are often avoided or different strategies are sought to avoid the use of the affected hand (Sköld, Josephsson, & Eliasson, 2004). As a result and due to the lack of practice, the actual performance of the affected hand might be worse than its capacity. This imbalance of capacity and actual performance might lead to a phenomenon referred to as ‘‘Developmental Disregard” (DD) (Houwink, Aarts, Geurts, & Steenbergen, 2011; Zielinski, Jongsma, Baas, Aarts, & Steenbergen, 2014). Children with DD avoid using their affected hand despite some unimanual skill. In addition, children with uCP often experience an involuntary symmetrical activation of the contralateral hand, i.e. mirrored movements (MMs). Such MMs are usually more pronounced in the less affected hand (Kuhtz-Buschbeck, Sundholm, Eliasson, & Forssberg, 2000; Woods & Teuber, 1978) and can have a negative impact on bimanual activities of daily living that require disparate use of both hands (Adler, Berweck, Lidzba, Becher, & Staudt, 2015). A causal factor for extensive MMs may be due to ipsilateral corticospinal projection patterns (Balbi, Trojano, Ragno, Perretti, & Santoro, 2000; Norton, Thompson, Chan, Wilman, & Stein, 2008). Ipsilateral retention of corticospinal projections from the less affected hemisphere to the affected hand are sometimes retained in children with uCP, possibly dependent on the timing of their congenital brain lesion (Staudt et al., 2004). Ipsilateral projection patterns are present during typical development but become redundant during early development, hypothesised to be due to activity dependent withdrawal (Eyre, Taylor, Villagra, Smith, & Miller, 2001). MMs are also evident in patients with hypogenesis of the corpus callosum (CC; Yucel et al., 2012), thus suggesting a potential mediating role of the CC for inter-hemispheric inhibition (Gooijers & Swinnen, 2014; Weinstein et al., 2013). A variety of different motor therapy programmes have been developed to address these motor impairments, some of which have been shown to be effective in improving upper limb function (Sakzewski, Gordon, & Eliasson, 2014; Sakzewski, Ziviani, & Boyd, 2014). Generally, the existing therapeutic concepts can be classified into (i) unimanual therapies such as Constraint Induced Movement Therapy (CIMT) (Hoare, Imms, Carey, & Wasiak, 2007) and (ii) bimanual therapies such as Hand Arm Bimanual Intensive Therapy (HABIT) (Charles & Gordon, 2006; Green et al., 2013) or (iii) a combination of the two (Aarts et al., 2012; Boyd et al., 2013). Therapy interventions of the second category in particular are designed specifically to improve BC, rather than just the functionality of the affected hand (Charles & Gordon, 2006; Gordon et al., 2011). A great variety of clinical assessments are currently used to estimate treatment success. They can be roughly categorized into measures that determine the ability of the affected hand during unimanual tasks, e.g. the Jebsen–Taylor Test of Hand Function (JTTHF; Jebsen, Taylor, Trieschmann, Trotter, & Howard, 1969; Taylor, Sand, & Jebsen, 1973) or during bimanual tasks, e.g. the Children’s Hand Use Experience Questionnaire (CHEQ) (Skold, Hermansson, Krumlinde-Sundholm, & Eliasson, 2011) and the Assisting Hand Assessment (AHA) (Krumlinde-Sundholm & Eliasson, 2003). These tests measure discrete skills, such as timing of grasp and release (e.g. JTTHF), spontaneous use and movement capacity of the AH during bimanual tasks (e.g. AHA) or report on functional performance of bimanual tasks (e.g. CHEQ). Even though therapy programmes are aimed specifically at the improvement of bimanual coordination, the outcome measures which are used tend to focus on the functionality of the affected hand, rather than measuring the integration of both hands. This is despite sophisticated methods having been developed on a more experimental level. Steenbergen, Hulstijn, de Vries, and Berger (1996), as well as Utley and Sugden (1998), investigated uni- and bi-manual reaching in children with uCP and showed that movement patterns were very similar when both hands reached at the same time, despite very dissimilar patterns when the same actions were performed one hand at a time. They demonstrated a coupling effect during bimanual hand use which was mainly due to a decrease in performance of the less affected hand. Looking at changes of BC during different developmental stages in typical developing children and adults, Birtles et al. (2011) used a bimanual

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box-opening task, requiring serial reaching. Their developmental comparisons suggest that in this task, a higher movement overlap (proportion of total task duration in which both hands are active simultaneously) is preferred for efficiency. These authors showed that the Temporal Coupling (TC) of both hands was more sequential in children less than six years of age, with a higher overlap in adults. Using a similar paradigm, Hung, Charles, and Gordon (2004) showed greater movement overlap in typical developing children as compared to children with uCP. The research group was also able to show differences in the outcome measure due to different types of therapy (CIMT vs. HABIT) which could not be shown by other clinical measures (Hung, Casertano, Hillman, & Gordon, 2011). Their task was somewhat different from Birtles et al. (2011) as the drawer opening task required differentiated patterns of elbow extension and flexion of the draw opening arm and elbow extension only during reaching of the targeting hand. Both groups focussed on the temporal relationships of the two hands and did not look at measures of path accuracy. The goal of this study is the development of a functional bimanual box opening task that is characterised by disparate movements of both hands, which can be used to investigate therapy related changes in BC in children with uCP. A paradigm similar to Birtles et al. (2011) was chosen, in which participants have to open a box with one hand and reach inside the box with the opposing hand to retrieve an object. The object retrieval was substituted by a button which, when pressed by the participant, indicated a clear end point of the movement. This paper aims to investigate the performance of children with unilateral CP on the bimanual box task and to relate performance to their level of impairment as well as identify which aspects of BC (temporal or spatial) are related to performance on clinical measures of uni- and bimanual function. 2. Methods 2.1. Participants Children who participated in one of four bimanual intensive therapy interventions that were undertaken in London and Cardiff (United Kingdom) as well as in Enschede and Nijmegen (Netherlands) in 2014, were invited to participate in this study. Inclusion criteria were diagnosis of uCP with a functional level I to III according to the Manual Ability Classification System (MACS) (Eliasson et al., 2006). Children with severe intellectual impairments who were unable to follow instructions were excluded. A total of 37 children participated in this study. Group characteristics are presented in Table 1. Prior to testing, all participants (or their caregivers, as appropriate) gave informed consent. Many of the children were part of a larger study exploring neurocognitive functions using EEG and or brain structures and functions using neuroimaging and transcranial magnetic stimulation. Participants were free to withdraw from the study at any time, without giving any reasons. The study was approved by the University Ethics Committee of Oxford Brookes University and the National Research Ethics Service (NRES) in the UK as well as by the Ethics Committee at Sint Maartenskliniek for the Netherlands. All research activity was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. 2.2. Methods and materials The participants were asked to perform a bimanual box opening task, similar to Birtles et al. (2011), during which they had to open a box with one hand and press a button inside the box with their opposite hand (Fig. 1). This task was chosen in preference to the drawer opening task to consider spatiotemporal timing of similar arm movements and minimise risk of differentially exacerbating spasticity of biceps of some children with the effort of pulling a drawer open. The task was performed under two conditions; the affected hand (AHC) or less affected hand (LAHC) opening the box. Participants were seated on a height adjustable chair to ensure a stable seating position with both feet touching the floor (or footplate). They were seated in front of a height adjustable table to ensure similar starting positions of the upper limbs, with elbows flexed at a 90° angle with hands resting on the table surface. The box was positioned at a distance of 25 cm from the edge of the table and adhered to the table. Children were then asked to open the box and press the button at a self-paced, comfortable speed. The task was repeated a total of 10 times, 5 times in condition LAHC and 5 times in condition AHC in the sequential order: 3*LAHC, 3*AHC, 2*LAHC, 2*AHC. 3-Dimensional kinematic motion analysis was performed using an electromagnetic motion tracking System, Polhemus G4 (Polhemus, Colchester, Vermont, USA). Apart from their position, sensors also record orientation (Euler Angles) allowing the projection of the centre of measurement into the centre of the hand. Position and orientation were measured at a frequency

Table 1 Participant group characteristics. N

Gender (m/f)

Age (years)

MACS (I/II/III)

Nijmegen Enschede London Cardiff

13 11 8 5

7/6 4/7 6/2 3/2

10.9 ± 1.7 13.1 ± 2.6 8.2 ± 1.6 9.6 ± 1.5

7/5/1 1/9/1 3/3/2 2/2/1

Total

37

20/17

10.9 ± 2.6

13/19/5

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Fig. 1. Schematic depiction of the box opening task.

of 120 Hz. Sensors were placed dorsally over the 3rd metacarpal bone. Customized software, written in LabVIEW 2014 (National Instruments, Austin, Texas, USA) was used to conduct the measurements. Set up took about five minutes with five minutes to administer the task. 2.3. Data processing Primary data processing, i.e. filtering and events setting, was performed using a semi-automated algorithm, programmed in MATLAB R2014b (The Mathworks Inc., Natick, MA, USA). For each trial, accuracy of event-setting was checked visually. Events were determined from data of vertical spatial displacement (z-direction) and velocity profiles as obtained through numerical differentiation of spatial position in x-, y- and z-direction (filtered with a 2nd order Butterworth filter at a cutoff frequency of 15 Hz) (Fig. 2). The choice of temporal variables was informed from the developmental outcomes of Birtles et al. (2011) and work with children with CP (Hung et al., 2004). Poor spatial accuracy (SA) has been demonstrated via higher path variability during aiming of movements in the affected hand of hemiplegic patients compared to their less affected hand and compared to healthy controls (Van Thiel, Meulenbroek, Hulstijn, & Steenbergen, 2000). Based on variables of interest from these previous studies, the following temporal outcome variables were extracted: Total task duration (TTD) as the temporal difference between start of first hand (I) and button press (V) and Temporal Coupling (TC) as the temporal difference between box opening (III) and start of second hand (IV), normalized to TTD. TC is comparable with what Hung et al. (2004) and Birtles et al. (2011) referred to as movement overlap (see Fig. 2). TC provides a measure of cooperation between hands. The lid opening action can be regarded as the frame of reference: if the second hand starts too early, it has to stop and start again, since it cannot enter the box until the lid is open, and if it starts too late, the task duration will increase unnecessarily. In addition the SA of the second hand, reflecting the path variability from the first onset of movement until trigger press, calculated as the sum of the Euclidean distance between consecutive measurement points, was extracted. Outcome variables were averaged over the 5 trials per condition (AHC or LAHC). 2.4. Clinical measures 2.4.1. Jebsen–Taylor Test of Hand Function (JTTHF) The JTTHF is a measure of one handed functionality of both the affected and less affected hands. It contains 6 different items (excluding the writing tasks due to difficulties of scoring for children) that comprise tasks that require fine motor, grasping and reaching skills, e.g. scooping up beans or lifting light and heavy objects. Outcome measure is the time to completion of each task. Failure of an item results in getting the maximum time of 180 s. Even though the JTTHF is poorly standardized, in particular for children with uCP, it is commonly used in clinical as well as research settings (e.g. Brandao et al., 2013; Fong, Jim, Dong, & Cheung, 2013; Islam et al., 2014; Klingels et al., 2012; Sakzewski, Ziviani, & Boyd, 2011). 2.4.2. Children’s Hand-Use Experience Questionnaire (CHEQ) The CHEQ (Hermansson, Skold, & Eliasson, 2013; Skold et al., 2011) is a self or proxy rated measure of functionality of the affected hand during 29 bimanual daily tasks. The answering procedure for each item (if applicable) is as follows: (a) Can the task be performed independently or with help; (b) If independently, whether or not the affected hand is involved; (c) If the affected hand is involved whether it’s used as a support or grasps actively. If the affected hand is involved, three additional questions are answered on a Likert scale from 1 (much worse) to 4 (equally compared to peers): Effectiveness of use of the affected hand (grasp effectiveness); Additional amount of time needed compared to peers (time taken); and Emotional perception of hand use (feeling bothered). The following four outcome variables of the CHEQ were extracted: (1) CHEQ R1 (ratio score of all tasks performed with involvement of the affected hand divided by all tasks performed independently), (2) CHEQ R2 (ratio score of all tasks in which the affected hand grasps actively divided by all tasks in which the affected hand is involved), (3) grasp effectiveness and (4) time taken.

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0.4

Vertical Displacement (m)

a

c

0.3

0.3

IV I

0.2

IV II

III

V

0.1

0.2

II

I

0.1

0.0

0.0 0.0

0.5

1.0

1.5

2.0

2.0

0.0

0.5

1.0

1.5

2.0

b

d

1.5

Velocity (m/s)

III V

1.5

I

1.0

IV II

III

V

0.5

IV I

1.0

II

III V

1.0 Time (s)

1.5

0.5

0.0

0.0 0.0

0.5

1.0 Time (s)

1.5

2.0

0.0

0.5

Fig. 2. Vertical displacement and velocity profiles of the affected (dashed line) and less affected (solid line) hand of a single trial in condition LAHC (left column) and AHC (right column). Roman numerals indicate time points of the events as described in the text. Note the different starting points of the second hand in conditions AHC and LAHC.

2.5. Statistical analyses Statistical analyses were performed, using R 3.1.2 (R Foundation for Statistical Computing, Vienna, Austria). Normality of distribution was tested using the Shapiro–Wilk and homogeneity of variances using Levene’s Test. Correlations between outcome variables and clinical measures were calculated using Spearman’s rho, as neither of the outcome variables was normally distributed. Correlations were calculated for each condition separately. Effect of condition (AHC or LAHC) and level of impairment (MACS) on TTD, TC and SA were analysed using a two-way mixed measures ANOVA with repeated measures on condition. Post Hoc testing of level of impairment was performed separately for each condition, using a Bonferroni corrected pairwise t-test. Differences between conditions were calculated using a repeated measures t-test. Visual inspection of the distribution pattern of TC revealed a bimodal distribution pattern for this variable. Significance of this distribution was tested, using Silverman’s Test of Multimodality (Hall & York, 2001). Wilcoxon Rank-Sum Test was used to calculate differences between subgroups identified in the bimodal distribution (after post hoc-allocation, Section 3.4). 3. Results 3.1. Total task duration Participants showed large individual differences in total task duration, ranging from 1.16 to 8.05 s in AHC and 1 to 3.7 s in LAHC. Results were however positively skewed, particularly for LAHC. 50% of the participants performed faster than 2.33 s in AHC and 2.2 s in LAHC (Table 2). ANOVA showed a significant effect for condition (F(1,34) = 12.5, p < .01), for level of impairment (F(2,34) = 8.37, p < .01) as well as an interaction effect between condition and impairment level (F(2,34) = 11.27, p < .001). Post hoc comparison showed that performance was significantly slower in condition AHC ( x = 2.70 s) than in LAHC ( x = 2.20 s) (p < .01). In condition AHC, slower TTD was only found to be significant for MACS level III. No significant difference could be found in condition LAHC (Fig. 3a).

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TTD showed significant positive correlations with JTTHF scores of the affected hand and condition AHC and with JTTHF scores of the less affected hand and condition LAHC. Furthermore higher scores in the CHEQ sub-scores of grasp effectiveness and time taken were correlated with a decrease in TTD (Table 3). 3.2. Temporal Coupling Median of TC did not significantly deviate from 0 (i.e. start of second hand and beginning of lid opening are at the same time) in either condition (Table 2).TC showed a significant effect for condition (F(1,34) = 7.69, p < .01) but not for level of impairment (F(2,34) = 0.36, p = .70) nor for the interaction between condition and impairment level (F(2,34) = .92, p = .41). Post hoc comparison showed that TC is more positive in condition AHC ( x = 0.13) than in LAHC ( x = 0.02), indicating an earlier start of the second hand relative to lid opening in condition AHC compared to LAHC (p < .01) (Fig. 3b). Correlations with clinical measures were significant only between TC in the AHC and CHEQ R2 (Table 3). A further breakdown of the variable TC into its components (onset of box opening and start of the 2nd hand) is necessary at this stage as it reveals more detailed information about the Temporal Coupling of the two hands. Fig. 4 depicts the timing of those events relative to the total task duration for the two conditions AHC and LAHC. Onset of box opening is significantly later in condition AHC ( x = 0.49), than in LAHC ( x = 0.36, p < .001), there is however no significantly different start of 2nd hand between conditions. Another salient aspect is the heterogeneity of variances which is significantly greater in AHC for both, beginning of box opening (p < .05) and start of 2nd hand (p < .001). A look at the distribution patterns of TC show the reason for the skewed distribution pattern in AHC (Fig. 5). A unimodal distribution pattern cannot be rejected for condition LAHC (p = .51) (Fig. 5a). In contrast, for condition AHC, TC did not follow a unimodal distribution (p < .05) but rather a bimodal one (p = .89) (Fig. 5b). The two modes in AHC are located at 0.04 (i.e. second hand starts after beginning of lid opening) and at 0.52 (i.e. second hand much earlier than beginning of lid opening); considered as strategy 1 (S1) and strategy 2 (S2) respectively. 3.3. Spatial accuracy SA showed a significant effect for level of impairment (F(2,34) = 7.62, p < .01) as well as an interaction effect between condition and level of impairment (F(2,34) = 7.46, p < .01). No significant effect could be found for condition (F(1,34) = 1.24, p = .27). Post hoc comparison showed significantly increased SA for MACS level III in condition AHC and a trend towards an increase in SA with higher levels of impairment (Fig. 3c). Correlations between SA and clinical outcomes showed significant correlations for condition AHC and all of the CHEQ variables (CHEQ R1, CHEQ R2, CHEQ eff and CHEQ time), however no significant correlations could be found for SA in condition LAHC (Table 3). 3.4. Subgroup analysis Participants were allocated post-hoc to two groups based on the bimodal distribution of TC in condition AHC. This was done to further explore the significance of the bimodal distribution of TC in the AHC condition on bimanual coordination and the impact on SA. Group allocation was based on the clear gap between the distributions around the two modes, S1 (TC < 0.3, n = 26) with a late start of the second hand and S2 (TC > 0.35, n = 11) with an early start of the second hand, relative to the box opening action (Fig. 5b). Between group comparisons (Wilcoxon Rank-Sum Test) of SA showed a trend for children showing the S2 pattern demonstrating poorer SA (z = 1.85, p = 0.065), however notable are two outliners in each group (Fig. 6). From both video observations and kinematic data, the pattern of movement in S2 was often asymmetrical and upwards and away from the direction of travel. In addition, children using S1 were more likely to use their affected hand during a bimanual task (difference in CHEQ R1: z = 2.41, p = 0.016, Fig. 7a) and also showed higher grasp effectiveness during bimanual movements than those using S2 (difference in CHEQ R2: z = 2.91, p = 0.004, Fig. 7b). 4. Discussion In this study, we explored hand kinematics during a bimanual task requiring disparate movements in children with uCP and related these to clinical measures of hand function and impairment. It was shown, that the performance on this experTable 2 Median and interquartile ranges for the three outcome variables and difference between the conditions AHC and LAHC.

TTD (s) TC SA (m)

AHC

LAHC

2.33 [1.89–3.07] 0.04 [ 0.06–0.38] 0.53 [0.47–0.59]

2.2 [1.68–2.69] 0.02 [ 0.08–0.07] 0.55 [0.51–0.63]

TTD = total task duration; TC = Temporal Coupling; SA = spatial accuracy; AHC = affected hand condition; LAHC = less affected hand condition.

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10

a

** **

9

***

***

8

TTD (s)

7 6 5 4 3 2 1 0 LAHC

AHC

1.0

b ** **

TC

0.5

0.0

−0.5 LAHC

AHC

c 1.0

***

***

SA (m)

0.9 0.8 0.7 0.6 0.5 0.4 MACS

0.3

I

II

III

0.2 LAHC

AHC

Condition Fig. 3. Outcome variables TTD (a), TC (b) and SA (c) according to level of impairment (MACS Level I-III) and condition. Boxplots indicate median, upper and lower quartile, range and outliers of the data. Asterisks indicate significant differences between conditions/levels of impairment (*p < .05, **p < .01, *** p < .001).

Table 3 Correlation coefficients (Spearman’s rho) of the outcome variables with clinical measures. TTD (s) AHC JTTHF AH (s) JTTHF LAH (s) CHEQ R1 CHEQ R2 CHEQ efficiency CHEQ time

0.39* 0.15 0.32 0.22 0.51** 0.41*

TC LAHC 0.21 0.37* 0.10 0.05 0.27 0.02

AHC 0.10 0.11 0.29 0.36* 0.01 0.01

SA (m) LAHC 0.06 0.26 0.04 0.22 0.18 0.12

AHC 0.27 0.1 0.46** 0.41* 0.59*** 0.45**

LAHC 0.32 0.13 0.19 0.04 0.31 0.13

JTTHF = Test of Hand Function; AH = affected hand; LAH = less affected hand; CHEQ = Children’s Hand Use Experience Questionnaire; CHEQ R2 = proportional use of active grasp of the AH when both hands are used; TTD = Total Task Time; TC = Temporal Coupling; SA = spatial accuracy; AHC = affected hand condition; LAHC = less affected hand condition; CHEQ R1 = proportional use of both hands during bimanual tasks. * p < .05. ** p < .01. *** p < .001.

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AHC

Event Start of 2nd hand

LAHC

Box opening 0.00

0.25

0.50

0.75

1.00

Time (relative to toal task duration) Fig. 4. Timing of the events: Start of 2nd hand (grey box) and beginning of box opening (white box) relative to the total task duration for condition AHC (upper) and LAHC (lower). Horizontal boxes show median, upper and lower quartile and range of the data. Time point 0 represents the start of movement for the lid opening hand and time point 1 the time point of button press (i.e. end of the task). Note the later onset of box opening and the much greater variance of start of 2nd hand in condition AHC.

6

a 5

density

4

3

2

1

0 −0.4

0.0

0.4

TC in condition LAHC 6

b 5

density

4

3

2

1

0 −0.4

0.0

0.4

TC in condition AHC Fig. 5. Histogram and density plot of TC in condition LAHC (a) and AHC (b). The dashed line indicates the zero point at which start of second hand and beginning of lid opening occur at the same time.

imental task was partly affected by the level of impairment as established with the MACS as well as the level of hand function established with the JTTHF and the CHEQ. Looking at the outcome variables in more detail, some further interesting aspects become apparent. TTD seems to be dependent on the level of functionality of the leading hand, i.e. the hand that opens the lid, indicated by the correlations between the JTTHF and the respective leading hand in each condition. In addition, TTD in the condition AHC

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is affected by the level of impairment. This is hardly surprising, as the opening of the lid seems to be the more difficult part of the task, hence the time to open the lid may increase with increased levels of impairment. Children with MACS level III showed poorer spatial accuracy in the second hand when the affected hand was the leading hand. The extensive movement range seemed to show a loss of control over the less affected hand in this bimanual configuration, particularly with an early start of the second hand observed in some of the participants. Interestingly, SA of the less affected hand during the AHC was highly correlated with all of the considered variables on the CHEQ, which was used as a clinical measure of functionality of the affected hand in a bimanual task. These results suggest, that the quality and amount of usage of the affected hand is related to the amount of control of the less affected hand in a bimanual task, in which the affected hand takes a leading role. What remains unknown is whether restraining the less affected hand (as in CIMT) for these children showing this form of interference, is an appropriate treatment, as the less affected hand also seems to show some impaired movement behaviour during bimanual tasks. With increasing levels of impairment, children with uCP show better execution when performing the task in LAHC compared to AHC, as indicated by the faster movement execution and more precise target reaching. The preferred movement execution in adults has shown lid-opening to be undertaken by the non-dominant hand and reaching or retrieving by the dominant (Birtles et al., 2011). The dominant hand thus adjusts temporally and spatially to (or articulates with, see Guiard, 1987) the movement produced by the non-dominant hand. Yet, Birtles et al., 2011 has shown that this preference is not evident in infants and young children (up to 6 years) who often showed a reversed preference (i.e. dominant hand to open the lid and non-dominant to reach) or used inconsistent patterns of movement execution. The authors suggested that this may be due to the anticipatory planning that is required, with younger children approaching the first phase of the task with their dominant hand preferentially as they are focussing on the initial task demands. However, in their study, the alternative condition (leading with the opposite hand) was not explored in order to contrast Temporal Coupling between conditions. While the non-dominant leading hand may be preferential for non-motor impaired adults and older children, this explanation does not necessarily account for the difficulties demonstrated in the lid-opening phase for children with uCP. Despite being the first phase, it was the more difficult aspect of the task due to the greater complexity of movement (e.g. control of grasping, lifting, speed and force) and thus children with severe impairments of their affected hand may preferentially use their dominant hand for this component. Interestingly, TC did not show any relation with most of the functional measures in either condition. The only significant correlation was found between TC in condition AHC and CHEQ R2, suggesting that the ability of Temporal Coupling is associated with an increased use of the affected hand during bimanual tasks. A more detailed inspection of TC however showed a bimodal distribution pattern for condition AHC however, not for LAHC. These observations suggest that children use two different types of strategies to solve the task in AHC. S1 showing smaller or even negative values for TC reflecting temporally more sequential movement behaviour with decreased movement overlap of the hands in the first phase of the task (before lid opening). S2 showing higher values for TC, i.e. very early start of the second hand relative to the beginning of lid opening in an asymmetrical pattern, often upwards and away from the direction of travel. The particular movement behaviour of the group performing S2 was not expected as it has not been demonstrated in previous studies investigating bimanual control during a disparate movement task in children with uCP (Hung et al., 2011, 2004; Hung, Charles, & Gordon, 2010). Even though these children may well have been present, their definition of the start of movement as being in a forward direction would have prevented identification of this subgroup. We thus allocated the participants post-hoc to two different groups based on movement strategy and compared the performance on the CHEQ between those two groups. We found significant differences in CHEQ R1 and CHEQ R2 between groups, indicating that children who display S2 are less likely to use their affected hand during bimanual tasks. Furthermore, our findings indicate a negative influence on early movement of the 2nd hand associated with poorer SA and reduced use of affected hand in bimanual skills. These combined results may tentatively be interpreted as an indication that the temporal overlap associated with S2 may result from (unintended) bimanual interference rather than from efficient bimanual coordination. Indeed behavioural observations suggested that the early involvement of the less-affected hand seemed to result in interfering movements between the hands. Movement interference in children with uCP has historically been researched as MM’s, where interference results in an involuntary symmetrical activation of the contralateral limb (Kuhtz-Buschbeck et al., 2000; Woods & Teuber, 1978). Such pronounced MM’s have recently been shown to have a negative impact on bimanual coordination in children with uCP when comparing similar levels of impairment (Adler et al., 2015). MM’s are often present in children with ipsilateral corticomotor projection patterns from the non-lesioned hemisphere to the affected hand, with evidence to suggest that these children may respond differently to CIMT than children with typical contralateral projections from the lesioned hemisphere to the impaired hand (Juenger et al., 2013; Kuhnke et al., 2008). In addition, the CC’s inhibitory capabilities seem to be an important factor to suppress MM’s (Yucel et al., 2012). Weinstein et al. (2013) showed reduced integrity of the midbody of the CC and altered corticospinal tract in children with uCP associated with MMs. However, when performing the bimanual box task we observed associated movements that were not necessarily symmetrical to the contralateral hand. A question arises as to whether the nature of the bimanual interference we observed is the same as that of MM’s. While the phenomenon of an early involvement of the second hand may be associated with a greater degree of impairment in hand skills, two of the 11 children in the S2 group demonstrated fairly good hand function (MACS level I) and three children with MACS level III were allocated to group S1. Questions remain regarding the nature of MMs which may either interfere with the more typical control parameters of the leading hand or potentially offering a ‘strategic’ plan with initiation

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III III

0.9

II

SA (m)

0.8

III

0.7

0.6

0.5

0.4 S1

S2

Group Fig. 6. Comparison of SA between post-hoc allocated groups S1 and S2. Boxplots indicated median, upper and lower quartiles and range of the data as well as outliers. The two outliers found in each group are labelled with the according MACS level of the individuals.

a

1.00

CHEQ R1

0.75

0.50

0.25

S1

S2

b

1.00

CHEQ R2

0.75

0.50

0.25

0.00 S1

S2

Group Fig. 7. Comparison of CHEQ ratio scores CHEQ R1 (a) and CHEQ R2 (b) between post-hoc allocated groups. Boxplots indicate median, upper and lower quartile and range of the data as well as outliers.

of the primary movement pattern. Further research is required to investigate if the two different solutions S1 and S2 are related to the presence or absence of bimanual interference or MMs. 4.1. Limitations This cross sectional study was limited by the small group size of the more severely impaired children (i.e. MACS level III), as BC is particularly affected in this subgroup but with possible different underlying mechanisms underpinning performance. In addition, the group was very heterogeneous (e.g. aetiology, underlying differences in brain injury), but limitations are inherent in the population (uCP). Furthermore, counter-balancing the order of the two conditions (AHC and LAHC) may have been helpful for exploring the influence of performance in the first condition upon that in the second as would exploration of preferred hand use for the lid-opening. Due to risk of assessment fatigue and constraints on time, we were unable to include additional upper limb assessments for the majority of children. Unfortunately, this precluded use of the AHA, which may have provided a better comparison of the temporal and spatial performance on the bimanual box task than the CHEQ for validation of the outcome variables.

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5. Conclusion The bimanual box task seems to be a suitable experimental tool to investigate BC (and thus potentially changes in BC related to motor learning and motor control) in children with uCP. The results tentatively suggested that higher values of movement overlap (Hung et al., 2004, 2011) are not necessarily an indicator of better bimanual control but may also be due to interfering or associated movements. Further investigation of bimanual interference, which goes beyond the small scaled symmetrical mirrored movements, seems to be necessary to understand its influence on bimanual movement execution and intervention outcomes. From a more technical side, the feasibility of setup, measurement and extraction of temporal and spatial variables using the bimanual box task show promise as a clinical measure of bimanual hand function and for determining levels of impairment. 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