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Exp Brain Res (2004) 155: 186–195 DOI 10.

1007/s00221-003-1716-x

RESEARCH ARTICLES

Dominique van Roon . Bert Steenbergen . Ruud G. J. Meulenbroek

Trunk recruitment during spoon use in tetraparetic cerebral palsy

Received: 20 August 2002 / Accepted: 5 September 2003 / Published online: 20 December 2003 # Springer-Verlag 2003

Abstract In the present study we investigated the extent to which individuals suffering from spastic tetraparesis as a consequence of cerebral palsy tune their trunk involvement to accuracy demands in a spoon-handling task. Twenty-two participants (ten adolescents with spastic tetraparesis and 12 control participants) had to transport a spoon filled with water or sugar to a small or a large bowl that was placed within reach. Even though trunk displacement was larger in the tetraparetic participants than it was in the control participants, the effects of the imposed accuracy constraints were remarkably similar. Participants in both groups increased trunk displacement with increasing precision requirements. Furthermore, in both groups the largest trunk involvement was found in the initial and final part of the substance-transporting phase, when wrist velocity was lowest. We propose several explanations for these findings and conclude that the large trunk involvement in individuals with tetraparetic cerebral palsy should, in any case, not be regarded as a primary symptom of the disorder, but rather as an adaptive reaction to increased task demands. Keywords Spoon use . Spastic tetraparesis . Trunk involvement . Accuracy constraints . Adaptation

Introduction
Eating with a spoon seems to be an easy task to perform. This everyday form of tool use, however, is quite complex when we consider the precise coordination of movements of the trunk, arm, hand, and fingers that is required to successfully complete the task. The task becomes particularly complex when a liquid has to be transported
D. van Roon (*) . B. Steenbergen . R. G. J. Meulenbroek Nijmegen Institute for Cognition and Information, University of Nijmegen, PO Box 9104, 6500 HE Nijmegen, The Netherlands e-mail: D.vanRoon@nici.kun.nl Tel.: +31-24-3612148 Fax: +31-24-3616066

(e.g. soup) because of the additional risk of spilling when bringing the spoon to the mouth. Compared to regular reaching and grasping tasks, in which accuracy demands impose themselves mainly at the end of the task (e.g. dependent on target size), transporting substances with a spoon requires the continuous monitoring of required accuracy as the movement unfolds. It is this feature of a spoon-handling task that makes it particularly interesting and new to use such a task to study the way in which people who have to cope with a permanent motor disorder handle combinations of accuracy demands. In the present study, we investigated to what extent the specific accuracy demands of spoon use are reflected in the recruitment of the trunk in participants suffering from a spastic tetraparesis as a consequence of cerebral palsy (CP). CP is a condition caused by chronic, non-progressive brain damage in young children. This damage can be caused by, for instance, an oxygen shortage at or around birth, intra-uterine infections, prematurity or (the removal of) a brain tumour at a very young age. It can cause motor deficits (e.g. spasticity, dystonia, ataxia, athetosis, hypotonia; Albright 1996) and sensory deficits (e.g. impaired proprioception and stereognosis; Cooper et al. 1995), but can also cause seizures and behavioural and cognitive problems. Spasticity arises in approximately 60% of the CP cases (Sugden and Keogh 1990). Sanger et al. (2003) argued that it is a disorder characterized by hypertonia, in which one or both of the following signs are present: (1) The resistance to an externally imposed movement increases when the velocity of stretch increases and varies with the direction of joint movement, and/or (2) this resistance rises fast above a threshold speed or joint angle. In general, voluntary muscle activation is disturbed. The impairment may involve muscular weakness, disordered coordination of synergistic agonist muscles, failure to inhibit antagonistic muscles, associated movements, stereotyped movement synergies, and decreased dexterity (Lance 1980; Barnes et al. 1994; Filloux 1996). As has been shown in studies of reaching, grasping and eating (Van Thiel and Steenbergen 2001; Van Roon et al. 2003), a behavioural

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characteristic of individuals with a spastic paresis as a result of CP is an increased involvement of the trunk. A similar characteristic was found in hemiparetic stroke patients (e.g. Cirstea and Levin 2000; Levin et al. 2002). Here, we wanted to find out whether this larger trunk involvement reflects a flexible adaptation to the disorder and the task constraints or, alternatively, whether it should be regarded as a manifestation of the disorder per se (Latash and Anson 1996; Steenbergen et al. 2000; Van Thiel and Steenbergen 2001; Steenbergen and Meulenbroek 2003). Studying the combined effects of task constraints and the disorder in everyday perceptuomotor tasks provides, in our view, a unique way to try to disentangle indices of flexible and rigid behaviour. Research in healthy individuals has shown that an increase in accuracy constraints, both during the movement and at the end of it, gives rise to a larger displacement of the trunk (Steenbergen et al. 1995; Van der Kamp and Steenbergen 1999; Mackey et al. 2000). Steenbergen et al. (1995) and Mackey et al. (2000) suggested that an increased use of the trunk, with its large mass and inertia, might help stabilize the arm–hand system because a damping effect might occur. Alternatively, the lower velocity of the wrist in tasks demanding higher accuracy might also underlie the larger trunk displacement. As demonstrated by several researchers, reaching movements at higher velocities are achieved primarily by smaller-mass body segments, while during such movements at lower velocities an increased contribution of greater-mass segments (with a larger inertia) is observed (Rosenbaum et al. 1991, 1995; Vaughan et al. 1996; Wang and Stelmach 2001). In the present study we examined whether individuals with spastic tetraparesis as a result of CP either flexibly tune the amount of trunk involvement to the various precision requirements or rigidly displace the trunk over a fixed distance during spoon-use, independent of the imposed accuracy demands. Our participants had to transport a spoon filled with either a fluid or a solid substance (manipulation of accuracy during transport) to a small or a large bowl (manipulation of accuracy at the end of the transport). Based on the findings of the studies mentioned above, we expected a larger trunk involvement in the tetraparetic group than in the control group. In addition, we expected a larger trunk involvement if water, rather than sugar, had to be transported and if the bowl into which the spoon had to be emptied was small rather than large. An absence of such accuracy effects would be expected if trunk use constituted a primary symptom of the disorder.

participants (mean age 25 years 6 months, SD 3 years 0 months, range 20;0–30;0 years;months) with no known history of neurological disorders took part in the experiment. The study was approved by the local ethics committee and performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. At the time of testing, all participants with tetraparesis were students at the Werkenrode Institute (Groesbeek, The Netherlands), where they followed an adapted educational program. They all had sufficient physical and cognitive abilities to perform the task under study and normal or corrected-to-normal vision. Four tetraparetic participants were able to walk independently, while the other six sat unstrappped in a wheelchair from which they performed their daily activities. We therefore inferred that all had functional sitting balance. All participants were naive as to the purpose of the task and gave their informed consent prior to data collection. Additional participant information is given in Table 1.

Task and procedure Participants were seated at a table on an ergonomic chair that could be adjusted such that the following criteria were met. When the forearms were on the table, the elbows were flexed at 90°. Additionally, the feet were flat on the ground (or placed on a foot rest) and the knees were also flexed at 90°. Prior to the start of the experiment, the participants of the tetraparetic group performed the Purdue Pegboard test (Tiffin 1968). As recommended in the examiner’s manual, they performed the test three times for 30 s with their preferred hand followed by three times for 30 s with their non-preferred hand. The total score for each hand is presented in Table 1. After the experimenter had given a verbal go-signal, the participant had to reach for a spoon filled with a particular substance, and pick it up. Subsequently, they had to transport the spoon to a cylindrical bowl that was placed further along the sagittal axis towards the back of the table (hereafter denoted as substancetransporting phase), and empty the spoon into the bowl (see Fig. 1 for the experimental set-up). The substance-transporting phase was the focus of our study, and all analyses are performed on this phase. Participants had to transport red-coloured water in half of the trials, whereas in the other half they had to transport sugar. The diameter of the bowl was 5 cm or 11 cm. To determine a participant-dependent, appropriate position of the bowl in the workspace, participants were instructed to hold the spoon in a power grip so that the stem of the spoon was parallel to the front edge of the table (x-axis, see Fig. 1), and actively stretch their arm as far as possible without moving their trunk.

Methods
Participants Ten individuals diagnosed as having spastic tetraparesis as a consequence of CP (mean age 17 years 2 months, SD 1 year 3 months, range 14;7–18;6 years;months) and twelve healthy control Fig. 1 Experimental set-up from the participant’s viewpoint: a starting block, b spoon holder, c spoon, d letter balance, e bowl

188 Table 1 Participant information (CP cerebral palsy) Subject Sex ID Age Active range Hand Purdue Pegboard scorec (years; months) of motion (cm)a preferrenceb Pref. hand Non-pref. hand Diagnosis

Tetraparetic participants 1 F 18;1 2 M 18;6 3 F 17;4 4 M 18;6 5 M 16;1 6 F 14;7 7 M 17;4 8 F 17;9 9 M 16;4 10 F 17;4 Control participants 1–12 8F/4M 25;6
a

29 34 43 42 42 32 47 39 50 32 35–42

Right Left Right Right Left Left Right Left Right Right Right

25 39 30 28 32 33 15 18 30 25

14 14 16 22 18 21 7 16 28 13

CP, CP, CP, CP, CP, CP, CP, CP, CP, CP,

spastic spastic spastic spastic spastic spastic spastic spastic spastic spastic

tetraparesis, epileptic tetraparesis tetraparesis tetraparesis tetraparesis tetraparesis tetraparesis tetraparesis tetraparesis tetraparesis, epileptic

53 49 – Norm scores for healthy individuals

Distance between the front edge of the table and the midpoint of the bowl. See Task and Procedure section for a detailed description of the method of determination of this active range of motion b As indicated by the participant c The total number of pins placed into the holes in three 30-s periods (see Task and Procedure section)

Subsequently, the bowl was positioned so that its midpoint corresponded to the midpoint of the spoon. We made the position of the bowl dependent on the distance that could be covered by moving only the arm, because we wanted to study the involvement of the trunk during task performance when this involvement was not strictly necessary to perform the task. On average, the distance between the front edge of the table and the midpoint of the bowl (active range of motion; see Table 1) in the tetraparetic group (mean 39 cm, SD 7.0 cm) was the same as this distance in the control group (mean 39 cm, SD 2.4 cm; t=0.085, P=0.933). Note that the distance that needed to be covered with the spoon in the substancetransporting phase (hereafter denoted as transport distance), was less than half the active range of motion (or more precisely, this distance minus 7 cm—the distance between the front edge of the table and the midpoint of the starting block—divided by two). The spoon had a stem that measured 12 cm in length and an aluminium round bowl (diameter of 4.5 cm and depth of 1.2 cm). It weighed approximately 80 g. The manipulations resulted in four unique conditions, defined by Substance (water, sugar), and Bowl (small, large). For each condition, 45 trials were performed resulting in a grand total of 180 trials per participant. The two substances were presented in two blocks of 90 trials, counterbalanced across the participants of each group. Within each block, the factor Bowl was randomized. The tetraparetic participants performed the task with their least affected hand, as indicated by the participant and confirmed by the Purdue-Pegboard scores. The control participants used the hand that they had indicated as being used for everyday unimanual tasks. At the start of each trial, the experimenter placed the spoon on top of a plastic cube of approximately 10 cm in height (located half-way between the midpoint of the starting block and the midpoint of bowl), just underneath a plastic slat and on top of a little metal detector, thereby leaving the stem ‘free in the air’ (see Fig. 1). Presenting the spoon like this allowed the participants to grasp the spoon in their preferred way. The spoon was filled with approximately 6 g of either sugar or water. Participants were asked to sit upright, with their back against the back of the chair. The palm of their preferred hand rested on the starting block to standardize the starting position of the hand. This block measured 10.0 cm in length, 14.3 cm in width, and 6.5 cm in height. It was

positioned 2 cm from the front edge of the table and approximately 8 cm to the ipsilateral side of the midsagittal plane of the body, so that the midpoint of the block corresponded with the midpoint of the stem of the spoon. The other hand rested on the tabletop. Participants were not restrained by any means, nor were any speed demands imposed. In addition, no instructions were given concerning the type of grip that had to be used. However, they were instructed to try not to spill any of the substance. At the end of each trial, the substance that was successfully transported to the bowl was weighed by means of a letter-balance (precision 0.5 g). Before the experiment started, each participant performed six practice trials in which three spoons filled with water and three spoons filled with sugar had to be transported to the small bowl. After half of the experimental trials, there was always a short break, but participants could always indicate when they needed extra rest. The total experiment took approximately 1.5 to 2 h of which 30 to 45 min were spent on preparations and 60 to 75 min on the performance of the 180 trials. A 3-D motion-tracking device (Optotrak 3020) was used for movement recording. Four infrared light-emitting diodes (IREDs) were placed on the wrist, elbow and both shoulders and their positions were sampled at a rate of 200 Hz with a spatial accuracy of 0.2 mm in the x-, y-, and z-dimension. The actual testing was also videotaped.

Data analysis The positional data were filtered using a zero-phase lag, secondorder Butterworth filter with a cutoff frequency of 10 Hz and then differentiated to calculate movement velocity and acceleration. Semi-automatic segmentation routines were used to define the start and end of the substance-transporting phase, on which all subsequent analyses were performed. The start of the movement was determined by the moment at which the wrist velocity in the ydirection (see Fig. 1) reached 20 mm/s after the spoon had lost

189 Fig. 2 Typical examples of task performance. Y-position profiles of the wrist, the ipsilateral and the contralateral shoulder (upper graphs) and the tangential wrist velocity profile (lower graphs) as a function of movement duration for one trial of a control participant (left graphs) and for one trial of a tetraparetic participant (right graphs). In both depicted trials water had to be transported to the small bowl

contact with the metal detector.1 The end of this phase was determined by the moment at which the wrist velocity in the ydirection fell below 10% of its peak velocity. On the basis of the displacement data of the wrist several standard kinematic variables (mean tangential velocity, maximum tangential velocity, percentage of the movement time to peak velocity, dysfluency of the movement, and wrist displacement [in the ydirection] relative to the transport distance) were determined. Dysfluency was determined by the number of zero-crossings per second in the acceleration profile of the wrist. The forward wrist displacement relative to the transport distance was taken as a measure of the way in which the bowl was approached (which was also dependent on the type of grip used) in combination with the location at which the spoon was emptied (e.g. in front of or behind the midpoint of the large bowl). When the bowl of the spoon was held out further to empty the spoon, or when the spoon was emptied earlier (closer to the front edge of the bowl), the distance that was covered by the wrist was shorter. To examine the trunk involvement in the substance-transporting phase we determined the absolute displacement in the y-direction of both the ipsilateral shoulder (i.e. the shoulder of the same body-side as the arm that performed the task) and the contralateral shoulder between the start and the end of that phase. The displacement of the contralateral shoulder in the y-direction was taken as a measure of sagittal trunk displacement. When the sagittal displacement of the ipsilateral shoulder was larger than the sagittal displacement of the contralateral shoulder, the trunk was rotated. Trunk rotation between the start and the end of the substance-transporting phase was calculated as the difference in the angle between the x-axis and the line connecting the IREDs on the ipsilateral and contralateral
1We checked in two control participants and two tetraparetic participants (the slowest and the fastest one of each group) whether different results were obtained if we determined the start by the moment at which the wrist velocity in the y-direction rose above 10% of peak wrist velocity in the y-direction after the spoon had lost contact with the metal detector. It appeared that the results were qualitatively similar to the results reported below.

shoulder. To determine the distribution of sagittal trunk displacement across the initial, middle and final part of the substancetransporting phase, we divided this phase into three equal parts on the basis of the distance covered by the wrist in the y-direction. Subsequently, we determined the displacement of the contralateral shoulder in the y-direction in each of the three parts of the substancetransporting phase.

Statistical analysis Means of the dependent variables across the replications of each condition were analysed using repeated measures analysis of variance (ANOVA). The design consisted of one between-subjects factor, Group (tetraparetic versus control), and two within-subjects factors, namely, Substance (water versus sugar) and Bowl (small versus large). To analyse the distribution of the displacement of the trunk across the three successive parts of the substance-transporting phase, and the mean wrist velocity in these three parts, we added an extra within-subjects factor Part (initial, middle and final part). When requirements for homogeneity of variances (Levene’s test) were not met, which was only the case for the displacement of the trunk in the final part of the substance-transporting phase, we used a parametric modification of the F-test (Welch’s test; see Maxwell and Delaney 1990) to study the differences between groups. Step-down analyses of statistically significant interactions were performed by means of contrasts. To determine the relationship between the sagittal trunk displacement and the mean wrist velocity, Pearson’s correlation coefficients were calculated for each participant separately, across all 180 trials. The level for significance was set to P≤0.05. As a measure of effect size η2-values are reported.

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Results
General task performance Both the control participants and the participants with spastic tetraparesis were able to perform the task. Hardly any of the substance was spilled. In each condition a total of 90 g of the substance (6 g in each of the 15 trials) had to be transported to the bowl. The control participants transported on average 89.5 g per condition (SD 1.1 g, range 85–90 g) and the tetraparetic participants 89 g (SD 1.1 g, range 84.5–90 g). It must be noted that the spilling almost always took place at the end of the task when the spoon was emptied. In Fig. 2, two examples of the recorded movements and corresponding movement kinematics are displayed (one trial for each group). Upon careful checking of the video recordings, it was established that the employed grip types were comparable across groups. In each group, two participants used predominantly power grips, while the other participants used precision grips. Kinematic data of the end-effector Table 2 shows the kinematic characteristics of the wrist movement in the substance-transporting phase for the tetraparetic group and the control group separately. Mean tangential wrist velocity To check whether our manipulations of accuracy had been effective, we examined their effects on the mean tangential wrist velocity. We expected that the task was performed at a lower speed if accuracy constraints were higher, as is normally the case in regular reaching tasks (e.g. Marteniuk et al 1987). The participants with spastic tetraparesis made slower movements than the control participants in the substancetransporting phase (143 mm/s and 192 mm/s, respectively; F(1,20)=20.20, P<0.001, η2=0.502). Across both groups, the movements were performed slower when water had to be transported than for sugar transportation (147 mm/s versus 193 mm/s; F(1,20)=117.89, P<0.001, η2=0.855), and when the bowl was small rather than large (157 mm/s versus 183 mm/s; F(1,20)=55.87, P<0.001, η2=0.736). A step-down analysis of the interaction between Substance, Bowl and Group (F(1,20)=4.84, P=0.04, η2=0.195) showed that the interaction between Substance and Bowl was only significant for the control group (F(1,11)=32.35, P<0.001, η2=0.746). In that group the difference in mean wrist velocity between the water condition and the sugar condition was larger when the substance was transported to the large bowl (difference 53 mm/s; F(1,11)=74.03, P<0.001, η2=0.871) rather than the small bowl (difference 38 mm/s; F(1,11)=66.52, P<0.001, η2=0.858).

subject SD and CV for each condition (combination of factors Substance and Bowl) and then averaging across the participants of each group (control and tetraparetic)

Coefficient of variation (%)

Tetraparetic Control Tetraparetic Control Tetraparetic Control

Within-subject SD

Table 2 Kinematic characteristics of the wrist for the substance-transporting phase (across both bowls and substances). The average within-subject standard deviations (SDs) and the average coefficients of variation (CVs) were determined by first calculating the within-

Mean (between-subject SD)

Mean tangential wrist velocity (mm/s) Peak tangential wrist velocity (mm/s) Movement time to peak velocity (% total movement time) Number of zero-crossings per second Wrist displacement (% transport distance)

192 (19) 278 (29) 52 (4) 2.8 (1.0) 64 (11) *P<0.05, **P<0.01, ***P<0.001

143 (32)*** 212 (53)*** 48 (4)* 5.2 (1.5)*** 70 (11)

19 31 6 1.7 9

23* 34 11*** 2.3* 8

10 11 12 59 15

17*** 17*** 25*** 47*** 12

191

Fig. 3 Mean tangential wrist velocity for each group separately in three successive parts of the substance-transporting phase. Error bars represent between-subjects variability (SDs)

the adopted emptying strategy (see Table 3). The distance that was covered by the wrist relative to the transport distance of the spoon was taken as a measure of this strategy. In two cases, the distance that was covered by the wrist was shorter than the transport distance of the spoon: when the bowl of the spoon was extended further to empty the spoon (which was easier when the spoon was held in a precision grip), and when the spoon was emptied closer to the front edge of the bowl. It appeared that the relative distance that was covered by the wrist was smaller when sugar was transported than for water transportation (F(1,20)=40.67, P<0.001, η2=0.670), and when the bowl was large rather than small (F(1,20)=18.69, P<0.001, η2=0.483). However, no difference was found between the control group and the tetraparetic group. Trunk recruitment Total trunk displacement and trunk rotation It was verified that the participants with spastic tetraparesis displaced their trunk more than the control participants during the substance-transporting phase (F(1,20)=6.49, P=0.019, η2=0.245; see Fig. 4), as we expected on the basis of previous research. The tetraparetic group displaced the trunk on average 11.8 mm, which equates with an average of 11.2% of the displacement of the wrist. The control group showed an average trunk displacement of 4.7 mm, which equates with an average of 5.5% of the displacement of the wrist. As a control measure, we examined trunk displacement prior to the substancetransporting phase (reaching towards and picking up the spoon), which also was larger in the tetraparetic group than in the control group (21.3 mm and 7.3 mm, respectively; F(1,20)=4.83, P=0.040, η2=0.194). The within-subjects standard deviation of the trunk displacement in the substance-transporting phase was larger for the tetraparetic group than for the control group, but this was probably a consequence of the larger mean displacement. This was substantiated by the absence of any difference between groups for the within-subjects coefficient of variation for trunk displacement. An important finding was that the participants were able to tune the amount of trunk displacement to the various precision requirements. Averaged across groups, the trunk displacement was larger when the substance had to be transported to the small bowl rather than to the large bowl
midpoint of the bowl in the substance-transporting phase: effects of factors Substance (sugar, water) and Bowl (large, small) Tetraparetic participants Water Sugar Small 161 (19) 71 (10) Large 182 (39) 66 (12) Small 152 (37) 69 (10) Water Large 133 (32) 70 (14) Small 105 (31) 75 (9) Large 177 (17) 64 (13)

Mean tangential wrist velocity in the initial, middle, and final part of the substance-transporting phase To further examine the course of wrist velocity during the substance-transporting phase, we divided this phase into three equal parts on the basis of the distance covered by the wrist. It appeared that the mean tangential velocity of the wrist was highest in the middle part of the substancetransporting phase and lower in the initial and final part (F(2,40)=153.50, P<0.001, η2=0.885), as is usually the case in regular reaching tasks (see Fig. 3). In both groups the difference in wrist velocity between the initial part and middle part, and between the middle and final part were statistically significant (statistics respectively F(1,11)=324.58, P<0.001, η2=0.967 and F(1,11)=178.68, P<0.001, η2=0.942 for the control group, and F(1,9)=86.68, P<0.001, η2=0.906 and F(1,9)=33.47, P<0.001, η2=0.788 for the tetraparetic group). No significant difference was found between the wrist velocity in the initial part and that in the final part. Furthermore, it was shown that a difference in wrist velocity between the two groups existed in all three parts (part 1: F(1,20)=9.99, P=0.005, η2=0.333; part 2: F(1,20)=17.54, P<0.001, η2=0.467; part 3: F(1,20)=23.20, P<0.001, η2=0.537). Wrist displacement as a percentage of the transport distance of the spoon Participants were left completely free with respect to the way in which the spoon was emptied in to the bowl. Here, we examined the effects of Group, Substance and Bowl on
Table 3 Means and between-subject standard deviations (in parentheses) of mean tangential wrist velocity and wrist displacement as percentage of the distance between spoonholder and Control participants Sugar Large Mean tangential wrist velocity (mm/s) Wrist displacement (% transport distance) 230 (32) 57 (15) Small 199 (20) 63 (10)

192

(F(1,20)=8.22, P=0.010, η2=0.291). It appeared that the effect of Substance was only present in the tetraparetic group (F(1,9)=20.69, P=0.001, η2=0.697). Besides a larger trunk displacement, the participants with spastic tetraparesis also showed a larger trunk rotation than the control participants during the substance-transporting phase (4.5° and 3.3°, respectively; F(1,20)=5.13, P=0.035, η2=0.204). As can be observed in Fig. 4, the difference between the ipsilateral and the contralateral shoulder displacement was larger in the tetraparetic group.
Fig. 4 Sagittal displacement of the ipsilateral and the contralateral shoulder (in millimetres) during the substance-transporting phase, for each group separately. Error bars represent between-subjects variability (SDs)

The distribution of trunk displacement across the initial, middle and final part of the substancetransporting phase To examine the time-course of trunk involvement during the transporting phase, we examined the trunk displacement in each of the three parts of the substancetransporting phase (initial, middle and final part). As shown in Fig. 6, the involvement of the trunk decreased from the initial to the middle part of the substancetransporting phase and then increased from the middle to the final part for both groups. A main effect of Part (F(2,40)=9.72, P<0.001, η2=0.327) was found, as well as an interaction between Part and Group (F(2,40)=5.04, P=0.011, η2=0.201). In the control group the displacement was 2.7 mm in the initial part, 0.5 mm in the middle part and 1.4 mm in the final part of the movement (note that these values are not cumulative but represent distances covered in each part separately). Since especially the last two displacements are very short, it must be kept in mind that they could have been a result of skin displacement during task performance. Nevertheless, step-down analyses showed that in this group the difference between the initial part and middle part, and between the middle and final part were statistically significant (statistics respectively F(1,11)=19.18, P=0.001, η2=0.635 and F(1,11)=13.89, P=0.003, η2=0.558). In the tetraparetic group the distances covered by the trunk were 3.8 mm, 2.3 mm and 5.6 mm, in the initial, middle, and final part, respectively. The trunk displacement did not differ between the initial and middle part, while this displacement increased during the final part (F(1,9)=9.33, P=0.014, η2=0.509). Furthermore, the difference between the two groups only existed in the middle and final part of the substance-transporting phase (F(1,20)=4.49, P=0.047, η2=0.183 and Welch’s W(1,11.2)=10.91, P<0.01, respectively), whereas the difference between the groups was not statistically significant in the initial part. Relationship between trunk displacement and mean tangential wrist velocity To determine the relationship between the sagittal trunk displacement and the mean tangential wrist velocity, Pearson’s correlation coefficients were calculated for

Fig. 5 Sagittal trunk displacement (in millimetres) during the substance-transporting phase as a function of Substance (sugar, water), Bowl (large, small) and Group (control, tetraparetic subjects). Error bars above the mean bars represent betweensubjects variability (SDs) and error bars within the bars represent the mean within-subject variability

Fig. 6 Sagittal displacement of the trunk (in millimetres) for each group separately in three successive parts of the substancetransporting phase. Error bars represent between-subjects variability (SDs)

(10.5 mm and 5.3 mm, respectively; F(1,20)=32.93, P<0.001, η2=0.622) and when water had to be transported rather than sugar (9.6 mm and 6.2 mm, respectively; F(1,20)=25.04, P<0.001, η2=0.556; see Fig. 5). However, an interaction between Substance and Group was found

193 Table 4 Correlations between sagittal trunk displacement and mean tangential wrist velocity in the substance-transporting phase (across all 180 trials) for each control and tetraparetic participant Subject ID Correlation coefficient Trunk displacement (mm) Mean tangential wrist velocity (mm/s) Mean (SD) Range Control participants 1 −0.18* 2 −0.53*** 3 −0.28*** 4 −0.32*** 5 −0.63*** 6 −0.19** 7 −0.63*** 8 −0.19* 9 −0.22** 10 +0.17* 11 −0.31*** 12 −0.07 Tetraparetic participants 1 −0.28*** 2 −0.26*** 3 −0.63*** 4 −0.53*** 5 −0.47*** 6 −0.40*** 7 +0.31*** 8 −0.46*** 9 −0.07 10 −0.26*** −12 to 27 −8 to 38 −4 to 16 −3 to 13 −11 to 18 −6 to 4 −5 to 16 −8 to 6 −5 to 20 −5 to 7 −1 to 50 −4 to 52 −1 −13 −5 −3 −1 −11 −20 −1 −20 −7 to to to to to to to to to to 36 15 40 66 93 75 20 59 65 29 Mean (SD) Range

1 (5) 5 (7) 5 (4) 5 (3) 2 (5) −1 (2) 4 (4) 0 (2) 4 (5) 0 (2) 15 (10) 16 (12) 10 (7) 2 (3) 16 (9) 20 (13) 22 (15) 17 (13) −2 (7) 12 (9) 14 (15) 7 (5)

164 211 204 169 166 213 196 180 184 198 217 203 108 152 142 125 141 162 168 115 210 107

(27) (36) (38) (31) (32) (27) (34) (26) (35) (21) (61) (30) (27) (18) (42) (50) (38) (45) (55) (37) (42) (31)

105 136 144 123 97 138 130 125 103 140 118 140 59 114 63 43 63 79 78 51 102 42

to to to to to to to to to to to to to to to to to to to to to to

272 307 308 284 262 281 278 242 286 260 337 289 199 201 267 228 230 309 302 197 301 194

*P<0.05, **P<0.01, ***P<0.001

each participant separately across all 180 trials. Significant negative correlations between trunk displacement and mean wrist velocity were found for 10 of 12 control participants (one-tailed sign-test, P=0.019) and for 8 of 10 tetraparetic participants (one-tailed sign-test, P=0.055), indicating that a decrease in the speed of moving coincided with an increase in trunk displacement. On average this correlation was approximately −0.30 in both groups (see Table 4).

Discussion
In this study, we examined how the damaged nervous system of individuals with tetraparesis as a result of CP deals with increased accuracy constraints. For this purpose, we studied spoon use because this task allowed us to manipulate accuracy demands both during transport (by variations in the substance to be transported) and at the end of the task (by variations in the size of the bowl in which the spoon needed to be emptied). The effect of the latter accuracy constraint on the mean wrist velocity is in line with reaching and grasping studies that also examined the effects of accuracy constraints at the end of the movement (Marteniuk et al. 1990; Bootsma et al. 1994; Berthier et al. 1996; Weir et al. 1998). In addition, the effects of manipulation of accuracy during the task

corroborated previous findings in a healthy subject population (cf. Van der Kamp and Steenbergen 1999). Our main question was whether the larger trunk recruitment commonly found in individuals with a paresis as a result of CP represents a fixed movement pattern or, alternatively, might be regarded as a flexible adaptation to deal with the combination of disorder and task constraints. Overall, participants with tetraparesis showed an increase in trunk involvement compared to control participants. Although absolute values of trunk displacement (and rotation) were small, when taken relative to wrist displacement trunk displacement in the tetraparetic group was more than double that of the control group (11.2% versus 5.5%). This finding extends previous findings on trunk involvement in individuals with unilateral brain damage, either from CP (cf. Steenbergen et al. 2000; Van Thiel and Steenbergen 2001) or from stroke (cf. Cirstea and Levin 2000; Levin et al. 2002), to individuals with more diffuse damage of the brain (tetraparetic patients). Hence, a general reorganization may involve an increased involvement of the trunk. Two additional remarks must be made to put this finding into perspective. First, we showed that prior to the substance-transporting phase, the tetraparetic participants already displayed a larger trunk involvement than the control participants did. This means that a larger anticipatory trunk displacement which might have been present in the control group can be ruled out as an

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explanation for the larger trunk displacement in the tetraparetic group in the substance-transporting phase. Second, as explained in the Methods section, the bowl was placed within the active range of motion for each participant and trunk recruitment was therefore not necessary for the performance of the task. The effects of the requirement for accuracy on trunk involvement were straightforward. Increasing the accuracy constraint at the end of the task caused an increased trunk displacement for both the control and the tetraparetic participants. Consequently, rather than displacing the trunk a fixed, standardized distance, tetraparetic participants flexibly tuned the degree of trunk involvement to the accuracy demands imposed, as has previously been shown in control participants (cf. Steenbergen et al. 1995; Mackey et al. 2000). Whereas the accuracy constraint during the movement had no effect on trunk involvement for the control participants, participants with tetraparesis increased trunk involvement when transporting water. In sum, tetraparetic participants dealt with increased accuracy constraints by an increased use of the trunk. This leads us to conclude that trunk involvement in this group may be regarded as a flexible adaptation to the imposed task demands. Note that the preferred hand of all tetraparetic participants was relatively mildly impaired, although they made slower movements, needed more time decelerating, and moved less fluently than the control participants. They were all able to perform the task without spilling. It therefore remains to be seen whether this pattern of results will hold true when more severely affected people are tested. To further examine the nature of trunk involvement, we also analysed its time-course. In both groups, the displacement was largest during the initial and the final part and smallest during the middle part, although in the tetraparetic group the decrease in trunk displacement from the initial to the middle part was not significant. One reason for this distribution of trunk displacement might be the speed of the movement in the three parts of the task. When mean wrist velocity was highest (in the middle part of the substance-transporting phase), the trunk displacement was smallest. In line with this, correlations between mean wrist velocity and trunk displacement were mainly negative in both groups (10 of 12 control participants, and 8 of 10 tetraparetic participants), indicating there was a clear tendency for increased trunk use with lower movement speed. A combination of these findings might, at least partly, explain why individuals with spastic tetraparesis displace their trunk more than healthy individuals, and also why trunk displacement increases when accuracy demands increase. If a task becomes more complex (e.g. as a result of motor and somatosensory problems or higher accuracy demands or both), the movement is performed more slowly. As a consequence of that, the trunk is recruited more (see also Rosenbaum et al. 1991, 1995; Vaughan et al. 1996; Wang and Stelmach 2001). A note of caution must be made here. The correlation coefficients that we found were not very large and we even found a positive correlation for one participant in each group.

Therefore, variations in movement speed did not exclusively account for variations in trunk involvement. However, it has to be pointed out that this experiment was not designed to test this specific hypothesis, as we did not explicitly manipulate movement speed. To be able to draw more definite conclusions on this matter, a wider range of velocities should be investigated. Are there alternative explanations for the increased trunk involvement? One factor that might have influenced trunk involvement is the emptying strategy that participants adopted. The emptying strategy entails both the way in which the spoon is oriented before emptying (cf. Roby-Brami 1997) and, especially relevant for the large bowl, the location at which the spoon is emptied (e.g. close to the front edge of the bowl). The different emptying strategies were reflected by the distance that was covered by the wrist relative to the transport distance of the spoon. Most participants used precision grips, which make it easier to extend the bowl of the spoon further. The distance that was covered by the wrist relative to the transport distance was on average 67%, indicating that the participants used the length of the stem of the spoon to shorten the distance that had to be covered by the wrist. Importantly, no difference in emptying strategy was found between the two groups, although, in general, the relative wrist displacement was larger when water was transported and when the bowl was small. Nevertheless, these findings can only partly account for the larger trunk displacement in these conditions, because the trunk displacement was not necessary to empty the spoon into the bowl, as was assessed prior to the start of the experiment. Combining this finding with the observed relationship between speed and trunk displacement leads us to the following explanation: when larger distances are covered by the wrist in the more complex conditions (small bowl, water), participants move their hand for a longer time at a lower velocity, leading to a larger trunk displacement. Another factor that may have influenced trunk involvement is the increased cocontraction of agonist/antagonist muscle pairs, which is a typical symptom accompanying spasticity in individuals with CP (O’Sullivan et al. 1998). As a result of the increased limb stiffness, the functional range of motion during task performance in the elbow and shoulder joints might be reduced. Increasing the displacement of the trunk might compensate for this decreased functional range of motion. Indeed, it was recently shown in a healthy subject population that cocontraction at the elbow and shoulder increases when pointing movements have to be made towards small targets rather than large ones (Gribble et al. 2003). Gribble and colleagues suggested that cocontraction might be a strategy employed by the motor system to increase arm movement accuracy. An electromyographic study is currently underway in our lab to examine whether the same strategy is used by individuals with spasticity. A final factor for the increased trunk use may be sought in the need to reduce variability of the end-effector trajectory, which is most prominent for high accuracy tasks (cf. Cirstea and Levin 2000). Our finding that the

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displacement of the trunk was largest in the tetraparetic participants in the final part of the movement might provide evidence for this since the instability of the endeffector is assumed to be largest near the end of the movement. In this final part, the elbow is most extended and, due to the muscular weakness in these individuals, movements of the end effector may then become more variable. However, with the present set-up we could not draw any definite conclusion with respect to this point and further research is needed to examine whether fixating the trunk will increase the end-effector dysfluency in this group. Summing up, similar to healthy people, tetraparetic individuals flexibly tune the amount of trunk involvement to variations in accuracy demands, despite the somatosensory and motor problems that these individuals have to cope with. An increased trunk displacement was found when accuracy constraints of the task were higher. We therefore conclude that the increased trunk involvement in individuals with mild tetraparesis as a consequence of CP should not be regarded as a primary symptom of the disorder.
Acknowledgements We thank all volunteers who participated in this study, Marcel Mutsaarts for his assistance in carrying out the experiment, and Chris Bouwhuisen for his technical support. This research was supported by a grant awarded by The Netherlands Organization for Scientific Research (NWO) to the second author for the research project ‘Adaptation in movement disorder’.

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