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Development of unimanual versus bimanual task performance in an isometric task
Human Movement Science 23 (2004) 461–474 www.elsevier.com/locate/humov
Development of unimanual versus bimanual task performance in an isometric task Y. Westenberg
a,b
, B.C.M. Smits-Engelsman J. Duysens b,e,f
a,c,d,*
,
a
c
Avans+, University for professionals, P.O. Box 2087, 4800 CB Breda, The Netherlands b SMK-Research, P.O. Box 9011, 6500 GM Nijmegen, The Netherlands Nijmegen Institute for Cognition and Information (NICI), Radboud University of Nijmegen, P.O. Box 9104, 6500 HE Nijmegen, The Netherlands d Motor Control Lab, Department of Kinesiology, K.U. Leuven, Belgium e Department of Rehabilitation, Radboud University of Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands f Department of Medical and Biophysics, Radboud University of Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
Abstract Sixty-three children between 5 and 12 years of age and 15 adults performed a unimanual and a bimanual isometric force task. The performance of the preferred hand in the unimanual task was compared to the performance of the preferred hand in the bimanual task. It was hypothesized that in the bimanual task the absolute error will be higher, there will be more irregularity and the participants will need more time due to the additional effort from the central nervous system, especially with respect to the communication between the hemispheres. Furthermore, in younger children bimanual force variability was expected to be higher due to developmental aspects concerning callosal maturation and attention. It was found that with respect to force generation the preferred hand was not affected by bilateral isometric force generation, but with respect to force regulation it was. The coefficient of variation (CV) of the
* Corresponding author. Address: Nijmegen Institute for Cognition and Information (NICI), Radboud University of Nijmegen, P.O. Box 9104, 6500 HE Nijmegen, The Netherlands. Tel.: +31 24 3615754/76 5238774; fax: +31 24 3616066. E-mail address: [email protected] (B.C.M. Smits-Engelsman).
0167-9457/$ - see front matter Ó 2004 Published by Elsevier B.V. doi:10.1016/j.humov.2004.08.018
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force was 34% larger in the bimanual task as compared to the unimanual task. For the time to target force, the increase was 28%. With repetition of the trials the CV decreased in the bimanual task, but only in the youngest age group. During development there was no change in absolute error, yet there was a major reduction in force variability in the bimanual task. It is suggested that improvement in interhemispheric communication and in the ability to focus attention plays a role in the decrease in variability with age. Ó 2004 Published by Elsevier B.V. PsycINFO classification: 2330; 2520; 2820 Keywords: Bimanual; Force variability; Motor development
1. Introduction When comparing a bimanual task to its unimanual counterpart, the former is more attention demanding and often performed less accurately and consistently than the latter. When measuring the maximal voluntary contraction force (MVC) of finger muscles in adults, Li, Danion, Latash, Li, and Zatsiorsky (2000) and Zijdewind and Kernell (2001) found a Ôbilateral deficitÕ. A bilateral deficit means that the MVC of simultaneous bilateral exertion is smaller than the sum of the unilateral exertions. The magnitude of the bilateral deficit found varied from 5% for the FDI (first dorsal interosseous) muscles (Zijdewind & Kernell, 2001) to 27% for finger flexor muscles (Li et al., 2000) and depended on whether the task was symmetric or asymmetric. A symmetric task was defined as a task in which the same combination of fingers in both hands is used. The more symmetric the task, the less was the bilateral deficit (Li et al., 2000). Again in adults Morrison and Newell (1998) found a bilateral deficit for the regularity of force output. The authors found that in a bimanual isometric force task the regularity of the force output of each index finger considered separately was greater than that of the total force of the unimanual task. In children Harbst, Lazarus, and Whitall (2000) found that bimanual tasks requiring in-phase activation between the hands were performed more accurately, more quickly, and with less force and timing variability than tasks requiring anti-phase actions and/or different levels of force to be produced simultaneously. Similarly, a bilateral deficit was found in reaction time tasks where the reaction times in simultaneous bilateral index finger flexions were longer than in unilateral conditions in adult participants (Taniguchi, Burle, Vidal, & Bonnet, 2001). Taniguchi et al. (2001) found an EEG correlate of the bilateral deficit. For the right hand (in right-handed persons), the activation of the sensorimotor area directly involved in the voluntary control was weaker for bilateral than for unilateral contralateral responses. According to the authors this may be due to the crossing effect of mutual interhemispheric inhibition. Other authors suggest that the control of timing, in bimanual tasks may be more tightly coupled in the motor system than the control of force (Harbst et al., 2000; Inui & Hatta, 2002; Rinkenauer, Ulrich, & Wing, 2001). As an inverse of the bilateral deficit there is the possibility of motor overflow in bimanual tasks (Li et al., 2000). Motor overflow, also called mirror movement, is
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the involuntary movement in the contralateral extremity that accompanies an intended movement (De-Guise & Lassonde, 2001). Motor overflow may lead to higher forces on bilateral exertions than on summed unilateral exertions. During maximal force production tasks in the study of Li et al. (2000), using two hands simultaneously force deficit was more likely to occur than in submaximal force production tasks, since it may lead to a combination of motor overflow and bilateral deficit effects (Li et al., 2000). For regularity of force output, motor overflow may have the same effect as bilateral deficit does. If in the bimanual task the irregularity of one hand leads to extra irregularity in the other hand, regularity of force output in the bimanual task will be less than in the unimanual task. Hence in bimanual force production tasks motor overflow and bilateral deficit may have an opposite effect for force generation, but they may reinforce each other for irregularity of force output. What are the brain structures involved in bimanual skills? In normal adults, Andres et al. (1999) proposed that the increase in task-related coherence in the early learning phase of bimanual skill acquisition reflected changes in interhemispheric communication that are especially related to bimanual learning and may be transmitted through the corpus callosum. In a kinematical analysis of bimanual in-phase and anti-phase movements, Stephan et al. (1999) revealed an impairment of both the temporal adjustment and the independence of movements between the hands in two adult patients with midline tumors. Lateralisation is also important. In right-handed adults a substantial left hemispheric involvement was found in the coordination of bimanual tasks (Debaere et al., 2001; Gutnik & Hyland, 1997; Ja¨ncke et al., 1998). Another aspect of motor overflow or mirror movements is that motor overflow is depending on age. Younger children exhibit greater associated movements in the contralateral hand during unimanual tasks (Abercrombie, Lindon, & Tyson, 1964; Cohen, Taft, Mahadeviah, & Birch, 1967; Ja¨ncke et al., 1998; Wolff, Gunnoe, & Cohen, 1983), although associated movements do not completely disappear in adulthood (Zijdewind & Kernell, 2001). The explanation for the developmental differences may be found in the development of interhemispheric communication. Fagard, Hardy-Le´ger, Kervella, and Marks (2001) stated that in children, at least till the age of 10 years, improved interhemispheric communication contributed to progress in bimanual coordination in line drawing tasks, especially those which require resisting the attraction of mirror movements. De-Guise and Lassonde (2001) found that, before the age of twelve, children could not learn a procedural skill that required bihemispheric integration during its acquisition. The most plausible explanation for this finding is a difference in the degree of callosal maturation between the age groups. On the other hand, Milling-Smith, Eunson, and Walsh (2002) did not find differences between 8-year-old children and adults with respect to in-phase skills such as needed to synchronize movements of two fingers when making or breaking contact. It seems that for the synchronization between the hands needed for in-phase skills the development has reached a plateau before the age of eight. The interest in this study was to look at the differences in using the preferred (right) hand in a single-handed isometric force task compared to using the preferred (right) hand in a two-handed isometric symmetric force task. It was hypothesized that there would be a higher absolute error and more irregularity, and that the
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participants would need more time in the bimanual task. This is expected because participants have to regulate two forces and are getting visual feedback from two cursors at the same time. Doing so will demand additional effort from the central nervous system, especially with respect to the communication between the hemispheres. Furthermore in younger children the movement quality is likely to be lower due to developmental aspects concerning callosal maturation and attention. Since variability of force is related to absolute levels of force, in this study the force control development is described in outcome variables relative to MVC and over a large range of force levels. An experiment was designed in which isometric force had to be maintained at five relative force levels (Smits-Engelsman, Westenberg, & Duysens, 2003).
2. Method 2.1. Participants Seventy-six children of three primary schools were approached to take part in the study. One of the inclusion criteria was right-handedness on annettÕs (1970) test for children under 9 years of age. The mean score on AnnettÕs test was 8.3 (SD 1.8), no significant differences between 5 and 6 year olds and 7 and 8 year olds were found. Furthermore, no developmental delay, motor problems or muscle diseases should be present. For all children this was confirmed by scores above the 5th percentile on the Manual dexterity subscore of the Movement ABC (Henderson & Sugden, 1992; Smits-Engelsman, 1998). After checking for the inclusion criteria, 63 children (mean age 8.5 year, SD 2.34 year, mean score on manual dexterity part of the MABC 1.79, SD 1.75) entered the study, 29 boys (46%) and 34 girls (54%) belonging to four age groups. Age group 1 (5–6 year olds) consisted of 18 children, age group 2 (7–8 year olds) consisted of 12 children, age group 3 (9–10 year olds) consisted of 16 children and age group 4 (11–12 year olds) consisted of 17 children. Furthermore, 15 adults (mean age 24.5, SD 2.22), 7 male and 8 female, entered the study (Table 1). All parents, children and adults gave a written consent to participate in the study. 1 2.2. Procedure and tasks All 78 participants had to perform two randomised isometric force tasks. One task had to be performed with the index finger of the preferred hand and the other task with the index fingers of both hands. To perform the isometric force task, participants were seated on an adjustable chair in front of a monitor, which was placed at eye level. On this monitor one yellow cursor was displayed at the side of the preferred hand in case of the one-handed task. To perform the isometric force task with 1
The children in this study were recruited as control children for a study on age and therapy related changes in cerebral palsy approved by the Medical Ethic Committee of Stichting Revalidatiecentra Limburg (SRL).
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Table 1 ParticipantÕs characteristics Age group
Age (years)
1 2 3 4 5
5–6 7–8 9–10 11–12 20–30
Gender Male
Total
Total number Female
8 6 7 8 7
10 6 9 9 8
18 12 16 17 15
36
42
78
both hands two yellow cursors were displayed on the monitor, one at the left side for the left hand and one at the right side for the right-hand (Fig. 1). Participants could control the vertical position of the cursor by applying force, with their index finger of the preferred (right) hand or with both index fingers, onto the end of a (two) lever(s). The harder they pressed, the higher the cursor(s) moved on the monitor. The participants were only allowed to use the flexor muscles of their index fingers. The other fingers, and their forearms, had to rest on the table. The aluminium levers transmitted the force onto a force transducer. On each trial the participants had to move the cursor(s) towards a target (grey bar) as fast as possible after the start signal, a short tone. When the cursor(s) reached this target another short tone indicated that a 10-s recording hold period started. During these 10 s the participant was required to keep the cursor(s) as steadily as possible over the position of the target. The instructions for the bimanual task were to keep eye on both the cursors. At the end of the 10 s a third tone sounded as a stop signal. Before the experiment started the maximum voluntary contraction (MVC) of the index flexor muscles was measured. The participants were required to keep the
Fig. 1. Experimental set-up: Example of a bimanual task, showing apparatus and monitor on which the grey bar can be seen at the 48% level and the cursors (beneath the grey bar) representing the generated force of the left and the right hand, respectively.
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yellow cursor(s) at the same height as the red cursor(s), which moved slowly up the screen indicating a steadily increasing force level. The level rose to 50 N in 30 s. The participants were instructed to let go when they felt that they could not attain the required force level any longer. This force level was taken as a measure of MVC. In the experiment six different levels of constant force were recorded for each task, ranging from 0% to 60% of MVC. The MVC was used to program the target force or the force required at 0%, 12%, 24%, 36%, 48% and 60% of the MVC for each participant. The feedback was adjusted so that 0% of MVC was exactly at the bottom of the screen of the monitor and 60% was at the top. Each force level (0%, 12%, 24%, 36%, 48% and 60%) was measured five times giving a total of thirty trials per participant. The 0% condition was used to measure and correct for equipment noise. Before each task a training session was given. The total of thirty trials took about 25 min. All trials were completely randomised for each participant. To measure the force exerted by the finger a high-quality strain gauge (Sokki Kenkyujo; type CLS-20KA) was used. This gauge is temperature compensated and highly linear. An amplifier (Burster; type 9154) delivered its output to a 12-bit AD-converter (DAS800). The computer sampled the signal at a rate of 1000 Hz. To provide the participant with stable feedback the signal was first reduced in frequency to 100 Hz and then filtered using a digital low-pass Finite-Impulse Response filter with a transition band from 5 to 15 Hz. This highly filtered signal was used to update the vertical positions of the cursor on the monitor sixty times a second. (Note that for data-analyses the raw signal was used both for the hold periods and for the time prior to and following the hold period.) In case of the bimanual task, force was recorded for the preferred and the nonpreferred hand. In this study only the data of the preferred hand were computed. The mean generated force, absolute error, variables measuring force regulation (standard deviation (SD), coefficient of variation (CV)) and time to target force were computed for each recording. The generated force (N) was computed as the median force level that the participant actually generated per trial. Medians were used to filter for outliers. In the subsequent analysis means per condition were calculated. The absolute error was defined as the absolute difference score between the target force and the generated force. SD was calculated over each hold period of 10 s. The Coefficient of Variation was defined as the mean generated force divided by the SD and multiplied by 100%. Time to target force was defined as the time (s) from the starting signal till the moment the grey target bar was reached. The dependent variables were evaluated by means of a General Linear Model, Repeated Measures design. For all dependent variables the interaction effect of gender and task was computed. Within-subject variables were task (2 levels), percentage of MVC (5 force levels) and repetitions (5). Age group (5 levels) was entered as between-subject variable. The two levels of the variable task consisted of a unimanual level and a bimanual level in order to compare the achievements of the preferred (right) hand in the unimanual task with the achievements of the preferred hand in the bimanual task. Alpha was set at 5% (two-tailed). Only the significant effects will be reported.
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3. Results 3.1. Force generation: MVC and mean generated force Significant differences in force generation between the unimanual and bimanual task were not found, meaning that the preferred hand performed comparable in the unimanual and in the bimanual task (Fig. 2). For MVC the means were: unimanual 24.22 N, bimanual 23.90 N, for mean generated force the means were: unimanual 8.49 N, bimanual 8.30 N. There was no developmental trend in this lack of significant difference in force generation, indicating that children made the same difference in force generation between a unimanual and a bimanual task as adults did. 3.2. Absolute error (AE) All participants were able to perform the requested tasks. Overall the AE during this experiment was low. Taken over all 3900 trials, the average deviation of the actual produced force from the target force (mean 8.66 N) was small, namely only 0.31 N, or about 3.6%. As expected, the AE in the bimanual task was higher than in the unimanual task (F(1, 73) = 12.691, p = 0.001). The deviation from the target force was 45% higher in the bimanual task (mean bimanual: 0.368 N, mean unimanual: 0.254 N). No developmental trend in differences between the unimanual and bimanual task was found for AE. 3.3. Force regulation: SD and CV
Difference between the tasks (%)
For force regulation it did make a difference if the task was completed with one or two hands. Both aspects of force regulation, SD and, CV, showed highly significant main effects of task (F(1, 73) = 9.246, p = 0.003, F(1, 73) = 14.410, p = 0.000, respectively) (Fig. 2). In both cases the scores on the bimanual task were higher, meaning that the participants produced more variable force in the bimanual task than in the 50 40 30 20 10 0 MVC
Force
SD *
CV *
Time *
AE *
-10
Fig. 2. Task differences: Bimanual task minus unimanual task for maximal voluntary contraction force (MVC, 1.3%), generated force (force, 2.2%), SD (20.8%), CV (33.8%), time to reach the target force (time, 28.2%) and absolute error (AE, 44.8%). * = significant, p < 0.005.
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unimanual task. The means were for SD: unimanual 0.536 N, bimanual 0.647 N, for CV: unimanual 7.700, bimanual 10.300. The difference in SD between the unimanual and bimanual task became smaller with repetition of the task, indicating that there was a learning effect in the twohanded task, in contrast with the single-handed task, as evaluated by the factor repetition (F(4, 292) = 3.418, p = 0.009). The differences between the unimanual and bimanual tasks in repetition 3 and 5 were still significant (F(1, 73) = 4.278, p = 0.042), while this was no longer the case for the differences between 4 and 5. Different patterns emerged for the age groups as shown by the interaction effect of repetition, task and age group on SD (F(16, 1168) = 1.895, p = 0.021). The analysis revealed that the learning effect was clearly age dependent, as is shown in Fig. 3. The greatest learning effect was seen in the youngest children (Fig. 3). This was confirmed by the fact that only in the youngest group the effect of task and repetition was significant (F(4, 68) = 4.3838, p = 0.002). Hence only the children in the youngest group showed a learning effect in the bimanual task. The results were basically similar for CV (interaction effect of repetition, task and age group on CV: F(16, 1168) = 2.141, p = 0.007). As for SD, the effect of task and repetition was significant only in the youngest age group (F(4, 68) = 5.311, p = 0.001), but in contrast with the findings on SD the effect of task was still significant in repetition 5 for age group 1 (F(1, 89) = 4.208, p = 0.043). With age the variability in force decreased. This change is best illustrated using CV, since then the difference in force levels is accounted for. As is depicted in Fig. 4, based on CV the younger children showed significantly greater differences between the unimanual and bimanual task than older children (interaction effect of task and age-group on CV: F(4, 292) = 3.197, p = 0.018). It can be seen that from 9–10 years on the difference between the unimanual and bimanual task becomes
Fig. 3. Differences between the age groups on absolute force variability (SD). SD of the Generated Force in the unimanual and the bimanual task for each Repetition (1–5) and per age group.
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25 *
20 CV (%)
15 *
10 5 0
5 and 6
7 and 8
unimanual
14.70
11.02
9 and 10 11 and 12 20 till 30 5.31
4.63
2.68
bimanual
20.46
16.61
6.58
5.35
2.63
Age groups (years)
Fig. 4. Developmental trend in relative force variability (CV). CV of the generated force in the unimanual and the bimanual task per age group with standard error. * = significant, p < 0.005.
smaller, so the largest part of development takes place before 11 years of age (age group 2–3: F(1, 26) = 5.175, p = 0.031) (Fig. 4). However, the significant difference between 9–10 year olds and adults proves that development is not yet complete at 10 years of age (age group 3–5: F(1, 29) = 4.467, p = 0.043) (Fig. 4). 3.4. Time to target force
Time difference (s)
Time difference (s)
An interaction effect for gender and task was found. Although there were no differences between male and female participants in the one-handed task, in the 5 and 6 years
7 and 8 years
11 and 12 years
20 till 30 years
9 and 10 years
2.00
1.00
0.00
Force level (%) 2.00
12 24
1.00
36 48 60
0.00
Dot/Lines show Means 1
2
3
Repetition
4
5
1
2
3
4
5
Repetition
Fig. 5. Developmental trend in time to reach the target force. The difference in time to reach the target force between the unimanual and bimanual task, for each force level (% of MVC), repetition (1–5) and age group.
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two-handed task male participants needed 15.2% more time to target force than female participants (F(1, 76) = 4.822, p = 0.031). A highly significant main effect of task was found for time to target force (F(1, 73) = 43.095, p = 0.000). The scores on the bimanual task were higher, meaning that the participants needed more time to target force in the bimanual task than in the unimanual task (unimanual 2.387 s, bimanual 3.060 s). The differences between the unimanual and bimanual conditions were larger when the force levels were higher, 21%, 23%, 25%, 34% and 34%, respectively, for the increasing force levels (F(4, 292) = 9.629, p = 0.000). In Fig. 5 one can see that after the age of 8 years children gradually show less variability in each repetition and for each force level and grow to more adult values (Interaction effect of repetition, force level, task and age-group on time to target force: F(64, 4672) = 1.390, p = 0.025). However, the difference between the tasks was still significant for adults (effect of task on time to target force for adults: F(1, 14) = 29.530, p = 0.000).
4. Discussion 4.1. Force generation, absolute error and force variability In the present study the MVC and the mean generated force for the right hand were not significantly different in the unimanual and the bimanual task. Other authors did find a bilateral deficit in measuring MVC of finger flexor muscles (Li et al., 2000; Zijdewind & Kernell, 2001). However, the focus of the present study was slightly different. Other groups defined bilateral deficit as the difference between the combined MVC of the bimanual task and the sum of the MVCs during the unimanual task (Li et al., 2000), while in this study the MVC of the preferred hand in the unimanual task was compared to the MVC of the preferred hand in the bimanual task. Differences in bilateral deficit could appear when the forces generated by the preferred and non-preferred hand in the bimanual task were different, but in none of the three studies this difference was significant. Furthermore, there was a high degree of symmetry of the bimanual task in the present study. Gutnik and Hyland (1997) already found that better spatial symmetry in limb movement was achieved when both hands employed similar within-hand strategies, as was the case in the present study. Other authors confirm the fact that the bilateral deficit is less in a symmetrical bimanual task compared to an asymmetrical task (Li et al., 2000). In the study of Li et al. (2000) different combinations of fingers within a hand were used, while in the present study the participants had to generate force only with the index fingers, which may be regarded as a simpler task. Simpler tasks may be less sensitive to bilateral deficit. Li et al. (2000) also found that in asymmetrical tasks more complexity (using fewer fingers within the hand and more fingers in the other hand) led to more bilateral deficit. The other study that revealed a bilateral deficit in force generation was only based on 5 adult participants (Zijdewind & Kernell, 2001). The assumption of Li et al. (2000) that sub-maximal force production tasks may lead to a combination of bilateral deficit and motor overflow seem to be confirmed
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by our findings. Since there was no significant difference between the unimanual and bimanual task on mean generated force the conclusion could be that the opposite effect of bilateral deficit and motor overflow may have led to this lack of difference. Nevertheless, the bimanual task demanded more additional effort than the unimanual task. This was also confirmed by the fact that the AE was higher in the bimanual task. Participants needed more time to reach the target force and showed more absolute (SD) and relative (CV) force variability in the bimanual task. These differences may reflect a rise in coordination effort in the bimanual task. These findings seem to confirm the findings of other authors, although they used different approaches. Morrison and Newell (1998) looked, by means of cross correlations on ApEn scores (amplitude and regularity of the force signal), at the coordination between hands in a bimanual isometric force task. They found that the regularity of the force output of each index finger considered separately was greater than that of the total force (Morrison & Newell, 1998). Taniguchi et al. (2001) used reaction time tasks and simultaneously measured the brain electrical activity. They reported that there was a deficit in reaction time for the bilateral response for the right index finger movement, both in adults and children (Taniguchi et al., 2001). The latter type of findings has led some authors to suggest that the timing of bimanual tasks is more tightly coupled than the control of force (for evidence for the dominance of temporal coupling over force coupling in bimanual tasks see Harbst et al., 2000; Inui & Hatta, 2002; Rinkenauer et al., 2001). The present results do not support this contention since the effects of task on the time to target force and on SD and CV all were highly significant for the whole group of participants. Admittedly, however, if only the adults were considered, the effect on the temporal variables was clearer than on the force control variables in the bimanual task. 4.2. Development The differences in AE between the uni- and bimanual task were constant with age. Milling-Smith et al. (2002) found that children reached a plateau before the age of eight measuring timing errors. Nevertheless, CV showed a clear developmental trend since for younger children the differences between the unimanual and bimanual task were greater than for older children (Fig. 5). So, CV seems to be more sensitive to measure development than error. The greatest steps in development were made before the age of about 10 years. This is in accordance with the assumption of Fagard et al. (2001) that in children improvement of interhemispheric communication, at least till the age of 10 years, contributes to progress in bimanual coordination. This development is faster as expected from some other studies. For example, De-Guise and Lassonde (2001) found that before the age of twelve, children could not learn a procedural skill that required bihemispheric integration during its acquisition. However, this was based on learning more difficult tasks namely asymmetrical out of phase skills. Hence, the difference in tasks may be a plausible explanation for the difference in development, although even in the present study development is not quite complete at 10 years of age.
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Several factors may contribute to the large variability found in many of the variables at young age. The immaturity of the neural substrate is a first candidate but one should also consider the lack of concentration often observed in young children. This lack of attention may explain the capricious patterns in SD and CV and in the time needed to target force at least till the age of 10 years. Temprado, Zanone, Monno, and Laurent (2001) stated that attention plays an important role in modifying the coupling between the limbs. In the present study it was found that the learning effect only concerned the youngest children. In this group a plateau in performance was reached at repetition 4, yet there was still a significant difference between the unimanual and bimanual task in repetition 5. It remains to be seen whether this effect would stay when the task was repeated more often. The second age group (7 and 8 years) showed no effect of repetition but did exhibit a clear overall increase in force variability in the bimanual task as compared to the unimanual version. From developmental studies it is known that changes in spatial accuracy and temporal variables show a non-monotonic profile with a temporary decrease in performance around 7–8 years of age (Bard, Hay, & Fleury, 1990; Hay, Bard, Fleury, & Teasdale, 1991). This might reflect qualitative changes in the movement control processes. With respect to the younger group, they showed better results in the unimanual task but not yet in the bimanual task. In age groups 3, 4 and 5 the differences in absolute force variability between the tasks rapidly decreased. 4.3. Conclusions In conclusion, it was found that the preferred hand was not affected by bilateral execution of an isometric task with respect to force generation (MVC and mean generated force). Although the task was simple, force control, as evaluated by absolute (SD) and relative (CV) force variability, was more difficult, and time to target force was longer in a bimanual isometric force task than in a unimanual task. Despite the difficulty, only the youngest children showed a learning effect. Developmental changes in force control were found at least till the age of ten, although adult values were not yet reached then. It seems likely that improvement in interhemispheric communication and in the ability to focus attention plays a role.
Acknowledgments We wish to thank all the children and their parents and all the adults for their commitment and willingness to participate in this study, and Mr. Peter de Jong for developing the OASIS software needed in this experiment.
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References Abercrombie, M. L. J., Lindon, R. L., & Tyson, M. G. (1964). Associated movements in physically handicapped children. Developmental Medicine and Child Neurology, 6, 573–580. Andres, F. G., Mima, T., Schulman, E., Dichgans, J., Hallett, M., & Gerloff, C. (1999). Functional coupling of human cortical sensorimotor areas during bimanual skill acquisition. Brain, 122, 855–870. Annett, M. (1970). A classification of hand preference by association analysis. British Journal of Psychology, 61, 303–321. Bard, C., Hay, L., & Fleury, M. (1990). Timing and accuracy of visually directed movements in children: Control of direction and amplitude components. Journal of Experimental Child Psychology, 50, 102–118. Cohen, H. J., Taft, L. T., Mahadeviah, M. S., & Birch, H. G. (1967). Developmental changes in overflow in normal and aberrantly functioning children. Journal of Paediatrics, 71, 39–47. Debaere, F., Swinnen, S. P., Be´atse, E., Sunaert, S., Vanhecke, P., & Duysens, J. (2001). Brain areas involved in interlimb coordination: A distributed network. NeuroImage, 14, 947–958. De-Guise, E., & Lassonde, M. (2001). Callosal contribution to procedural learning in children. Developmental Neuropsychology, 19, 253–272. Fagard, J., Hardy-Le´ger, I., Kervella, C., & Marks, A. (2001). Changes in interhemispheric transfer rate and the development of bimanual coordination during childhood. Journal of Experimental Child Psychology, 80, 1–22. Gutnik, B., & Hyland, B. (1997). Spatial coordination in a bimanual task related to regular switching of movement vectors. Perceptual and Motor Skills, 84, 371–384. Harbst, K. B., Lazarus, J. A., & Whitall, J. (2000). Accuracy of dynamic isometric force production: The influence of age and bimanual activation patters. Motor Control, 4, 232–256. Hay, L., Bard, C., Fleury, M., & Teasdale, N. (1991). Kinematics of aiming in direction and amplitude: A developmental study. Acta Psychologica, 77, 203–215. Henderson, S. E., & Sugden, D. A. (1992). The movement assessment battery for children. San Antonio, IL: The Psychological Corporation. Inui, N., & Hatta, H. (2002). Asymmetric control of force and symmetric control of timing in bimanual finger tapping. Human Movement Sciences, 21, 131–146. Ja¨ncke, J., Peters, M., Schlaug, G., Posse, S., Steinmetz, H., & Mullergartner, H. W. (1998). Differential magnetic resonance signal change in human sensorimotor cortex to finger movements of different rate of the dominant and subdominant hand. Cognitive Brain Research, 6, 279–284. Li, S., Danion, F., Latash, M. L., Li, Z.-M., & Zatsiorsky, V. M. (2000). Characteristics of finger force production during one- and two-handed tasks. Human Movement Science, 19, 897–923. Milling-Smith, O., Eunson, P., & Walsh, E. G. (2002). Maturation of finger-synchronization skills. Developmental Medicine and Child Neurology, 44, 181–184. Morrison, S., & Newell, K. M. (1998). Interlimb coordination as a function of isometric force output. Journal of Motor Behavior, 30, 323–342. Rinkenauer, G., Ulrich, R., & Wing, A. M. (2001). Brief manual force pulses: Correlations between the hands in force and time. Journal of Experimental Psychology: Human Perception and Performance, 27, 1485–1497. Smits-Engelsman, B. C. M. (1998). Movement assessment battery for children: Dutch manual. Lisse, IL: Swets en Zeitlinger B.V.. Smits-Engelsman, B. C. M., Westenberg, Y., & Duysens, J. (2003). Development of isometric force and force control in children. Cognitive Brain Research, 17, 68–74. Stephan, K. M., Binkofski, F., Halsbamd, U., Dohle, C., Wunderlich, G., Schnitzler, A., Tass, P., Posse, S., Herzog, H., Sturm, V., Zilles, K., Seitz, R. J., & Freund, H. J. (1999). The role of ventral medial wall motor areas in bimanual co-ordination: A combined lesion and activation study. Brain, 122, 351–368. Taniguchi, Y., Burle, B., Vidal, F., & Bonnet, M. (2001). Deficit in motor cortical activity for simultaneous bimanual responses. Experimental Brain Research, 137, 259–268.
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Temprado, J. J., Zanone, P. G., Monno, A., & Laurent, M. (2001). A dynamical framework to understand performance trade-offs and interference in dual tasks. Journal of Experimental Psychology: Human Perception and Performance, 27, 1303–1313. Wolff, P. H., Gunnoe, C. E., & Cohen, C. (1983). Associated movements as a measure of developmental age. Developmental Medicine and Child Neurology, 25, 417–429. Zijdewind, I., & Kernell, D. (2001). Bilateral interactions during contractions of intrinsic hand muscles. Journal of Neurophysiology, 85, 1907–1913.
Development of unimanual versus bimanual task performance in an isometric task Y. Westenberg
a,b
, B.C.M. Smits-Engelsman J. Duysens b,e,f
a,c,d,*
,
a
c
Avans+, University for professionals, P.O. Box 2087, 4800 CB Breda, The Netherlands b SMK-Research, P.O. Box 9011, 6500 GM Nijmegen, The Netherlands Nijmegen Institute for Cognition and Information (NICI), Radboud University of Nijmegen, P.O. Box 9104, 6500 HE Nijmegen, The Netherlands d Motor Control Lab, Department of Kinesiology, K.U. Leuven, Belgium e Department of Rehabilitation, Radboud University of Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands f Department of Medical and Biophysics, Radboud University of Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
Abstract Sixty-three children between 5 and 12 years of age and 15 adults performed a unimanual and a bimanual isometric force task. The performance of the preferred hand in the unimanual task was compared to the performance of the preferred hand in the bimanual task. It was hypothesized that in the bimanual task the absolute error will be higher, there will be more irregularity and the participants will need more time due to the additional effort from the central nervous system, especially with respect to the communication between the hemispheres. Furthermore, in younger children bimanual force variability was expected to be higher due to developmental aspects concerning callosal maturation and attention. It was found that with respect to force generation the preferred hand was not affected by bilateral isometric force generation, but with respect to force regulation it was. The coefficient of variation (CV) of the
* Corresponding author. Address: Nijmegen Institute for Cognition and Information (NICI), Radboud University of Nijmegen, P.O. Box 9104, 6500 HE Nijmegen, The Netherlands. Tel.: +31 24 3615754/76 5238774; fax: +31 24 3616066. E-mail address: [email protected] (B.C.M. Smits-Engelsman).
0167-9457/$ - see front matter Ó 2004 Published by Elsevier B.V. doi:10.1016/j.humov.2004.08.018
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force was 34% larger in the bimanual task as compared to the unimanual task. For the time to target force, the increase was 28%. With repetition of the trials the CV decreased in the bimanual task, but only in the youngest age group. During development there was no change in absolute error, yet there was a major reduction in force variability in the bimanual task. It is suggested that improvement in interhemispheric communication and in the ability to focus attention plays a role in the decrease in variability with age. Ó 2004 Published by Elsevier B.V. PsycINFO classification: 2330; 2520; 2820 Keywords: Bimanual; Force variability; Motor development
1. Introduction When comparing a bimanual task to its unimanual counterpart, the former is more attention demanding and often performed less accurately and consistently than the latter. When measuring the maximal voluntary contraction force (MVC) of finger muscles in adults, Li, Danion, Latash, Li, and Zatsiorsky (2000) and Zijdewind and Kernell (2001) found a Ôbilateral deficitÕ. A bilateral deficit means that the MVC of simultaneous bilateral exertion is smaller than the sum of the unilateral exertions. The magnitude of the bilateral deficit found varied from 5% for the FDI (first dorsal interosseous) muscles (Zijdewind & Kernell, 2001) to 27% for finger flexor muscles (Li et al., 2000) and depended on whether the task was symmetric or asymmetric. A symmetric task was defined as a task in which the same combination of fingers in both hands is used. The more symmetric the task, the less was the bilateral deficit (Li et al., 2000). Again in adults Morrison and Newell (1998) found a bilateral deficit for the regularity of force output. The authors found that in a bimanual isometric force task the regularity of the force output of each index finger considered separately was greater than that of the total force of the unimanual task. In children Harbst, Lazarus, and Whitall (2000) found that bimanual tasks requiring in-phase activation between the hands were performed more accurately, more quickly, and with less force and timing variability than tasks requiring anti-phase actions and/or different levels of force to be produced simultaneously. Similarly, a bilateral deficit was found in reaction time tasks where the reaction times in simultaneous bilateral index finger flexions were longer than in unilateral conditions in adult participants (Taniguchi, Burle, Vidal, & Bonnet, 2001). Taniguchi et al. (2001) found an EEG correlate of the bilateral deficit. For the right hand (in right-handed persons), the activation of the sensorimotor area directly involved in the voluntary control was weaker for bilateral than for unilateral contralateral responses. According to the authors this may be due to the crossing effect of mutual interhemispheric inhibition. Other authors suggest that the control of timing, in bimanual tasks may be more tightly coupled in the motor system than the control of force (Harbst et al., 2000; Inui & Hatta, 2002; Rinkenauer, Ulrich, & Wing, 2001). As an inverse of the bilateral deficit there is the possibility of motor overflow in bimanual tasks (Li et al., 2000). Motor overflow, also called mirror movement, is
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the involuntary movement in the contralateral extremity that accompanies an intended movement (De-Guise & Lassonde, 2001). Motor overflow may lead to higher forces on bilateral exertions than on summed unilateral exertions. During maximal force production tasks in the study of Li et al. (2000), using two hands simultaneously force deficit was more likely to occur than in submaximal force production tasks, since it may lead to a combination of motor overflow and bilateral deficit effects (Li et al., 2000). For regularity of force output, motor overflow may have the same effect as bilateral deficit does. If in the bimanual task the irregularity of one hand leads to extra irregularity in the other hand, regularity of force output in the bimanual task will be less than in the unimanual task. Hence in bimanual force production tasks motor overflow and bilateral deficit may have an opposite effect for force generation, but they may reinforce each other for irregularity of force output. What are the brain structures involved in bimanual skills? In normal adults, Andres et al. (1999) proposed that the increase in task-related coherence in the early learning phase of bimanual skill acquisition reflected changes in interhemispheric communication that are especially related to bimanual learning and may be transmitted through the corpus callosum. In a kinematical analysis of bimanual in-phase and anti-phase movements, Stephan et al. (1999) revealed an impairment of both the temporal adjustment and the independence of movements between the hands in two adult patients with midline tumors. Lateralisation is also important. In right-handed adults a substantial left hemispheric involvement was found in the coordination of bimanual tasks (Debaere et al., 2001; Gutnik & Hyland, 1997; Ja¨ncke et al., 1998). Another aspect of motor overflow or mirror movements is that motor overflow is depending on age. Younger children exhibit greater associated movements in the contralateral hand during unimanual tasks (Abercrombie, Lindon, & Tyson, 1964; Cohen, Taft, Mahadeviah, & Birch, 1967; Ja¨ncke et al., 1998; Wolff, Gunnoe, & Cohen, 1983), although associated movements do not completely disappear in adulthood (Zijdewind & Kernell, 2001). The explanation for the developmental differences may be found in the development of interhemispheric communication. Fagard, Hardy-Le´ger, Kervella, and Marks (2001) stated that in children, at least till the age of 10 years, improved interhemispheric communication contributed to progress in bimanual coordination in line drawing tasks, especially those which require resisting the attraction of mirror movements. De-Guise and Lassonde (2001) found that, before the age of twelve, children could not learn a procedural skill that required bihemispheric integration during its acquisition. The most plausible explanation for this finding is a difference in the degree of callosal maturation between the age groups. On the other hand, Milling-Smith, Eunson, and Walsh (2002) did not find differences between 8-year-old children and adults with respect to in-phase skills such as needed to synchronize movements of two fingers when making or breaking contact. It seems that for the synchronization between the hands needed for in-phase skills the development has reached a plateau before the age of eight. The interest in this study was to look at the differences in using the preferred (right) hand in a single-handed isometric force task compared to using the preferred (right) hand in a two-handed isometric symmetric force task. It was hypothesized that there would be a higher absolute error and more irregularity, and that the
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participants would need more time in the bimanual task. This is expected because participants have to regulate two forces and are getting visual feedback from two cursors at the same time. Doing so will demand additional effort from the central nervous system, especially with respect to the communication between the hemispheres. Furthermore in younger children the movement quality is likely to be lower due to developmental aspects concerning callosal maturation and attention. Since variability of force is related to absolute levels of force, in this study the force control development is described in outcome variables relative to MVC and over a large range of force levels. An experiment was designed in which isometric force had to be maintained at five relative force levels (Smits-Engelsman, Westenberg, & Duysens, 2003).
2. Method 2.1. Participants Seventy-six children of three primary schools were approached to take part in the study. One of the inclusion criteria was right-handedness on annettÕs (1970) test for children under 9 years of age. The mean score on AnnettÕs test was 8.3 (SD 1.8), no significant differences between 5 and 6 year olds and 7 and 8 year olds were found. Furthermore, no developmental delay, motor problems or muscle diseases should be present. For all children this was confirmed by scores above the 5th percentile on the Manual dexterity subscore of the Movement ABC (Henderson & Sugden, 1992; Smits-Engelsman, 1998). After checking for the inclusion criteria, 63 children (mean age 8.5 year, SD 2.34 year, mean score on manual dexterity part of the MABC 1.79, SD 1.75) entered the study, 29 boys (46%) and 34 girls (54%) belonging to four age groups. Age group 1 (5–6 year olds) consisted of 18 children, age group 2 (7–8 year olds) consisted of 12 children, age group 3 (9–10 year olds) consisted of 16 children and age group 4 (11–12 year olds) consisted of 17 children. Furthermore, 15 adults (mean age 24.5, SD 2.22), 7 male and 8 female, entered the study (Table 1). All parents, children and adults gave a written consent to participate in the study. 1 2.2. Procedure and tasks All 78 participants had to perform two randomised isometric force tasks. One task had to be performed with the index finger of the preferred hand and the other task with the index fingers of both hands. To perform the isometric force task, participants were seated on an adjustable chair in front of a monitor, which was placed at eye level. On this monitor one yellow cursor was displayed at the side of the preferred hand in case of the one-handed task. To perform the isometric force task with 1
The children in this study were recruited as control children for a study on age and therapy related changes in cerebral palsy approved by the Medical Ethic Committee of Stichting Revalidatiecentra Limburg (SRL).
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Table 1 ParticipantÕs characteristics Age group
Age (years)
1 2 3 4 5
5–6 7–8 9–10 11–12 20–30
Gender Male
Total
Total number Female
8 6 7 8 7
10 6 9 9 8
18 12 16 17 15
36
42
78
both hands two yellow cursors were displayed on the monitor, one at the left side for the left hand and one at the right side for the right-hand (Fig. 1). Participants could control the vertical position of the cursor by applying force, with their index finger of the preferred (right) hand or with both index fingers, onto the end of a (two) lever(s). The harder they pressed, the higher the cursor(s) moved on the monitor. The participants were only allowed to use the flexor muscles of their index fingers. The other fingers, and their forearms, had to rest on the table. The aluminium levers transmitted the force onto a force transducer. On each trial the participants had to move the cursor(s) towards a target (grey bar) as fast as possible after the start signal, a short tone. When the cursor(s) reached this target another short tone indicated that a 10-s recording hold period started. During these 10 s the participant was required to keep the cursor(s) as steadily as possible over the position of the target. The instructions for the bimanual task were to keep eye on both the cursors. At the end of the 10 s a third tone sounded as a stop signal. Before the experiment started the maximum voluntary contraction (MVC) of the index flexor muscles was measured. The participants were required to keep the
Fig. 1. Experimental set-up: Example of a bimanual task, showing apparatus and monitor on which the grey bar can be seen at the 48% level and the cursors (beneath the grey bar) representing the generated force of the left and the right hand, respectively.
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yellow cursor(s) at the same height as the red cursor(s), which moved slowly up the screen indicating a steadily increasing force level. The level rose to 50 N in 30 s. The participants were instructed to let go when they felt that they could not attain the required force level any longer. This force level was taken as a measure of MVC. In the experiment six different levels of constant force were recorded for each task, ranging from 0% to 60% of MVC. The MVC was used to program the target force or the force required at 0%, 12%, 24%, 36%, 48% and 60% of the MVC for each participant. The feedback was adjusted so that 0% of MVC was exactly at the bottom of the screen of the monitor and 60% was at the top. Each force level (0%, 12%, 24%, 36%, 48% and 60%) was measured five times giving a total of thirty trials per participant. The 0% condition was used to measure and correct for equipment noise. Before each task a training session was given. The total of thirty trials took about 25 min. All trials were completely randomised for each participant. To measure the force exerted by the finger a high-quality strain gauge (Sokki Kenkyujo; type CLS-20KA) was used. This gauge is temperature compensated and highly linear. An amplifier (Burster; type 9154) delivered its output to a 12-bit AD-converter (DAS800). The computer sampled the signal at a rate of 1000 Hz. To provide the participant with stable feedback the signal was first reduced in frequency to 100 Hz and then filtered using a digital low-pass Finite-Impulse Response filter with a transition band from 5 to 15 Hz. This highly filtered signal was used to update the vertical positions of the cursor on the monitor sixty times a second. (Note that for data-analyses the raw signal was used both for the hold periods and for the time prior to and following the hold period.) In case of the bimanual task, force was recorded for the preferred and the nonpreferred hand. In this study only the data of the preferred hand were computed. The mean generated force, absolute error, variables measuring force regulation (standard deviation (SD), coefficient of variation (CV)) and time to target force were computed for each recording. The generated force (N) was computed as the median force level that the participant actually generated per trial. Medians were used to filter for outliers. In the subsequent analysis means per condition were calculated. The absolute error was defined as the absolute difference score between the target force and the generated force. SD was calculated over each hold period of 10 s. The Coefficient of Variation was defined as the mean generated force divided by the SD and multiplied by 100%. Time to target force was defined as the time (s) from the starting signal till the moment the grey target bar was reached. The dependent variables were evaluated by means of a General Linear Model, Repeated Measures design. For all dependent variables the interaction effect of gender and task was computed. Within-subject variables were task (2 levels), percentage of MVC (5 force levels) and repetitions (5). Age group (5 levels) was entered as between-subject variable. The two levels of the variable task consisted of a unimanual level and a bimanual level in order to compare the achievements of the preferred (right) hand in the unimanual task with the achievements of the preferred hand in the bimanual task. Alpha was set at 5% (two-tailed). Only the significant effects will be reported.
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3. Results 3.1. Force generation: MVC and mean generated force Significant differences in force generation between the unimanual and bimanual task were not found, meaning that the preferred hand performed comparable in the unimanual and in the bimanual task (Fig. 2). For MVC the means were: unimanual 24.22 N, bimanual 23.90 N, for mean generated force the means were: unimanual 8.49 N, bimanual 8.30 N. There was no developmental trend in this lack of significant difference in force generation, indicating that children made the same difference in force generation between a unimanual and a bimanual task as adults did. 3.2. Absolute error (AE) All participants were able to perform the requested tasks. Overall the AE during this experiment was low. Taken over all 3900 trials, the average deviation of the actual produced force from the target force (mean 8.66 N) was small, namely only 0.31 N, or about 3.6%. As expected, the AE in the bimanual task was higher than in the unimanual task (F(1, 73) = 12.691, p = 0.001). The deviation from the target force was 45% higher in the bimanual task (mean bimanual: 0.368 N, mean unimanual: 0.254 N). No developmental trend in differences between the unimanual and bimanual task was found for AE. 3.3. Force regulation: SD and CV
Difference between the tasks (%)
For force regulation it did make a difference if the task was completed with one or two hands. Both aspects of force regulation, SD and, CV, showed highly significant main effects of task (F(1, 73) = 9.246, p = 0.003, F(1, 73) = 14.410, p = 0.000, respectively) (Fig. 2). In both cases the scores on the bimanual task were higher, meaning that the participants produced more variable force in the bimanual task than in the 50 40 30 20 10 0 MVC
Force
SD *
CV *
Time *
AE *
-10
Fig. 2. Task differences: Bimanual task minus unimanual task for maximal voluntary contraction force (MVC, 1.3%), generated force (force, 2.2%), SD (20.8%), CV (33.8%), time to reach the target force (time, 28.2%) and absolute error (AE, 44.8%). * = significant, p < 0.005.
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unimanual task. The means were for SD: unimanual 0.536 N, bimanual 0.647 N, for CV: unimanual 7.700, bimanual 10.300. The difference in SD between the unimanual and bimanual task became smaller with repetition of the task, indicating that there was a learning effect in the twohanded task, in contrast with the single-handed task, as evaluated by the factor repetition (F(4, 292) = 3.418, p = 0.009). The differences between the unimanual and bimanual tasks in repetition 3 and 5 were still significant (F(1, 73) = 4.278, p = 0.042), while this was no longer the case for the differences between 4 and 5. Different patterns emerged for the age groups as shown by the interaction effect of repetition, task and age group on SD (F(16, 1168) = 1.895, p = 0.021). The analysis revealed that the learning effect was clearly age dependent, as is shown in Fig. 3. The greatest learning effect was seen in the youngest children (Fig. 3). This was confirmed by the fact that only in the youngest group the effect of task and repetition was significant (F(4, 68) = 4.3838, p = 0.002). Hence only the children in the youngest group showed a learning effect in the bimanual task. The results were basically similar for CV (interaction effect of repetition, task and age group on CV: F(16, 1168) = 2.141, p = 0.007). As for SD, the effect of task and repetition was significant only in the youngest age group (F(4, 68) = 5.311, p = 0.001), but in contrast with the findings on SD the effect of task was still significant in repetition 5 for age group 1 (F(1, 89) = 4.208, p = 0.043). With age the variability in force decreased. This change is best illustrated using CV, since then the difference in force levels is accounted for. As is depicted in Fig. 4, based on CV the younger children showed significantly greater differences between the unimanual and bimanual task than older children (interaction effect of task and age-group on CV: F(4, 292) = 3.197, p = 0.018). It can be seen that from 9–10 years on the difference between the unimanual and bimanual task becomes
Fig. 3. Differences between the age groups on absolute force variability (SD). SD of the Generated Force in the unimanual and the bimanual task for each Repetition (1–5) and per age group.
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25 *
20 CV (%)
15 *
10 5 0
5 and 6
7 and 8
unimanual
14.70
11.02
9 and 10 11 and 12 20 till 30 5.31
4.63
2.68
bimanual
20.46
16.61
6.58
5.35
2.63
Age groups (years)
Fig. 4. Developmental trend in relative force variability (CV). CV of the generated force in the unimanual and the bimanual task per age group with standard error. * = significant, p < 0.005.
smaller, so the largest part of development takes place before 11 years of age (age group 2–3: F(1, 26) = 5.175, p = 0.031) (Fig. 4). However, the significant difference between 9–10 year olds and adults proves that development is not yet complete at 10 years of age (age group 3–5: F(1, 29) = 4.467, p = 0.043) (Fig. 4). 3.4. Time to target force
Time difference (s)
Time difference (s)
An interaction effect for gender and task was found. Although there were no differences between male and female participants in the one-handed task, in the 5 and 6 years
7 and 8 years
11 and 12 years
20 till 30 years
9 and 10 years
2.00
1.00
0.00
Force level (%) 2.00
12 24
1.00
36 48 60
0.00
Dot/Lines show Means 1
2
3
Repetition
4
5
1
2
3
4
5
Repetition
Fig. 5. Developmental trend in time to reach the target force. The difference in time to reach the target force between the unimanual and bimanual task, for each force level (% of MVC), repetition (1–5) and age group.
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two-handed task male participants needed 15.2% more time to target force than female participants (F(1, 76) = 4.822, p = 0.031). A highly significant main effect of task was found for time to target force (F(1, 73) = 43.095, p = 0.000). The scores on the bimanual task were higher, meaning that the participants needed more time to target force in the bimanual task than in the unimanual task (unimanual 2.387 s, bimanual 3.060 s). The differences between the unimanual and bimanual conditions were larger when the force levels were higher, 21%, 23%, 25%, 34% and 34%, respectively, for the increasing force levels (F(4, 292) = 9.629, p = 0.000). In Fig. 5 one can see that after the age of 8 years children gradually show less variability in each repetition and for each force level and grow to more adult values (Interaction effect of repetition, force level, task and age-group on time to target force: F(64, 4672) = 1.390, p = 0.025). However, the difference between the tasks was still significant for adults (effect of task on time to target force for adults: F(1, 14) = 29.530, p = 0.000).
4. Discussion 4.1. Force generation, absolute error and force variability In the present study the MVC and the mean generated force for the right hand were not significantly different in the unimanual and the bimanual task. Other authors did find a bilateral deficit in measuring MVC of finger flexor muscles (Li et al., 2000; Zijdewind & Kernell, 2001). However, the focus of the present study was slightly different. Other groups defined bilateral deficit as the difference between the combined MVC of the bimanual task and the sum of the MVCs during the unimanual task (Li et al., 2000), while in this study the MVC of the preferred hand in the unimanual task was compared to the MVC of the preferred hand in the bimanual task. Differences in bilateral deficit could appear when the forces generated by the preferred and non-preferred hand in the bimanual task were different, but in none of the three studies this difference was significant. Furthermore, there was a high degree of symmetry of the bimanual task in the present study. Gutnik and Hyland (1997) already found that better spatial symmetry in limb movement was achieved when both hands employed similar within-hand strategies, as was the case in the present study. Other authors confirm the fact that the bilateral deficit is less in a symmetrical bimanual task compared to an asymmetrical task (Li et al., 2000). In the study of Li et al. (2000) different combinations of fingers within a hand were used, while in the present study the participants had to generate force only with the index fingers, which may be regarded as a simpler task. Simpler tasks may be less sensitive to bilateral deficit. Li et al. (2000) also found that in asymmetrical tasks more complexity (using fewer fingers within the hand and more fingers in the other hand) led to more bilateral deficit. The other study that revealed a bilateral deficit in force generation was only based on 5 adult participants (Zijdewind & Kernell, 2001). The assumption of Li et al. (2000) that sub-maximal force production tasks may lead to a combination of bilateral deficit and motor overflow seem to be confirmed
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by our findings. Since there was no significant difference between the unimanual and bimanual task on mean generated force the conclusion could be that the opposite effect of bilateral deficit and motor overflow may have led to this lack of difference. Nevertheless, the bimanual task demanded more additional effort than the unimanual task. This was also confirmed by the fact that the AE was higher in the bimanual task. Participants needed more time to reach the target force and showed more absolute (SD) and relative (CV) force variability in the bimanual task. These differences may reflect a rise in coordination effort in the bimanual task. These findings seem to confirm the findings of other authors, although they used different approaches. Morrison and Newell (1998) looked, by means of cross correlations on ApEn scores (amplitude and regularity of the force signal), at the coordination between hands in a bimanual isometric force task. They found that the regularity of the force output of each index finger considered separately was greater than that of the total force (Morrison & Newell, 1998). Taniguchi et al. (2001) used reaction time tasks and simultaneously measured the brain electrical activity. They reported that there was a deficit in reaction time for the bilateral response for the right index finger movement, both in adults and children (Taniguchi et al., 2001). The latter type of findings has led some authors to suggest that the timing of bimanual tasks is more tightly coupled than the control of force (for evidence for the dominance of temporal coupling over force coupling in bimanual tasks see Harbst et al., 2000; Inui & Hatta, 2002; Rinkenauer et al., 2001). The present results do not support this contention since the effects of task on the time to target force and on SD and CV all were highly significant for the whole group of participants. Admittedly, however, if only the adults were considered, the effect on the temporal variables was clearer than on the force control variables in the bimanual task. 4.2. Development The differences in AE between the uni- and bimanual task were constant with age. Milling-Smith et al. (2002) found that children reached a plateau before the age of eight measuring timing errors. Nevertheless, CV showed a clear developmental trend since for younger children the differences between the unimanual and bimanual task were greater than for older children (Fig. 5). So, CV seems to be more sensitive to measure development than error. The greatest steps in development were made before the age of about 10 years. This is in accordance with the assumption of Fagard et al. (2001) that in children improvement of interhemispheric communication, at least till the age of 10 years, contributes to progress in bimanual coordination. This development is faster as expected from some other studies. For example, De-Guise and Lassonde (2001) found that before the age of twelve, children could not learn a procedural skill that required bihemispheric integration during its acquisition. However, this was based on learning more difficult tasks namely asymmetrical out of phase skills. Hence, the difference in tasks may be a plausible explanation for the difference in development, although even in the present study development is not quite complete at 10 years of age.
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Several factors may contribute to the large variability found in many of the variables at young age. The immaturity of the neural substrate is a first candidate but one should also consider the lack of concentration often observed in young children. This lack of attention may explain the capricious patterns in SD and CV and in the time needed to target force at least till the age of 10 years. Temprado, Zanone, Monno, and Laurent (2001) stated that attention plays an important role in modifying the coupling between the limbs. In the present study it was found that the learning effect only concerned the youngest children. In this group a plateau in performance was reached at repetition 4, yet there was still a significant difference between the unimanual and bimanual task in repetition 5. It remains to be seen whether this effect would stay when the task was repeated more often. The second age group (7 and 8 years) showed no effect of repetition but did exhibit a clear overall increase in force variability in the bimanual task as compared to the unimanual version. From developmental studies it is known that changes in spatial accuracy and temporal variables show a non-monotonic profile with a temporary decrease in performance around 7–8 years of age (Bard, Hay, & Fleury, 1990; Hay, Bard, Fleury, & Teasdale, 1991). This might reflect qualitative changes in the movement control processes. With respect to the younger group, they showed better results in the unimanual task but not yet in the bimanual task. In age groups 3, 4 and 5 the differences in absolute force variability between the tasks rapidly decreased. 4.3. Conclusions In conclusion, it was found that the preferred hand was not affected by bilateral execution of an isometric task with respect to force generation (MVC and mean generated force). Although the task was simple, force control, as evaluated by absolute (SD) and relative (CV) force variability, was more difficult, and time to target force was longer in a bimanual isometric force task than in a unimanual task. Despite the difficulty, only the youngest children showed a learning effect. Developmental changes in force control were found at least till the age of ten, although adult values were not yet reached then. It seems likely that improvement in interhemispheric communication and in the ability to focus attention plays a role.
Acknowledgments We wish to thank all the children and their parents and all the adults for their commitment and willingness to participate in this study, and Mr. Peter de Jong for developing the OASIS software needed in this experiment.
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