Between-limb asynchronies during bimanual coordination: Effects of manual dominance and attentional cueing

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Neuropsychologia, Vol. 34, No. 12, pp. 1203 1213, 1996 Copyright '.~; 1996 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0028-3932/96 $15.00+0.00

Between-limb asynchronies during bimanual coordination: Effects of manual dominance and attentional cueing STEPHAN P. SWINNEN,* KRIS JARDIN* and R U U D M E U L E N B R O E K t *Motor Control Laboratory, Department of Kinesiology, K. U. Leuven, Belgium; tDepartment of Psychology, University of Nijmegen, Nijmegen, The Netherlands

(Received 16 January 1996; accepted 2 May 1996) Abstract--Whereas previous studies on interlimb coordination have mainly underscored the ubiquitous tendency to synchronize the motions of the limbs, the present experiment revealed a small, but distinct, interlimb asynchrony or phase offset, i.e. the dominant limb led the non-dominant limb during the production of bimanual circle drawing. This asynchrony was clearly evident in the majority of right-handers, but not in left-handers. Moreover, attentional cueing affected the size of the asynchrony. Instructions to visually monitor the dominant limb or non-dominant limb strengthened and weakened the phase offset, respectively. A multifactorial neural account is proposed to underly the temporal asynchrony. Copyright © 1996 Elsevier Science Ltd Key Words: bimanual coordination; asynchrony; hand preference; attention; motor control; hemisphere specialization.

dination modes. The former mode involves symmetrical limb movements, i.e. flexing and extending both limbs simultaneously (homologous muscle groups). This pattern can be produced easily and with a high degree of consistency, even in patients who suffer from various central nervous system disorders [40]. The anti-phase or asymmetrical coordination mode requires one limb to flex, whereas the other is extended, or vice versa (nonhomologous muscle groups), and is usually performed with a lower consistency. Alternative patterns that deviate from both these modes, or patterns requiring interdependent bimanual control, are much more difficult to perform. Attempts to produce such patterns are often accompanied with a regress to these preferred coordination modes [12, 43]. In spite of the overwhelming evidence in favour of phase synchronization, recent studies have pointed to small, but distinct, asynchronies that can be observed either at the initiation of discrete bimanual movements [32] or on a more continuous scale during the production of cyclical movements [2(~28]. For example, Stucchi and Viviani [26] investigated bimanual ellipse drawing in the frontoparallel plane and found that the dominant limb led the non-dominant limb in both right- and left-handers with a temporal offset of about 15 30 msec on average. They proposed that the periodic movements were timed

Introduction

When attempting to perform various combinations of tasks with the upper limbs, it becomes evident that some task combinations are easy to perform, whereas others are extremely difficult. For example, when trying to perform discrete movements with different spatiotemporal features, patterns of interference arise and errors in one task reflect the features of the other task [3, 6, 14, 25, 32, 30, 33, 38, 39]. These patterns of interference arise from a natural tendency to synchronize the upper limbs, resulting in preferred patterns of interlimb coordination. The synchronization tendency is often so powerful that considerable practice is required to overcome this effect in order to produce differentiated patterns of activity in the upper limbs [31, 39]. In recent years, systematic attempts have been undertaken to describe and characterize preferred patterns of intralimb [16] and interlimb coordination [9]. With respect to interlimb coordination, these patterns have been identified as the in-phase and anti-phase c o o r # Address for correspondence: Laboratory of Motor Control, Department of Kinesiology, K.U. Leuven, Tervuurse Vest 101, 3001 Heverlee, Belgium; e-mail: Stephan.Swinnen@FLOK. KULEUVEN.AC.BE. 1203

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by a lateralized functional m o d u l e a n d that the async h r o n y arised f r o m the necessity to t r a n s m i t t i m e - k e e p i n g i n f o r m a t i o n to the o t h e r hemisphere. In the present study, an a t t e m p t was m a d e to o b t a i n m o r e detailed i n f o r m a t i o n a b o u t the interlimb async h r o n y d u r i n g b i m a n u a l circle d r a w i n g by m e a n s o f continuous relative phase measures. M o r e o v e r , to o b t a i n further insights into the causal n a t u r e o f this a s y n c h r o n y a n d its m o d u l a t i o n s in the face o f externally i m p o s e d constraints, the effects o f a t t e n t i o n a l cueing were investigated. F u r t h e r m o r e , the role o f h a n d preference was studied. Stucchi a n d Viviani [26] did n o t d e m o n s t r a t e differences between right- a n d left-handers in spite o f the fact that b o t h g r o u p s are k n o w n to differ f u n d a m e n t a l l y in the w a y t h a t they cope with b i m a n u a l c o o r d i n a t i o n tasks [18]. F u r t h e r m o r e , the a u t h o r s did n o t show a n y effect o f a l l o c a t i o n o f a t t e n t i o n t o w a r d s the d o m i n a n t or n o n - d o m i n a n t limb on the a s y n c h r o n y , a n d they c o n c l u d e d , therefore, t h a t a t t e n t i o n a l focus did n o t m o d u l a t e the relative p o s i t i o n s o f the h a n d s in time a n d space. W h e r e a s Stucchi a n d Viviani [26] a t t a c h e d s o u n d emitters to one h a n d to direct a t t e n t i o n , we instructed subjects to visually m o n i t o r either the d o m i n a n t or nond o m i n a n t h a n d d u r i n g s e p a r a t e trials. These experimental c o n d i t i o n s were c o m p a r e d to c o n d i t i o n s in which no specific vision instructions were p r o v i d e d a n d in which subjects p e r f o r m e d the circle d r a w i n g s while blindfolded.

Method Subjects Twenty undergraduate students of the Catholic University of Leuven participated in the experiment. Ten subjects were identified as right-handers and 10 as left-handers by means of the Oldfield questionnaire. They were recruited from a large pool of students (>200). Only subjects with a distinct preference for either the right or left hand were selected, excluding those who demonstrated any signs of inconsistent hand preference. Subjects were not previously involved in a similar experiment and were not paid for their services.

Apparatus and task The apparatus consisted of two XY-digitizing tables (LC20TDS Terminal Display Systems) positioned in the horizontal plane in front of the subject. The accuracy of registration was 0.25mm. To sample data from both digitizers in a parallel fashion at high baud rates, a dual serial input card with cache memory was used. Subjects moved across the digitizers, holding a Z-pen in each hand. Kinematic data were acquired from both digitizers with respect to the x-axis and y-axis components at a sampling frequency of 150 Hz. The x-axis and y-axis component was parallel to the transverse and sagittal plane, respectively. A computer-controlled electronic metronome indicated the cycling frequency (1 Hz). Subjects were comfortably seated on a height-adjustable chair with one digitizer on the left of their median plane and

the other on the right (see Fig. 1). Both forearms were positioned just above the surface of the tables. The task consisted of tracing the contour of a target circle (diameter: 8 cm) which was affixed to each digitizer. The distance between the centres of the circles was 35.8 cm. Subjects were instructed to draw one complete circle with each limb per beat of the metronome and for a total duration of 15 sec per trial. The movements were always initiated with the tip of the stylus positioned at the centre of the circle.

Procedure Subjects were instructed to draw circles in a symmetrical fashion, using both upper limbs. One limb moved in a clockwise (CW) and the other in a counter clockwise (CCW) fashion (Left CW-Right CCW and Left CCW-Right CW). Four trials were performed in each condition. The circle drawings were performed under four different vision conditions: (1) free vision, (2) visual monitoring of the dominant hand, (3) visual monitoring of the non-dominant hand, and (4) blindfolded. During the free-vision condition, subjects were free to adopt any visual strategy that they preferred. During the second condition, subjects were instructed to direct their attention to the dominant hand and to visually monitor its movements. During the third condition, subjects were to monitor their non-dominant hand. A video-camera and a monitor were used to control for the direction of vision to the instructed hemifield. During the blindfolded condition, the experimenter helped the subject to position the styli of the digitizer at the centre positions, and subjects were prohibited from using vision at any time during the 15-sec trial duration. The effects of these manipulations on interlimb asynchronies during circle drawing were investigated. Subjects were instructed to draw the circles as accurately as possible while synchronizing the limbs at the beat of the metronome. No specific link between the spatial aspects of movement and the beat of the metronome was established. Following the 'start' command, pacing of the metronome was initiated and subjects performed the required movement for a duration of 15 sec. The order in which the experimental conditions were performed, was randomized across subjects.

Data analysis The data analysis focused on the spatiotemporal features of the individual limb motions by means of cycle duration and circle amplitude measures as well as the relative phasing between the x-axis and y-axis component within a limb (intralimb coordination). Interlimb coordination was also quantified through relative phase analyses: the phase difference was computed between the x-axis component of the left and right limbs, and a similar procedure was applied to the y-axis components. Circle diameter. The spatial measure of the left and right limb motions consisted of the absolute value of the peak-positive to the peak-negative amplitude along the x-axis and y-axis ( = diameter) for each individual cycle. Means and S.D.s were calculated across trials of the same condition. The target circle diameter was 8 cm. Cycle duration. Cycle duration or period was defined as the time elapsing between two successive positive peaks along the x-axis component. Means and S.D.s were calculated for each cycle and were averaged across trials. The metronome-imposed cycle duration was 1000 msec. Relativephase. Phase refers to a description of the stage that a periodic motion has reached, i.e. the point of advancement of a signal within its cycle. The difference in phase angle, also referred to as the relative phase, provides a signature of the

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Fig. I. View of the experimental apparatus: the bimanual digitizer setup. coordination pattern that is observed between the limbs [5, 9, 36]. The continuous phase of the x-axis and y-axis component of each arm oscillation was calculated, using a formula adapted from Kelso and coworkers [10, 23]. Subsequently, relative phase between the limbs was computed according to the following formula: ~b = 0D-- 0ND = tan '[(dXD/dt)/XD] - t a n - I[(dXND/dI)/XND], where 0D refers to the phase of the dominant limb movement at each sample, XD is the position of the dominant limb after rescaling to the interval - 1 , 1 for each cycle of oscillation, and dXD/dt is the normalized instantaneous velocity. The same notation applies to the non-dominant limb (ND). This computation was performed between the respective x-axis components of both limbs as well as between their y-axis components. This procedure is based on the following mathematical conventions. The relevant variables to describe the state of an arm movement or any other system with oscillatory features are its momentary position and velocity (the state variables). In graphical terms, these variables can be considered as coordinates of a point in a two-dimensional Cartesian coordinate system with the position being represented in the x-axis and velocity in the y-axis (a phase-plane). When the oscillations are harmonic, the phase-plane representation evolves into a circular trajectory. If position and velocity are rescaled to the interval [ - 1 , + 1], these Cartesian coordinates become equivalent to the cosine and sine values of the phase angle, which are then used for computation of the tangent of that angle. It is possible, therefore, to represent the state of that system by polar coordinates (0-360 °) instead of the Cartesian coordinates. Following computation of the phase angle in each limb, the relative phase was computed by subtraction of the phase angles. These data were subsequently averaged across the cycles of the x-axis and y-axis component within a trial as well as across trials to obtain a measure of the mean relative phase. The S.D. around the mean relative phase was computed to obtain an estimate of variability. The right arm was used as the reference

limb in right-handers and the left arm in left-handers. Accordingly, positive values are indicative of a phase lag of the nondominant limb with respect to the dominant limb, irrespective of manual dominance. To assess the quality of circle drawing within each limb, a relative phase analysis was computed between the oscillatory x-axis and y-axis components within a limb (0x 0v), using a procedure similar to the one described previously for assessing interlimb coordination. This analysis was based on the premise that a perfect circle drawing is characterized by a 90 ° phaseoffset between the x-axis and y-axis component. This is exemplified in Fig. 2 where the oscillatory displacement traces of the x-axis and y-axis component of a representative movement are shown as a function of time on the left side of the figure. The resulting circle drawing is shown on the right side. Whereas there are alternative ways to measure the quality of circle drawing, the current measure provides an overall indirect estimate of the quality of intralimb coordination between the wrist, shoulder, and elbow movements, as inferred from the endeffector kinematics. Because this analysis does not distinguish between drawing a circle and an ellipse, it is necessary to complement it with measures of the x-axis and y-axis diameter. These diameters are the same for a circle, but deviate from each other for elliptical configurations.

Results Between-limb measures: relative phase A 2 x 4 ( G r o u p x Vision) A N O V A with repeated measures o n the last factor was c o n d u c t e d on the m e a n a n d S.D. scores separately. ' G r o u p ' consisted of the righthanders a n d left-handers. 'Vision' consisted of four levels: free vision, vision directed to the d o m i n a n t or n o n - d o m i -

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nant limb, and blindfolded. As preliminary analyses did not reveal any significant differences between inward and outward circle drawing, this factor was excluded from subsequent analyses. The analysis of mean relative phase revealed that all mean values were positive. This implies that the dominant limb generally led the non-dominant limb. The group effect was significant [F(1,18)=7.21, P<0.05]. The phase lag between the dominant and nondominant limb was larger in right-handers than in lefthanders ( M = 10.73 and 2.69°), respectively. Significant differences were also observed among the four vision conditions [F(3,54)= 11.69, P<0.01 (Fig. 3, left side)]. The phase offset was largest when vision was directed to the dominant hand. A smaller phase offset was observed under the free-vision and blindfolded conditions. The smallest phase offset was observed when the subject was instructed to visually monitor the non-dominant limb. Aposteriori tests revealed significant differences between the condition in which the dominant limb was monitored and monitoring of the non-dominant limb, the free, and blindfolded condition ( P < 0.01). The phase offsets during monitoring of the non-dominant limb were significantly smaller than those observed in the free and blindfolded condition (P < 0.05). The only pairwise difference failing to reach significance was that between the free and blindfolded condition (P>0.05). The G r o u p × Vision interaction was not significant [F(3,54)< 1]. This implies that the effect of the vision conditions did not differ significantly between handedness groups. In order, mean

relative phase scores for the free-vision condition, the conditions with visual monitoring of the dominant or non-dominant limb, and the blindfolded condition were 11.12 °, 14.5 ~, 6.57' and 10.72 c' for the right-handers and 2.24 ~:, 5.57", 0.44 ~', and 2.49 ° for the left-handers. In order to obtain insights into the sign of the asynchrony across subjects, individual mean relative phase scores within the group of right-handers and left-handers were studied. Within the group of right-handers, the right hand consistently led the left hand in eight out of the 10 subjects and across the various performance conditions. Two subjects showed an inconsistent pattern with leading by both the right and left hands. The group of left-handers was less homogeneous: the left hand predominantly led the right hand in four subjects, the right hand led the left hand in two subjects, and no consistent sign in phase offset was observed in the remaining four subjects. It is also noteworthy that the phase offset varied over the duration of the trial, even in the right-handed subjects who showed a clear phase lag of the non-dominant limb. This is shown in Fig. 4 representing a trial of a righthanded subject during the free vision condition. The circle drawings of the left and right arm are shown in the top row. Underneath these relative motion plots are the xaxis and y-axis components of the displacement profiles as a function of time. The bottom graph shows the continuous relative phase scores with respect to both the xaxis and y-axis component. Even though the right limb leads the left limb most of the time, there are also small 10

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portions of the trial where the phase lag is reversed (as indicated by phase scores below the zero line). Analysis of the relative phase variability scores revealed a marginally significant main effect for group [F(1,18) =4.15, P = 0.05]. The S.D. scores were smaller in left-handers than in right-handers ( M = 8 . 7 3 and 9.77', respectively). Significant differences were also observed

a m o n g the four vision conditions [F(3,54) = 6.43, P < 0 . 0 1 (Fig. 3, right side)]. Interlimb coordination was most consistent during monitoring of the d o m i n a n t limb. It was slightly less consistent during the blindfolded and the free vision condition. Performance was least consistent when subjects were to m o n i t o r their n o n - d o m i n a n t limb. A - p o s t e r i o r i tests revealed that monitoring the d o m i n a n t

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limb resulted in smaller variability scores t h a n m o n i toring the n o n - d o m i n a n t limb a n d the free vision condition ( P < 0 . 0 1 ) . M o r e o v e r , the S.D. scores u n d e r b l i n d f o l d e d c o n d i t i o n s were significantly lower t h a n during m o n i t o r i n g o f the n o n - d o m i n a n t limb ( P < 0.05). The r e m a i n i n g pairwise c o m p a r i s o n s were n o t significant ( P > 0 . 0 5 ) . The G r o u p x Vision i n t e r a c t i o n was not significant [F(3,54) < 1]'L

Within-limb relative phase analyses Relative phase was c o m p u t e d between the x-axis a n d y-axis c o m p o n e n t s within a limb to o b t a i n a general estimate o f the quality o f intersegmental c o o r d i n a t i o n , as inferred f r o m the kinematics o f the end effector. As i n d i c a t e d previously, the p r o d u c t i o n o f a perfect circle is c h a r a c t e r i z e d by a 90 ° phase offset between the x-axis and ),-axis c o m p o n e n t . A 2 x 2 x 4 ( G r o u p x L i m b x Vision) A N O V A with r e p e a t e d measures on the last two factors was c o n d u c t e d on the m e a n relative phase a n d v a r i a b i l i t y scores separ-

? In addition to the continuous estimate of relative phase, the discrete estimate was computed as well. The latter is based on two relative phase estimates per cycle and is very similar to the discrete estimate commonly used in the literature which is based on one estimate. The phase difference was measured with respect to the peak positions of the reference limb. Similar ANOVAs, as used with respect to the continuous estimates, were also used for the discrete estimate and yielded very similar results. The group effect was significant IF(l, 18) = 7.6, P < 0.05]. The phase lag between both limbs was larger in right-handers than in left-handers ( M = l l . 4 1 and 2.81 ~', respectively). The effect for vision was significant [F(3,54)= 11.88, P<0.01]. The phase offset was largest when vision was directed to the dominant hand ( M = 10.64"). A slightly smaller phase offset was observed under the free vision condition and blindfolded condition ( M = 7.13 and 6.83 °, respectively). The smallest phase offset was observed when the subject was instructed to visually monitor the non-dominant limb ( M = 3 . 8 4 ) . The Group x Vision interaction was not significant [F(3,54)< 1]. In order, mean relative phase scores for the free vision condition, the condition with visual monitoring of the dominant and nondominant limb, and the blindfolded condition were 11.81:, 15.47 °, and 7.08' and 11.28 ~: for right-handers and 2.46", 5.8, 0.6 '~, and 2.39 '~ for the left-handers. Analysis of the variability scores revealed a significant main effect for group [F(I,18)=4.88, P<0.05]. The S.D. scores were smaller in left-handers than in right-handers (M=6.78 and 7.82, respectively). Significant differences were also observed among the four vision conditions [F(3, 54)= 18.8, P<0.01]. Interlimb coordination was most consistent under blindfolded performance conditions ( M = 6 . 4 ) . It was slightly less consistent when subjects were instructed to visually monitor their dominant limb ( M = 6.79°). Performance was least consistent when subjects were to monitor their non-dominant limb ( M = 7.9T ~) and when they were left free to choose their own visual strategy (M = 8.05). The Group x Vision interaction was not significant [F(3,54)< 1]. Overall, it can be concluded that there is a substantial degree of convergence between the continuous and discrete relative phase measures with respect to the present task.

ately. The factor limb referred to the d o m i n a n t a n d nond o m i n a n t limb. The analysis o f the m e a n relative phase revealed no significant differences between r i g h t - h a n d e r s and left-handers ( M = 8 9 . 3 5 ° a n d 9 0 . 8 1 , respectively) [F(1,18)= 1.25, P > 0 . 0 5 ] . The m e a n relative phase was significantly smaller in the d o m i n a n t limb ( M = 8 8 . 1 7 ' ) than in the non-dominant limb (M= 91.94) [F(1,18) = 18.49, P < 0.01]. The m a i n effect o f vision was n o t significant [F(3,54)= 1.08, P > 0.05]. In order, m e a n s for the free c o n d i t i o n , the c o n d i t i o n with m o n i t o r i n g o f the d o m i n a n t and n o n - d o m i n a n t limb, a n d the blindfolded c o n d i t i o n were 9 0 . 3 , 90.34:, 8 9 . 9 a n d 89.89:. N o n e o f the interaction effects reached significance (P>0.05). The m o r e interesting analysis o f the S.D. scores did not reveal a significant g r o u p effect either [F(1,18)= 3.06, P > 0 . 0 5 ] . S.D.s for r i g h t - h a n d e r s a n d left-handers were 8.59 ~ a n d 7.75 '~', respectively. The consistency o f circle d r a w i n g was higher in the d o m i n a n t limb ( M = 6 . 9 2 ) t h a n in the n o n - d o m i n a n t limb ( M = 9.42'), a n d this effect was highly significant [F(1,18) = 139.97, P < 0.01 ] (see Fig. 5). M o r e o v e r , the four vision c o n d i t i o n s h a d a differential effect on consistency o f circle d r a w i n g [F(3,54)--55.74, P > 0 . 0 1 ] . W h e n p e r f o r m a n c e was a v e r a g e d across b o t h limbs, m o n i t o r i n g the d o m i n a n t limb resulted in the most consistent p e r f o r m a n c e ( M = 7 . 3 9 ) , followed by the freevision c o n d i t i o n ( M = 7 . 5 9 ) , the c o n d i t i o n in which the n o n - d o m i n a n t limb was m o n i t o r e d ( M = 8 . 1 2 ) , and the b l i n d f o l d e d c o n d i t i o n which resulted in the least consistent p e r f o r m a n c e ( M = 9 . 7 ) . The effect o f the vision m a n i p u l a t i o n s also differed between the d o m i n a n t and n o n - d o m i n a n t limb, resulting in a significant Visionx L i m b i n t e r a c t i o n [F(3,54) -- 23.92, P < 0.01 (see Fig. 5)]. D e p e n d i n g on the visual m a n i p u l a t i o n , the differences between the d o m i n a n t and n o n - d o m i n a n t limb were increased or depressed. S e p a r a t e A N O V A s were conducted on the d a t a o f the d o m i n a n t a n d n o n - d o m i n a n t limb. Subsequently, pairwise a-posteriori tests were cond u c t e d on the effect o f vision. W i t h respect to the d o m i n a n t limb, all pairwise c o m p a r i s o n s were significant ( P < 0 . 0 1 ) , except for the c o m p a r i s o n between the c o n d i t i o n , in which the n o n d o m i n a n t limb was m o n i 12°,..~10_ .~ 8a. 4-

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Visual Condition Fig. 5. The consistency of circle drawing with respect to the dominant and non-dominant limb across the four vision conditions.

S. P. Swinnen et al./Bimanual asynchronies tored, and the blindfolded condition (P>0.05). With respect to the non-dominant limb, all pairwise comparisons were also found significant ( P < 0.01), except for the comparison between the free vision condition and the condition in which the non-dominant limb was monitored ( P > 0.05). In other words, visual monitoring of the dominant limb had a beneficial effect on the stability of the circle drawing in the dominant limb and a detrimental effect on the non-dominant limb. On the other hand, visual monitoring of the non-dominant limb had a detrimental effect on the drawings produced in the dominant limb and generated the highest degree of consistency in the non-dominant limb, relative to the other conditions. It appears from these findings that differences in consistency of circle drawing between both limbs were increased when monitoring the dominant limb and were depressed when monitoring the non-dominant limb. The Vision x Limb effect also interacted significantly with group [F(3,54) = 3.06, P < 0.05]. The data pattern for both limbs was very similar for the right- and left-handers, except during blindfolded performance conditions. Here, the difference in consistency between the limbs was much larger for the right-handers than for the left-handers. Apparently, right-handers experienced more difficulty making consistent circles with their left hand than lefthanders with their right hand. The remaining interaction effects did not reach significance (P > 0.05).

Spatiotemporal analyses: cycle duration and circle diameter Cycle duration. In order to verify whether subjects complied with the timing instructions, means for the different conditions were computed. The mean cycle duration was 996 and 987msec for right-handers and left-handers, respectively. Differences in mean cycle duration between the dominant and non-dominant limb were also very small, i.e. 991 and 992msec, respectively. Means for the free vision condition, the condition with monitoring of the dominant and non-dominant limb, and the blindfolded condition were 987,992, 991 and 996 msec, respectively. Circle diameter. Mean amplitudes and their S.D. scores were analysed separately by means of a 2 x 2 x 2 x 4 (Group x Limb x Movement Axis xVision) ANOVA with repeated measures on the last three factors. Movement axis was added to compare the length of the horizontal (x-axis component) and vertical diameter (y-axis component) of the circle. Analysis of the mean diameters did not reveal any significant differences between righthanders and left-handers (M--7.99 and 7.95 cm, respectively) IF(I,18)< 1]. The average diameters measured in the dominant limb ( M = 7.71 cm) were significantly smaller than those of the non-dominant limb ( M = 8 . 2 4 c m ) [F(1,18) = 36.73, P < 0.01]. No significant differences were observed between the lengths of the x-axis and y-axis

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diameters [F(1,18) = 2.06, P > 0.05 (mean diameters with respect to the x-axis and y-axis were 7.92 and 8.02 cm)]. The main effect of vision was highly significant [F(3,54) = 62.88, P < 0.01]. The circle diameter was largest when the subject monitored the dominant limb (M =8.49cm), followed by the free-vision condition ( M = 8.45 cm), the condition with monitoring the nondominant limb ( M = 7.95 cm), and the blindfolded performance condition ( M = 6.99 cm). Three interaction effects were significant (Limb x Vision, Movement Axis× Vision and Limb x Movement Axis x Vision), but these will not be discussed in further detail because they are only considered to be of marginal importance. Analysis of the diameter variability scores did not reveal any significant differences between right-handers and left -banders (M = 0.53 and 0.54 cm) [F( 1,18 ) < 1]. The diameter S.D.s were significantly smaller for the dominant limb (M = 0.47 cm) than for the non-dominant limb ( M = 0 . 6 c m ) [F(1,18)=146.53, P<0.01]. The diameter lengths were also significantly more variable along the x-axis ( M = 0 . 5 9 c m ) than along the ),-axis component ( M = 0 . 4 9 cm) [F(1,18) =74.79, P<0.01]. The main effect of vision was not significant [F(3,54)< 1]. In order, S.D.s observed during the free condition, during visual monitoring of the dominant and non-dominant limb, and during the blindfolded condition were 0.52, 0.54, 0.54 and 0.55cm. Similar to the analysis of the mean diameter scores, three interaction effects were significant: the Limb x Vision, Movement Axis x Vision and Limb x Movement Axis x Vision. With respect to the dominant limb, the highest variability scores were observed when the subject was instructed to monitor the non-dominant limb and the lowest when instructed to monitor the dominant limb. The remaining two vision conditions were positioned in between the aforementioned conditions. In order, variability scores during the free vision condition, the condition with monitoring of the dominant and non-dominant limb, and the blindfolded condition were 0.47, 0.38, 0.57, and 0.49 cm. Aposteriori tests on the data of the dominant limb revealed that all pairwise comparisons were significant (P < 0.01), except for the comparison between the free vision and blindfolded condition ( P > 0.05). With respect to the nondominant limb, the highest variability scores were observed when the subject monitored the dominant limb and the lowest when monitoring the non-dominant limb. Again, intermediate variability scores were obtained in the remaining two performance conditions. In order, variability scores during the free vision condition, the condition with monitoring of the dominant and nondominant limb, and the blindfolded condition were 0.59, 0.70, 0.52, and 0.61. A-posteriori tests on the data of the non-dominant limb revealed that all pairwise comparisons were significant (P < 0.01 and P < 0.05), except for the comparison between the free vision and blindfolded condition (P>0.05). The remaining two interactions are only of marginal importance and will not be discussed here any further.

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Discussion

More than half a century ago, Von Hoist [37] drew attention to the synchronization between simultaneously active fin movements in fish, for which he coined the term "Magnet Effect". Recent studies on interlimb coordination in humans have generally confirmed the presence of similar synchronization tendencies between the limbs [8, 36] that are sometimes so powerful that alternative movement patterns become difficult to produce, unless practice is provided. The present study confirmed and extended previous evidence of a tight coupling between the upper limbs during the production of twodimensional drawing movements in the transverse plane. No disruptions or transitions in relative phase were observed while subjects were moving according to the symmetrical or in-phase coordination mode (see also [24,

26]). Whereas phase synchronization clearly dominated at the macro scale, interlimb asynchronies became evident at the micro scale of analysis. In spite of instructions to synchronize the limb motions, the present findings revealed that the dominant limb predominantly led the non-dominant limb. Furthermore, this asynchrony was a function of manual dominance and attentional bias. In a general way, the observed asynchrony between the upper limbs supports previous findings by Stucchi and Viviani [26], who identified a similar phenomenon during bimanual ellipse drawing in the frontoparallel plane. They found that the dominant hand led the non-dominant hand by about 15 30 msec, depending on the coordination mode. Whereas Stucchi and Viviani only computed the difference in passage time of the limbs at one location, we computed interlimb phase offsets continuously within each oscillation cycle. In spite of substantial differences in the experimental procedures, in the geometrical features of the task, and in the data analysis (particularly the computation of differences between the relative positions of the hands), similar temporal asynchronies were observed in Stucchi and Viviani's study and our study. Across experimental conditions and groups, the observed average phase offset was 7.11 in the present study. In view of the realized cycle duration which was close to the target duration of 1000msec (i.e. 992msec) this phase difference corresponds to a temporal delay between the limbs of approximately 20 msec. This delay varied across the visual conditions and also differed between left-handers and right-handers (from 0.6 ': to 15.47 °, i.e. from 2 to 43 msec). In previous work with right-handers, similar phase offsets were found during the production of circle drawings with both upper limbs (31msec), whereas the offsets were somewhat smaller during circle drawing with both feet (17 msec) [27]. In addition, overall temporal delays in the order of 15msec were observed during bimanual line drawing [28]. The current delays are higher than the overall values reported by Treffner and Turvey [34] during the swinging of hand-held pendulums in the sagital plane

where the dominant limb led the non-dominant limb only by about 5.4msec. The latter study also reported more inconsistencies in the group of right-handers with respect to the phase lag between the dominant and non-dominant limb. The observed interlimb asynchrony is not simply a consequence of a difference in cycle duration, between the dominant and non-dominant limb, which was less than 2msec. It does not appear to result directly from differences in dexterity between the dominant and nondominant limb either, even though these effects were clearly present as inferred from differences in diameter consistency and in the consistency of the circle drawings. The latter effects would induce some variability in the asynchrony, but not necessarily a particular direction of the asynchrony. The observation of similar interlimb asynchronies in Stucchi and Viviani's study [26] and our study is rather remarkable when considering the task differences. Stucchi and Viviani had their subjects produce ellipsoidal movements in the frontoparallel plane. Moreover, they investigated in-phase (symmetrical) and anti-phase (asymmetrical) movements across various cycling frequencies and in the absence of metronome pacing during data acquisition. The task that we used was more constrained in that subjects generated circle drawings in the horizontal plane while movements were paced by a metronome. A template drawing was available at all times (except during the blindfolded condition). Moreover, we only studied in-phase movements which were performed at a single speed level. However, some of our data do not conform with their findings. First, Stucchi and Viviani did not observe major differences in asynchrony between left-handers and righthanders, whereas we did. Secondly, they contended that attentional biases towards the dominant or non-dominant limb did not play an important role in determining the relative positions of the limbs. Conversely, we found that attentional biases through visual instructions affected the size of the asynchrony. These points of divergence are discussed in more detail next. In the present study, the direction of the phase offset between the limbs was found to be consistent in the majority of right-handers but not in left-handers. The overall phase offset between the dominant and non-dominant limb was 11.41 ~ vs 2 . 8 1 or 32 vs 8 msec for righthanders and left-handers, respectively. Whereas the right hand led the left hand in the majority of right-handed subjects, the left hand only led in four out of ten lefthanded subjects. Among the remaining left-handers, two subjects showed a right-hand leading pattern and the remaining four an inconsistent pattern. These observations are not to be associated with inconsistencies in hand use as only very consistent left-handers were included in the present study. The findings suggest that bimanual control is more complicated and probably less lateralized in left-handers as compared to right-handers. It is commonly agreed that the group of left-handers is

S. P. Swinnen et al./Bimanual asynchronies less uniform than right-handers in brain !ateralization. Accordingly, subdivisions have been proposed. For example, Peters and Murphy [19] showed, by means of cluster analysis, that there may be as many as five handedness subgroups. Left-handers also differ from righthanders with respect to asymmetry patterns in bimanual tasks [17, 18]. It thus remains possible that even a homogeneous group of consistent left-handers (as used in the present study) is composed of subgroups that differ in brain organization in general and in motor control networks in particular. Whereas Stucchi and Viviani [26] did not observe any effects of unilateral attentional allocation on interlimb asynchrony, the present study showed that phase offsets were affected by vision manipulations. Irrespective of the handedness groups, the temporal asynchrony was largest when subjects were instructed to visually monitor the dominant limb and smallest when instructed to monitor the non-dominant limb. Phase offsets in the free-vision condition were located in between the aforementioned conditions. The vision instructions clearly reached their goal as they affected the quality of circle drawing (consistency of intralimb relative phasing and circle diameter). In other words, there was a positive effect on the limb movement that received focal attention, irrespective of whether this happened to be the dominant or non-dominant limb. It is hypothesized that visually mediated attention facilitated the coupling between afferent input sources and motor output whereby the dominant limb control system is more amenable to finer tuning than the non-dominant limb system. The failure to observe an effect of attentional bias in Stucchi and Viviani's [26] study is possibly due to their use of a sound emitter. This sound source was possibly not as pervasive as the visual cueing technique that we used to modulate attentional focus. Nevertheless, even though visual manipulations modulated the interlimb asynchrony in our study, vision was not the main source of the phase offset because it was also observed under blindfolded conditions where its size was similar to that observed under free vision conditions. It appears that the phase offset is inherent in bilateral limb control, which is characterized by a functional asymmetry in the deployment of attention to the limbs and which is dependent upon visuokinesthetic or kinesthetic afferences. This difference in attentional priming is associated with a differentiation in the quality of motor output. That this asynchrony is less clear in left-handers than in righthanders may reflect the former's greater degree of flexibility in allocating attention to both limbs. Given that attentional allocation is compromised in split-brain patients [7], it is reasonable to assume that the corpus callosum plays a prominent role in the organization and control of bimanual trajectories. A final issue that needs to be addressed concerns the locus or origin of the interlimb asynchrony. Stucchi and Viviani [26] suggested that the asynchrony is of central rather than of peripheral origin. More specifically, they

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hypothesized that the asynchrony is due to the necessity of transmitting time-keeping information to the other hemisphere. Not only proximal but also more distal forelimb representations have been found to exhibit a modest-to-dense homotopic callosal projection in animals, depending on the motor cortical area involved [20]. Previous estimates of inter-hemispheric transmission times in reaction-time studies, based on differences between crossed and uncrossed responses to sensory stimuli, have predominantly ranged from l to 10msec (for an overview, see [15]). The asynchronies observed in the present and other studies during bimanual figure drawing have been larger, but this may be a result of task differences. Whereas the interhemispheric transmission time hypothesis cannot be ruled out at the present time, we hypothesize that a multifactorial neural account may lay at the basis of the asymmetry. In addition to interhemispheric transmission times, the asynchrony may be a consequence of differences in the efferent networks controlling both limbs. For example, recent work on transcranial magnetic stimulation has provided support for the notion that hand preference is associated with lateralized differences in the excitability of motor system projections [35]. More specifically, it has been observed that the threshold for activation of the right hand (limb) muscles is lower than that of the left-hand (limb) muscles in righthanders. Underlying this phenomenon may be a differential excitability and synaptic efficacy among the motoneurons involved in the control of the dominant limb as compared to the non-dominant limb. However, even more peripheral phenomena may account for the phase lag. In a multilimb reaction time study, in which subjects were to move as quickly as possible after presentation of a visual stimulus, we observed differences ( < 5 msec) between the motor times of the left and right limb during bimanual elbow flexions [29]. The motor time refers to the time that elapses between the first signs of increased muscle activity and the initiation of limb displacement. Thus, overall motor unit recruitment time to overcome the limb's inertia differed between the dominant and non-dominant limb, but these differences were small and can only account in part for the aforementioned bimanual asynchronies. Bearing in mind this functional asymmetry between both neuromuscular systems, it is conceivable that a feedback-based phase resetting mechanism is in operation to prevent phase differences from exceeding a particular threshold value. It appears that such a mechanism would be necessary to prevent a progressive increase of the phase lag across the duration of the trial. The present findings invite some speculations about the cerebral control of bimanual cyclical coordination. Our observations are consistent with the notion that the left-hemisphere of right-handers plays a primary role in motor control functions in general [13] and interlimb coordination in particular [29]. This is inferred from the fact that the dominant limb led the non-dominant limb and also from the former's overall superior circle drawing

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capabilities. These findings are consistent with the hypothesis that the left hemisphere in right-handers is superior in movement execution [1,2, 21,22]. In addition, the left-hemisphere may also be endowed with superior bilateral control functions that are possibly recruited during the production of bimanual coordination patterns. Clinical evidence suggests that deficits in the left hemisphere affect both limbs, whereas lesions of the right hemisphere predominantly affect the contralateral limbs [4, 41, 42]. Stated differently, left hemisphere lesions also cause motor dysfunctions of the ipsilateral (left) hand. Similarly, studies using functional magnetic resonance imaging have demonstrated a substantial activation of the left motor cortex during ipsilateral movements [111. The present perspective is consistent with Peters' general suggestion that there is an advantage to an arrangement in which the initiation and termination of the movement trajectories in the two hands are issued by a unilateral source [18]. This may be conceived as a lateralized functional module that is responsible for the timing of bimanual periodic movements. Additional research is required to further establish the precise origin of the phase offset and to investigate its dependence on experimental manipulations and subject characteristics. This asynchrony deserves attention along with the ubiquitous tendency for interlimb synchronization. These phenomena are not incompatible, but rather reflect unique features of bimanual control at different scales of analysis.

Acknowledgements--Support for the present study was provided through a grant from the Research Council of K.U. Leuven, Belgium (Contract No. OT/94/30) and the National Fund for Scientific Research in Belgium (Project S 2/5-ND. E 112). The authors are indebted to Prof. C. B. Walter for his insightful comments on an earlier draft of the manuscript.

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