Egocentric and Allocentric Constraints in the Expression of Patterns of Interlimb Coordination

Transcription

1 Egocentric and Allocentric Constraints in the Expression of Patterns of Interlimb Coordination Stephan P. Swinnen and Kris Jardin Motor Control Laboratory, K. U. Leuven Ruud Meulenbroek University of Nijmegen Natalia Dounskaia Russian Academy of Sciences, Moscow Myriam Hofkens-Van Den Brandt Motor Control Laboratory, K. U. Leuven Abstract w Tasks that are easy when performed in isolation become difficult when performed simultaneously in the upper and/or lower limbs. This observation points to basic CNS constraints in the organization of patterns of interlimb coordination. The present studies provide evidence for the existence of two basic coordinative constraints whose effects may be additive under certain conditions. On one hand, the egocentric constraint denotes a general preference for moving the limbs toward or away from the longitudinal axis of the body in a symmetrical fashion and is of primary importance during the coordination of homologous limbs. On the other hand, the allocentric con- straint refers to a general preference to move the limbs in the same direction in extrinsic space and pertains to the coordination of nonhomologous limbs (eg., various combinations of the upper and lower limbs). In the present context, constraints are considered as expressions of basic features of CNS operation that give way to preferred coordination patterns to which the system is naturally drawn or biased. The identification and description of these constraints is considered of critical importance to obtain a better understanding of the control of coordination patterns. INTRODUCTION The majority of the daily motor tasks that humans perform require some degree of coordination among segments of a limb and/or between limbs. These actions are performed against the background of postural control mechanisms that anticipate for the possible destabilization induced by these focal actions. Whereas many studies have dealt with unilateral goaldirected movements such as reaching and grasping, considerable efforts have recently been made to uncover the basic modes of interlimb coordination during the production of discrete and cyclical movements. These efforts are inspired by the general observation that certain tasks, performed easily in isolation, become difficult when performed simultaneously. Apparently, these difficulties are associated with the violation of elementary constraints imposed by the central nervous system and/or by the biophysical architecture of the motor apparatus. Even though we are still Massacbuselts Institute of Technology a long way from a well-established description of these constraints, recent experimental efforts have made significant advances in this respect. For example, two preferred modes of interlimb coordination have been identified to which the human motor system is naturally drawn, that is, the in-phase (I$ = 0') and anti-phase mode ($ = 180') (Kelso, 1984; Schoner & Kelso, 1989; Turvey, 1990). Within this context, relative phase has been proposed as an adequate collective variable or abstract relational quantity that characterizes the ordered spatiotemporal patterning between the moving segments or limbs. When extending this principle, it appears that no uniform taxonomy currently exists to categorize coordination modes along the in-phase/anti-phase dichotomy. The pragmatic convention that has predominantly been used in past research is to refer to the most stable of Journal of Cognitive Neuroscience 9.3, pp

2 both patterns as the in-phase mode and to the least stable as the anti-phase mode, irrespective of the criterion that is implicitly embedded in such a categorization. Whereas muscle pairing has inherently been used as the principal criterion for bimanual (upper limb, hand, wrist, and finger) coordination tasks, an extrinsic spatial criterion has emerged from coordination research involving combinations of the upper and lower limbs. We will refer to the former as the egocentric and to the latter as the allocentric principle or constraint. The egocentric constraint is defined with respect to the longitudinal axis of the body (intrinsic space coordinates). It refers to the observation that bilaterally symmetrical movements, requiring the simultaneous activation of homologous muscles, are performed more accurately and consistently than asymmetrical movements involving nonhomologous muscles. Therefore, it can also be referred to as the mirror-image or iso-muscular constraint. During symmetrical movements, the homologous limbs move toward or away from the body midline or longitudinal axis together. In the case of asymmetrical movements, one limb is moved toward the body while the other is moved away from the body midline. The allocentric constraint is defined with respect to extrinsic space coordinates and refers to the fact that some categories of limb movements made in the same direction are produced more accurately and consistently than movements in different directions. Evidence sup porting the important role of both principles in the organization of coordination patterns is discussed next. When performers are faced with performing discrete bimanual movements that differ in their spatiotemporal pattern, they often encounter (mutual) synchronization tendencies, that is, each limb tends to adopt the features of the other limb (Franz, Zelaznik, & McCabe, 1991; Heuer, 1985; Marteniuk, MacKenzie, & Baba, 1984; Sherwood, 1994). It often takes substantial amounts of practice to overcome this effect (Swinnen, Young, Walter, & Serrien, 1991; Swinnen, Walter, Beirinckx, & Meugens, 1991; Swinnen, Walter, Lee, & Serrien, 1993; Walter & Swinnen, 1990,1992,1994). The ubiquitous tendency for interlimb synchronization has also been documented for cyclical bimanual movements. This becomes particularly evident when high-speed requirements are imposed on the subject. For example, when a subject is initially prepared in the asymmetrical (anti-phase) mode after which the cycling frequency is increased, a transition occurs to the symmetrical (in-phase) mode unless this change is intentionally resisted (Kelso, 1984; Carson, Byblow, & Goodman, 1994). Beyond a critical frequency, only the symmetrical coordination mode can be produced with a high degree of stability. As a result of this elementary tendency for phase and frequency synchronization, alternative coordination modes are difficult to produce. While the majority of past coordination studies involved the coordination of the upper limbs (homolo- gous), some have addressed the coordination of upper and lower limbs (nonhomologous). For example, Baldissera, Cavallari, and Civaschi (1982) investigated the production of parasagittal movements of the homolateral (ipsilateral) wrist and foot and found that movements in different directions (one limb moving up while the other moves down) were more difficult to produce than movements in the same direction (both limbs moving up or down together). Direction was defined according to extrinsic space coordinates. The authors stated that performing limb movements in different directions (non-isodirectional) required a strong attentive effort from the subject and often resulted in a tendency to reverse spontaneously to the easier (iso-directional) pattern under increasing cycling frequency conditions. Because the former pattern was found to be more vulnerable to destabilization than the latter pattern, irrespective of hand position (prone or supine), the authors concluded that coordinative stability was primarily determined by the spatial relationship between the limb movements instead of particular patterns of muscle pairing. Subsequent experiments involving different limb segments on the same and different side of the body have further underscored the role of direction as a principal determinant of coordinative stability (Kelso & Jeka, 1992; Swinnen, Dounskaia, Verschueren, Serrien, & Daelman, 1995). The aforementioned coordinative principles or constraints have so far been identified in relative isolation of each other. Furthermore, these principles have been associated with different limb combinations as well as different planes of motion. Therefore, it largely remains to be determined under which experimental conditions the aforementioned principles hold. Another issue of interest is whether the egocentric and allocentric constraints are additive or subtractive in determining coordinative stability when both apply under particular experimental circumstances (e.g., coordination patterns requiring the activation of homologous muscle groups and occurring in the same versus different allocentric directions). Finally, it remains to be investigated whether the aforementioned allocentric principle is limited to particular planes of motion and limb combinations or whether it represents a global constraint that determines coordinative stability. The present experiments were designed to address the role of the egocentric and allocentric constraints during the coordination of the homologous and nonhomologous limbs. Whereas the majority of previous coordination studies made use of unidimensional recordings, we studied two-dimensional circular drawing patterns. In addition to these trajectory requirements, a particular coordination mode between the limbs was to be maintained. In Experiment 1, use was made of a bimanual circle drawing task. In Experiment 2, homologous, homolateral, and heterolateral limb combinations were studied. All movements were produced in the transverse or paratransverse plane and involved two relative phase Swlnnen et al. 349

3 modes between the limbs with respect to both the X- and Y-axis component of the two-dimensional movements. EXPERIMENT 1 The present study addressed the role of the egocentric and allocentric constraint during bimanual coordination. Subjects were instructed to produce eight bimanual tasks that differed from each other with respect to the relationship between the limbs along the X- and Y-axis component. Circular trajectories can be decomposed into two sinusoidal motions that occur in orthogonal directions with a 90" phase offset between both signals. Use was made of two digitizers that registered displacement of the stylus with respect to the parasagittal (Yaxis) and transverse (X-axis) dimensions. Four different types of relative phasing patterns were tested using various combinations of clockwise and counterclockwise motions: (1) X-axis in-phase / Y-axis in-phase (Xh/Y,,J; (2) X-axis anti-phase / Y-axis in-phase (Xanti/Ka; (3) X-axis in-phase / Y-axis anti-phase (Xin/Yanti>, and (4) X-axis anti-phase / Y-axis anti-phase (Xanti/Yanti>. In-phase movements involved the simultaneous activation of homologous muscle groups, whereas anti-phase movements involved nonhomologous muscle groups. When categorizing the movements according to an extrinsic spatial reference frame, the in-phase pattern along the X-axis required the limbs to move in opposite directions, whereas the anti-phase pattern resulted in iso-directional movements. Along the Y-axis, however, the in-phase coordination pattern corresponded with limb movements in the same direction and the anti-phase pattern with movements in different directions. Thus, whereas the egocentric and allocentric constraints converged along the Y-axis component, they did not along the X-axis component. This set of conditions was expected to provide insights into the degree of convergence between both principles and has not been investigated previously. The quality of between- and within-limb coordination was quantified using relative phase analyses. Our first aim was to investigate the generalizability of the differential accuracy and consistency of the in-phase and antiphase coordination modes across more complex coordination patterns and with respect to both movement dimensions (X and Y). In addition, it was hypothesized that the egocentric constraint plays a more important role than the allocentric constraint during coordination of the homologous limbs. Because the primary focus of the study pertained to unravelling the coordination constraints under a variety of bimanual coordination conditions that varied in complexity, no manipulation of cycling frequencies was administered. A second goal was to investigate the potential existence of a small but distinct phase offset between the limbs. There is currently some discrepancy in the literature with respect to this phenomenon. While Stucchi and Viviani (1993) observed a lag between both limbs during ellipse drawing, Semjen et al. (1995) failed to confirm this finding during the production of circles. Method Subjects Twelve undergraduate students of the Katholieke Universiteit Leuven participated in the experiment. All subjects (eight males, four females) were right-handed as assessed by the Oldfield questionnaire. They had not been previously involved in a similar experiment and were not paid for their services. Apparatus and Task The apparatus consisted of two XYdigitizing tables (LC2O-TDS Terminal Display Systems) positioned in the horizontal plane in front of the subject. The accuracy of registration was 0.25 mm. 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- and Y-axis component at a sampling frequency of 150 Hz. The X-axis component was parallel to the transverse plane, and the Y-axis component was parallel to the sagittal plane and perpendicular to the X-axis. A computercontrolled electronic metronome indicated the goal cycling frequency (1 Hz). Subjects were seated on a height-adjustable chair with one digitizer on the left of their median plane and the other on the right (Figure 1). They were comfortably seated with both forearms and elbows positioned just above the surface of the tables. The task consisted of tracing the contour of a target circle (diameter: 8 cm) that was affixed to each digitizer. The distance between the centers of both circles was 35.8 cm. Subjects were instructed to draw one circle with each limb per second. Each trial lasted 15 sec. The movements always started with the tip of the stylus positioned at the center of the circle. The first stroke following movement initiation was upward in the first four conditions. In the remaining conditions, the left hand moved upward whereas the right hand moved downward. Procedure Subjects were instructed to generate the circle drawings while attempting to produce and maintain the prescribed relative phasing patterns between the limbs. There were eight bimanual task conditions (Figure 2). Condition I and I1 required the simultaneous activation of homologous muscle groups at all times with respect to both the X- and Y-axis component. These mirror movements were executed inward or outward, that is, one limb produced a clockwise rotation and the other 350 Journal of Cognitive Neuroscience Volume 9, Number 3

4 Figure 1. View of the experimental apparatus: the bimanual digitizer setup. a counterclockwise rotation (X in-phase/y in-phase, or Xin/Yin). Conditions I11 and IV were characterized by the simultaneous activation of homologous muscle groups along the Y-axis and nonhomologous muscle groups along the X-axis, resulting in clockwise or counterclockwise movement directions for both hands, respectively (X anti-phase/y in-phase, or X,,i/Yin). Conditions V and VI required the activation of homologous muscle groups with respect to the X dimension and nonhomologous groups with respect to the Y dimension (X in-phase/ Y anti-phase, or Xi,,/Yanti). The final two conditions (VII and VIII) required the simultaneous activation of nonhomologous muscles along both movement dimensions, resulting in a clockwise movement for one limb and a counterclockwise movement for the other limb (X antiphase/y anti-phase, or Xanti/Yanti). Subjects were instructed to maintain the required phasing pattern as well as possible while obeying the imposed cycling frequency. Before initiation of a trial, the stylus was positioned on the center of the circle. Following the ready command by the experimenter, subjects received a start command and pacing of the metronome was initiated. Prior to data acquisition, two unimanual trials (one for each limb) were provided to familiarize the subject with the task. hvo trials of each experimental condition were registered following one bimanual warm-up trial. 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 amplitude measures as well as the relative phasing between the X- 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 Diametez The spatial measure of the left and right limb motions consisted of the absolute value of the peak-positive to peak-negative amplitude for each individual cycle along the X- and Y-axes (= diameter). Means and SDs 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 Swinnen et al. 351

5 CONDITION LEFTHAND RIGHT HAND PHASE PATTERN ALLOCENTRIC DIRECTION X: in-phase different direction Y: in-phase same direction I X: in-phase different direction Y: in-phase same direction X: anti-phase same direction Y: in-phase same direction X: anti-phase same direction Y: in-phase same direction X: in-phase different direction Y: anti-phase different direction X: in-phase different direction Y: anti-phase different direction viii 0 Q X: anti-phase same direction Y: anti-phase different direction X: anti-phase same direction Y: anti-phase different direction Jn-phase : homologous muscles activated simultaneously : mirror movements. Anti-phase : non-homologous muscles activated simultaneously : non-mirror movements. Figure 2. Schematic representation of the experimental conditions of Experiment Journal of Cognitive Neuroscience Volume 9, Number 3

6 peaks along the X-axis component. Means and SDs were calculated for each cycle and were averaged across the two trials of each condition. The metronome-imposed cycle duration was 1000 msec. Relative Phase. 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 relative phase, provides a signature of the coordination pattern that is observed between the limbs (Haken, Kelso, & Bunz, 1985; "urvey, 1990). The continuous phase of the X- and Y-axis component of each arm oscillation was calculated, using a formula adapted from Kelso, Scholz, and Schoner (1986). Subsequently, relative phase between the limbs was computed according to the following formula: whereby OR refers to the phase of the right arm movement at each sample, XR is the position of the right forearm after rescaling to the interval [-1,1] for each cycle of oscillation, and dx,/dt is the normalized instantaneous velocity. 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 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. It is therefore possible to represent the state of that system by polar coordinates (0 to 360") instead of the Cartesian coordinates. This is accomplished through the formula shown above. When using polar coordinates, the state of the system is described by its angular coordinate or phase angle (and radius). 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. Following computation of the continuous estimate of relative phase with the formula shown above (using the range 0 to 180" and -180 to 0' per unit circle), the absolute difference in phase angle was extracted at the two peak position landmarks of the reference limb. Accordingly, the program routine provided two sets of phase differences, one at peak extension and one at peak flexion of the limb. These data were subsequently averaged to provide an estimate of relative phase accuracy. The SD around the mean relative phase was computed to obtain an estimate of the variability in relative phase. As mentioned previously, use was made of an absolute double discrete measure of relative phase that ranged between 0 and 180' in order to compare the quality of interlimb coordination across experimental conditions. While this unsigned measure fails to reveal which of two limbs leads or lags, it has the advantage that it can be applied to signals whose phase relation is unstable and displays transitions. In addition to the absolute measure, a signed measure of relative phase was used to study interlimb phase offsets, and this technique was only applied to those conditions characterized by relatively stable coordination patterns. To assess the quality of circle drawing within each. x-axis - Y-axis 0 1 7, Displacement X-axis (a) (b) Flguie 3. Displacement-time traces of the X- and Y-axis Component (a) and the resulting circle drawing (b). Swinnen et al. 353

7 limb in addition to the X and Y measures of diameter noted above, a relative phase analysis was computed between the oscillatory X- and Y-axis components (ex - &), using a procedure similar to the one previously described for assessing interlimb coordination. This analysis was based on the premise that a perfect circle drawing is characterized by a 90" phase offset between the X- and Y-axis component. This is exemplified in Figure 3 where the oscillatory displacement traces of the X- 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. While 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. Because this analysis does not distinguish between performing a circle and an ellipse, it is necessary to complement it with measures of the X- and Y-axis diameter. These diameters are the same for a circle but deviate from each other when ellipses are drawn. Results Cycle Duration A 2 x 4 (Body Side x Coupling Pattern) repeated measures ANOVA was conducted on the mean cycle duration scores as well as on the variability of cycle duration. Body side referred to the left and right arm. Coupling pattern consisted of four levels: XuJYh, Xmti/Yh, Xin/Yanti, and Xanti/Ymti. The analysis of mean cycle duration revealed a significant effect for body side, F(1, 11) = 40.79, p <.01 (MSe = 86.46). Average cycle duration in the left limb was 8 msec slower than in the right limb (M = msec, M = msec, respectively). The differences in cycle duration between the four coupling patterns were not significant, F(3, 33) < 1 (MSe = ). Means for the four conditions were: M Xh/Yh = msec, M Xmti/Y, = msec,mxiljymti = msec, and M Xmti/Ymti = msec. The interaction between both factors was not significant (p >.05). The analysis of cycle duration variability showed no significant main effects: body side, F(1, 11) = 4.37, p >.05 (MSe = ), coupling pattern, F(3, 33) < 1. The interaction effect was not significant either (p >.05). Diameter A 2 x 4 x 2 (Body Side x Coupling Pattern x Movement Axis) repeated measures ANOVA was applied to the mean diameters (peak-to-peak amplitudes) of the circle as well as their SDs. Movement axis referred to the X and Y dimension. The statistical analysis revealed that the mean diameter of the left circles (M = 8.67 cm) was significantly larger than the diameter of the right circles (M = 8.11 cm),f(l, 11) = 24.17,p c.01 (MSe = 1.25). The main effects of coupling pattern and movement axis were not significant,f(l, 11) c 1, and F(1, 11) = 4.25,p >.05 (MSe =.85), respectively. None of the interaction effects were significant (p >.05). With respect to the variability of the diameters, significant main effects for all three variables were identified: body side, F(1, 11) = 26.41,~ <.01 (MSe =.08); coupling pattern, F(3, 33) = 7.64,p <.01 (MSe =.02); and movement axis,f(l, 11) = 55.34,p <.01(MSe =.03). The diameters of the left-hand circle (M = 0.66 cm) were less consistent than those produced with the right-hand (M = 0.51 cm). With respect to the coupling patterns, the most consistent diameters were observed when both limbs moved in-phase along both axes (M Xin/Yin = 0.53 cm). Variability scores in the remaining coupling conditions were significantly higher (M Xanti/Yin = 0.58 cm; M Xmti/Ymti = 0.59 cm; M XuJYanti = 0.63 cm) (p <.05 and p c.ol). Finally, the variability in amplitude was higher along the X-axis (M = 0.65 cm) than along the Y-axis (M = 0.51 cm). None of the interaction effects reached significance (p >.05). Within Limb Relative Phase Analyses Preliminary analyses revealed that the variable referring to direction sense (clockwise versus counterclockwise) did not show any significant effects. Therefore, it was excluded from subsequent analyses. The absolute deviation from the required 90" phase offset between the X- and Y-axis components was computed as well as the variability of these scores. A 2 x 4 (Body Side x Coupling Pattern) repeated measures analysis of variance (ANOVA) was conducted on the relative phase error and variability scores separately. The analysis of relative phase error revealed that the absolute deviation from the required relative phase of 90" was simcantly larger for the left arm (M = 9.19") than for the right arm (M = 5.93"),F(1, 11) = 41.12,p <.01 (MSe = 12.4). The error scores were not significantly affected by the coupling pattern,f(3,33) = 2.18,p >.05 (MSe = 3.07) (M Xh/Yin = 7.77"; M Xa"ti/Yh = 7.41"; M Xh/Yanti = 7.95"; M Xanti/Ymti = 7.12'). No significant interactions were observed (p >.05). Analysis of the variability scores revealed a significant main effect for body side,f(l, 11) = 88.81,p <.01 (MSe = 4.48). Circles drawn with the left (nondominant) limb (M = 8.23") were less consistent than those drawn with the right (dominant) limb (M =.5.35"). The main effect of coupling pattern was also significant, F(3,33) = 6.35, p c.01 (MSe = 2.32). SD scores for the homologous coupling pattern (MXh/Yh = 6.16") were lower than for the remaining coupling patterns. The highest SD scores were observed for the task that required movements in opposite directions along both axes according to extrinsic space coordinates (M XiJYmti = 7.51 "). The remaining two coupling patterns were positioned in between 354 Journal of Cognitive Neuroscience Volume 9, Number 3

8 the aforementioned patterns (M Xanti/Yh = 6.81"; M Xmti/Yanti = 6.70'). A differential effect of coupling pattern was observed with respect to the right as compared to the left limb circles, resulting in a significant Body Side x Coupling Pattern interaction, F(3,33) = 10.02,p c.01 (MSe =.51) (Figure 4). Whereas the variability measures were similar among the four coupling patterns for the right limb, they diverged more in the left limb. Under the latter circumstances, the lowest SD scores were observed for the X-,/Ym condition, followed by the Xanti/Yanti,Xanti/Y-,, and X,,,/Yanti condition. Between Limb Relative Phase Analyses Graphical representation of some bimanual coordination conditions. Typical relative motion plots of a representative subject are shown for the most stable and least stable experimental condition (Figures 5a and 5b). Performance of the XJYh coupling pattern, requiring the simultaneous activation of homologous muscle groups at all times, is shown in the upper graph (Figure 5a). The relative motion plots representing the circle drawing are 107 -ff XantiIYin 8 +- XinIYanti E "I +- XantiIYanti $ 7 d n5 Left \ I I Right Body Side Figure 4. The interaction between body side and coupling pattern with respect to the standard deviation of relative phase. shown on top. The displacement profiles of the X- and Y-axis dimensions of both limbs as a function of time are represented underneath the circle drawings. As can be Figure 5a. Circle drawings produced in the left and right limb for a representative subject during the Xi,/Ya coupling conditions. Left Arm FIGURE 5 A XinMin Right Arm z - I I & Displacement X-axis i ; Displacement X-axis 8 n E 6 0 Y - 4 1: x-axis 8 n E 6 s [ o Y-axis p -2.- n 4 4 Swinnen et al 355

9 Figure 5b. Circle drawings produced in the left and right limb for a representative subject during the XantJYanti coupling conditions. Lett Ann FIGURE 5 6: XaWanti Rlght Arm 6 'P $.:.g Displacementx-axis Displaeanentx-axis x-axis Time (8) 8 8Y o o -F& -2 a 4 4 Y-axis observed, this pattern of interlimb coordination requiring mirror movements along both axes is performed with a high degree of stability without any noticeable phase deviation or transition. This was the case for all subjects. The least stable pattern requires anti-phase coordination along both the X- and Y-axis component and is shown in Figure 5b. This condition was most vulnerable to phase transitions. Inspection of this pattern across subjects revealed considerable interindividual differences. Few subjects succeeded in performing the required coupling pattern without showing transitions. Following the transition, the X,,,/Kn pattern predominated (Figure 5a). Across all experimental conditions, phase transitions occurring with respect to one axis were always accompanied by phase transitions in the other axis, implying that the direction of rotation of the circles was never changed from clockwise to counterclockwise or vice versa. A more detailed analysis of the phase transitions through interactive graphics demonstrated that not a single transition was observed during the X-,/Y, coupling pattern. In the XmtdY-, and X-,/Ymti coupling pat- tern, transitions were observed on 4 and 44% of the trials, respectively. The largest number of transitions were observed during the Xmti/Yanti coupling pattern, namely on 75% of the trials. The transition route observed in the latter trials was not always from anti-phase to in-phase but also vice versa, possibly reflecting the subjects' intentions to reestablish the required patterns. Accuracy and Consistency of Relative Phasing. The statistical analysis was focused on the absolute deviations from the target relative phasing pattern as well as on the SDs of relative phase. A 2 x 2 (Relative Phase Pattern x Movement Axis) repeated measures ANOVA was conducted on both the absolute error and consistency measures. The relative phase pattern consisted of two levels (i.e., in-phase and anti-phase). The variable movement axis pertained to the X- and Y-axis component. Analysis of the absolute error scores showed a significant main effect for relative phase pattern, F(1, 11) = 44.49,~ c.01 (MSe = ). The in-phase pattern (M = 29.5') was performed more accurately than the anti- 356 Journal of Cognitive Neuroscience Volume 9, Number 3

10 Figure 6. The interaction between phase pattern and movement axis with respect to relative phase error (a) and the standard deviation of relative phase (b). P In-phase Anti-phase In-phase Anti-phasc Phase Pattern PhasePattern (a) (b) phase pattern (M = 81.66"). The main effect of movement axis was not significant, F(1, 11) = 1.58,p >.05 (MSe = 6.68). However, the interaction between phase pattern and movement axis was significant, F(1, 11) = 15.14,~ c.01 (MSe = ) (Figure 6, left side). The in-phase pattern was performed less accurately along the X-axis than along the Y-axis. Conversely, the anti-phase pattern was performed more accurately along the X-axis than along the Y-axis. Analysis of the variability scores showed a significant main effect for relative phase pattern, F(1, 11) = 16.49, p c.01 (MSe = 29.16), and movement axis, F(1, 11) = 23.59,p c.01 (MSe = 1.28), the in-phase pattern (M = 11.82') was performed more consistently than the antiphase pattern (M = 18.16") and the coordination patterns were more variable along the X-axis (M = 15.79') than along the Y-axis component (M = 14.20'). The interaction between phase pattern and movement axis was also significant, F(1, 11) = 24.62,p c.01 (MSe = 19.95) (Figure 6, right side). Whereas differences in consistency between the in-phase and anti-phase modes were very small along the X-axis (Mh-phase = 15.82'; Manti-phase = 15.75'), larger differences were observed along the Y-axis component (&&,-phase = 7.83'; Mmti-phase = 20.56'). In addition to the previous ANOVA's, the absolute error and SD data were also analyzed by means of a one-way ANOVA with four repeated measures for coupling pattern (i.e., X,,,/Y.,, X,JYh, XdY,ti, and XmJYmti). In other words, the previous variables for phase pattern and movement axis were combined into one factor with four levels. With respect to absolute phasing error, a significant main effect for coupling pattern was observed, F(3, 33) = 28.68,p c.01 (MSe = ). The X,,,/Yh pattern was performed most successfully (M = 12.88'), followed by the X,dYh (M = 22.64'), XJY,ti (M = 71.76'1, and X,JY,ti pattern (M = '). Analysis of the variability scores revealed a significant main effect for coupling pattern, F(3, 33) = 12.35,p c.01 (MSe = ). The SD's gradually increased in the following order: X,,,/yin (M = 6.53'), X,dYh (M = 11.40'), XmJYmti (M = 18.03") to X,,,/Ymti condition (M = 24.00"). Signed Relative Phasing Measures. To investigate the potential existence of any phase lag between both limbs, the signed relative phasing scores were analyzed with respect to the stable X,,,/Yh and XmtdYh conditions. The right limb served as the reference limb. The relative phase was calculated with respect to the reference interval [-n, +n] for in-phase patterns and [0, 2x1 for the anti-phase patterns. A 2 x 2 (Coupling Pattern x Movement Axis) repeated measures ANOVA was conducted on the signed relative phase data. Coupling pattern consisted of two levels: the X,,,/yi,, and X,,JYh pattern. Movement axis referred to the X- and Y-axis dimension. The mean scores generally confirmed that the left hand lagged with respect to the rat hand. The effect for movement axis was significant, F(1, 11) = 10.69,p c.01 (MSe = 9.15). Phase lagging of the left hand was smaller along the Y-axis (M = 9.90') than along the X-axis (M = 12.75'). The difference between the X,,,/Yh (M = 9.65") and the X,tJYh (M = 13.00') coupling pattern was not significant, F(1, 11) = 2.44,~ >.05 (MSe = 54.82). The interaction effect was not significant either (p >.05). Inspection of the continuous signed relative phase traces through interactive graphics revealed that this phase lag was not constant but showed some variation across the 15-sec trial duration. Discussion Previous work on bimanual coordination has provided evidence for the existence of two preferred and stable modes of coordination, called symmetrical (in-phase) Swinnen et al. 357

11 and asymmetrical (anti-phase) (Cohen, 1971; Kelso, 1984; Kelso et al., 1986; Stucchi & Viviani, 1993). Moreover, it has generally been confirmed that the former mode is produced with higher degrees of stability than the latter. The present experiment confirmed and extended these observations to two-dimensional drawing tasks in which interlimb coordination modes were manipulated with respect to both the X- and Y-axis component, resulting in four distinct coupling patterns. Analyses of interlimb relative phasing confirmed that the in-phase mode (he mologous muscle groups) was produced with a higher degree of accuracy and consistency than the anti-phase mode (nonhomologous muscle groups), underscoring the importance of the egocentric constraint in bimanual coordination. Even though the egocentric constraint dominated, the extrinsic spatial orientation of the limb movements also appeared to affect bimanual coordination. This is inferred from the significant interaction observed between coupling mode and movement dimension. While in-phase movements were produced with higher accuracy and consistency with respect to the Y-axis than with respect to the X-axis, anti-phase movements were generated more successfully along the X- than along the Y-axis component (Figure 6). This finding is possibly mediated by the allocentric constraint. More specifically, the coupling patterns that were found to be most accurate and consistent within the in-phase and anti-phase mode involved limb motions in the same allocentric direction (i.e., in-phase movements with respect to the Y-axis component and anti-phase movements with respect to the X-aiis component). Thus, while the egocentric constraint was dominant, the effect of the allocentric constraint was possibly superposed on the effect of the egocentric constraint. The aforementioned account is also supported by the statistical analysis involving the four levels of coupling pattern. The analysis of relative phase error revealed that the Xh/Y, pattern (homologous muscle groups) was produced most accurately at all times. The XmtdYmti pattern (nonhomologous muscle groups) was found to be least accurate. The two remaining coupling patterns demonstrated intermediate accuracy: the XmtdYm pattern was produced more accurately than the XuJYmti pattern. While the former involved iso-directional movements with respect to both dimensions according to extrinsic space coordinates, the latter pattern involved non-iso-directional movements with respect to both dimensions. The pattern of data observed with respect to the SD of relative phase was similar, except that the variability of the X,,,/Ymti pattern was lower than that of the XmtdYanti pattern. This is not surprising because subjects, trying to perform the more difficult Xmti/Ymti pattern, exhibited more frequent phase transitions than in the remaining conditions. This resulted in the production of incorrect but more stable in-phase coupling patterns. Often, these transitions occurred early in the trial. Finally, assessment of the quality of circle drawing by means of relative phase analyses between the X- and Y-axis component within each limb further underscored that the most consistent circle drawings were produced under the Xh/yin interlimb coupling mode. The highest variability was observed in the Xin/Yanti condition. The remaining two coupling conditions were positioned in between the aforementioned patterns and did not differ substantially from each other. In summary, two principles appear to determine the accuracy and stability of bimanual coordination patterns. Most important is the egocentric constraint, or the general preference to activate the homologous muscles simultaneously: It results in symmetrical movements with respect to the longitudinal axis of the body. Of secondary importance is the allocentric constraint, or the general preference to move the limbs in the same direction according to extrinsic space coordinates. It appears that the effects induced by the allocentric constraint are superposed on those exhibited by the egocentric constraint during bimanual coordination. While the limbs appeared tightly synchronized in the Xh/Yh and Xmti/Y, conditions, detailed analyses of the signed relative phase scores revealed a small but distinct asynchrony or phase offset between the right and left limb. The dominant right limb led the nondominant limb by 9.65" in the XJYh pattern and by 13.00" in the XmtdYh pattern. Considering that subjects orbited through a 360" phase angle in approximately 1 sec (i.e., 1009 and 1010 msec), the aforementioned phase lags represent temporal offsets of about 27 and 36 msec, respectively. These temporal offsets are close to those reported by Stucchi and Viviani (1993) with respect to ellipse drawing. In agreement with their findings, we also observed larger offsets during anti-phase than during in-phase coordination. Stucchi and Viviani (1993) argued that this time delay between both limb motions was a consequence of the lateralization of timing commands for periodic bimanual movements, necessitating the transmission of timekeeping information to the other hemisphere. While previous studies reporting performance differences between the dominant and nondominant hand have predominantly compared both limbs under unilateral performance conditions, the present study demonstrated that the superior performance of the dominant limb also became evident under bimanual performance conditions. This was inferred from fhe within-hb relative phase analysis between the x- and Y-axis component, showing a more successful production of the circle in the right than in the left limb. Furthermore, the diameter of the right limb circle was more consistent than the diameter of the left limb circle. These observations open interesting perspectives for the assessment of hand dominance or manual lateralization under bimanual in addition to the conventional unirnanual performance conditions. 358 Journal of Cognitive Neuroscience Volume 9, Number 3

12 Experiment 1 confirmed the decisive role of the egocentric constraint with respect to bimanual coordination. Moreover, a subordinate role for the allocentric constraint was hypothesized to account for the interaction between coupling mode and movement dimension. Experiment 2 focused on the generalizability of these constraints across various two-limb combinations: homologous, homolateral (ipsilateral), and heterolateral (diagonal). A first series of hypotheses related to the generalizability of both coordination constraints. To our knowledge, the egocentric or mirror-image symmetry constraint has so far only been demonstrated under bimanual performance conditions even though it appears plausible that it can at least be generalized to bilateral leg coordination. Furthermore, the question remained whether the egocentric principle is limited to task conditions that involve strictly homologous muscle groups or whether it can be expanded to different muscle groups that share the same function (e.g., the internal rotators or the extensors of the arm and leg during two-limb coordination). Previous research dealing with the role of the allocentric constraint was limited to performance of unidmensional hand and foot or arm and lower leg patterns in the parasagittal plane (Baldissera et al., 1982; Baldissera, Cavallari, Marini, & Tassone, 1991; Kelso & Jeka, 1992; Swinnen, Dounskaia et al., 1995). The present experiment provided a unique set of conditions to investigate the generalizability of this constraint across twodimensional movements performed in a different plane of motion: (para-)transverse instead of parasagittal. It was predicted that the extrinsic or allocentric constraint generalized across effector combinations and planes of motion. A second series of hypotheses pertained to the differences among effector combinations. Based on previous findings in humans (Kelso & Jeka, 1992; Swinnen, Dounskaia et al., 1995) and animals (Cruse & Warnecke, 1992; Halbertsma, 1983; Wetzel & Stuart, 1977), it was predicted that interlimb coordination is produced more accurately and consistently in the homologous than in the nonhomologous effector combinations. In addition, heterolateral effector coordination was predicted to be more accurate and consistent than homolateral coordination (Swinnen, Dounskaia et al., 1995). A final goal of Experiment 2 was inspired by the previously observed small but significant asynchrony between the upper limbs. More specifically, the question was addressed whether this phase lag was unique to the bimanual case or whether it was also evident during bilateral leg coordination and/or during the coordination of the upper and lower limbs. Inclusion of coordination patterns involving limbs on the same and different sides of the body was considered potentially interesting to further unravel the origin or locus of the phase lag, particularly with respect to Stucchi and Viviani's (1993) interhemispheric transmission hypothesis. Method Subjects 'helve 20- to 24-year-old female undergraduates enrolled at the Katholieke Universiteit Leuven participated in the experiment. All subjects were declared righthanded and right-footed on the basis of the Oldfield questionnaire, which was expanded with two practical tests on foot preference (i.e., kicking a ball and picking up an object with the toes). None of the subjects had been previously involved in a similar experiment. Apparatus and Task The same dual digitizer setup was used as in the previous experiment. The position of the boards depended on the effector combination. The digitizers were positioned horizontally and parallel to each other on the table during homologous arm coordination and on the floor during homologous leg coordination. For the remaining limb combinations, one digitizer was placed on the table and the other on the floor.the task consisted of tracing the contour of a target circle (diameter: 9 cm), which was drawn in black on each digitizer. The horizontal distance between the centers of both circles was 41 cm for the homologous and heterolateral (diagonal) conditions and 9 cm for the homolateral (ipsilateral) conditions. In the latter conditions, the center of the circle for the upper limb was located more laterally than for the lower limb in order not to physically prevent visual control of these limbs in case subjects desired to do so. To alleviate the normally required substantial isometric contraction of the hip flexors to lift the legs from a seated position, both upper legs were supported by a sling that was attached to the ceiling by means of ropes. This bandage suspended the distal part of the upper leg, which was held in a horizontal position. Consequently, muscle activity was only required to produce the circle task. A Plexiglas sole was attached underneath the foot, and it contained a lcm hole between metatarsal 1 and 2 to firmly stabilize the pen during circle drawing. Similar to Experiment 1, subjects were instructed to draw circles continuously for a duration of 15 sec and at a cycling frequency of 1 Hz. Six effector combinations were performed: (1) homologous arms, (2) homologous legs, (3) homolateral or ipsilateral left (left arm and left leg), (4) homolateral right (right arm and right leg), (5) heterolateral 1 (right arm and left leg), and (6) heterolatera1 2 (left arm and right leg) (Figure 7). Within each effector combination, four different coupling patterns were performed, consisting of a combination of two coupling modes (in-phase and anti-phase) and two movement dimensions (X- and Y-axis component). Swinnen et al. 359

13 HOMOLOGOUS ~~ ~~ ~ HETEROLATERAL HOMOLATERAL HETEROLATERAL HOMOLOCOUS ARMS HOMOLOCOUS LEGS RIGHT ARM/ LEFT ARM I HOMOLATERAL LEFT HOMOLATEPAL RIGHT LEFTLFG RIGHT LEG x-axis : in-phase Y-axis : In-phase left arm right arm X-axis : anti-phase Y-axis : left arm right arm In-phase x-axis : in-phase Y-axis: anti-phase left arm right arm left right 0 arm I left x-axis : anti-phase Y-axis: anti-phase left arm right arm 00 Figure 7. Schematic representation of the experimental conditions of Experiment 2 In view of previous evidence for the primary role of the egocentric constraint during bimanual coordination and for the allocentric constraint during coordination of the upper and lower limbs, the following convention was used in the present experiment to categorize coordination patterns according to the in-phase and antiphase mode. For the homologous effector combinations, use was made of a categorization based on egocentric or body space coordinates: Patterns requiring the simultaneous activation of homologous or nonhomologous muscle groups were defined as in-phase and anti-phase, respectively. For all the remaining effector combinations involving the upper and lower limbs, the mutual direction of the limb motions according to allocentric or extrinsic space coordinates served as the primary criterion: Allocentric iso-directional movements were denoted as in-phase and non-isodirectional movements as anti-phase modes (Figure 7). Procedure Each subject was instructed to draw circles in a continuous fashion while maintaining the prescribed relative phasing pattern, and the latter requirement was stressed more vigorously than in Experiment 1. Subjects always started with the stylus positioned at the center of the circle. Following the start signal, they moved to the contour of the circle, trying to produce the required pattern of interlimb coordination. In addition, subjects were also encouraged to maintain the required phasing pattern even if they experienced a phase transition. Instructions with respect to the correct phasing pattern were more explicit than in the previous experiment. Subjects were left free to visually monitor any of the limb movements. No visual feedback strategy was imposed in order to assess the spontaneous coordination tendencies. Two trials of each of the four coupling patterns were produced within each of the six limb combinations, resulting in a total of forty-eight trials. Prior to registration of the test trials, two warm-up trials were performed to familiarize subjects with the required coupling pattern. At the start of each new task, the required coupling pattern was explained to the subject by means of illustrations, and the experimenter verified whether the pattern was correctly understood. The order in which the 360 Journal of Cognitive Neuroscience Volume 9, Number 3

14 tasks were to be performed was randomized across subjects. Data Analysis The data analysis focused again on the spatiotemporal features of the individual limb motions by means of cycle duration and amplitude (diameter) measures and on a quantification of the coordination within and between limbs through relative phase analyses. Results Cycle Duration Mean CycZe Duration. A 2 x 2 x 3 (Limb Type x Body Side X Effector Combination) repeated measures ANOVA was conducted on the mean cycle duration scores as well as on the variability of cycle duration. Limb vpe consisted of two levels (i.e., the arm versus the leg). Body side referred to the limb motions on the right and left side. The three levels of effector combination represented the homologous, homolateral (ipsilateral), and heterolateral (diagonal) limb pairs. The analysis of mean cycle duration did not reveal any significant main effects: limb type, F( 1,ll) < 1, body side, F(1,ll) < 1, effector combination,f(2,22) = 2.7,p >.05 (MSe = ). Average cycle duration was 1007 msec in the arm and I006 msec in the leg. The difference in cycle duration between the circles drawn with the left as compared to the right limb was also very small: M1,ft = lo06 msec,mright = 1007 msec). Mean cycle durations for the homologous, homolateral, and contralateral limbs were 995, 1018, and 1007 msec, respectively. None of the interaction effects reached significance (p >.05), except for the Body Side x Limb Combination interaction, F(2, 22) = 5.32,p <.05 (MSe = 863). While differences in mean cycle duration between the left and right limbs were smallest for the heterolateral combination (Mlefi = 1008 msec, Mfight = 1006 msec), they were somewhat larger for the homologous combination (Mleft = 999 msec, Mright = 991 msec) and largest for the homolateral combination (Mleft = 1009 msec, Mfight = 1026 msec). Variability of Cycle Duration. The main effect for limb type was not significant,f(l, 11) = 1.37,p >.05 (MSe = ). Variability of cycle duration was 46.9 msec for the arm and 48.7 msec for the leg. Differences in SD s between the circles drawn with the left as compared to the right limb were also very small and did not reach significance, F(1, 1 1) < 1 (Mlefi = 48 msec, Mfight = 47.5 msec). The main effect for effector combination was significant, F(2, 22) = 21.1,p <.01 (MSe = 319.9). Variability scores were smallest for the homologous combination (M = 40.2 msec) and largest for the homolateral combination (M = 56.8 msec), whereas the heterolateral combination was positioned in between the aforemen- tioned conditions (M = 46.2 msec). A posteriori tests revealed that all the SD scores differed significantly from each other (p <.Ol). None of the interaction effects were significant (p >.05). Diameter A 2 x 2 x 2 x 3 (Limb vpe x Body Side x Movement Axis x Effector Combination) repeated measures ANOVA was applied to the mean diameters weak-to-peak amplitudes) of the circle as well as their SD s. The variable movement axis was added to the analysis because it was of interest to determine whether the X- and Y-axis diameters differed from each other. Mean Circle Diameter The statistical analysis revealed that the mean diameter of the circles drawn with the arm were significantly smaller than those drawn with the leg (M = 8.68 and 9.69 cm, respectively), F(1,ll) = 39.3, p <.01 (MSe = 1.84). No signrficant differences were observed between the left (M = 9.32 cm) and right circles (M = 9.04 cm), F(1, 11) = 2.86,~ >.05 (MSe = 2.01). The main effect of movement axis was significant, F(1, 11) = 5.27,p <.05 (MSe =.95). The diameter was smaller along the X-axis (M = 9.05 cm) than along the Y-axis (M = 9.31 cm). Significant differences were also observed among the three limb combinations, F(2,22) = 6.56,~ <.01 (MSe = 1.49). Means for the homologous, homolateral, and heterolateral effector combinations were 8.84,9.48, and 9.21 cm, respectively. Three interaction effects were significant. The Limb Type x Movement Axis interaction indicated that the arms produced larger diameters along the X-axis than along the Y-axis (M = 8.9 and 8.46 cm), whereas the converse effect was observed for the legs (M = 9.20 and cm), F(1, 11) = 20.75,p <.01 (MSe = 1.71). The Limb Type x Effector Combination interaction was also significant, F(2,22) = 7,p <.01 (MSe = 1.55). Across all effector combinations, the mean diameters were smaller for the arms than for the legs. However, while only small differences were observed in the homologous condition (M- = 8.71, Mleg = 8.98), they were larger in the heterolateral (M- = 8.63,Mleg = 9.8) and largest in the homolateral condition (M- = 8.69,Mleg = 10.27).Finally, the Limb vpe x Hector Combination x Movement Axis interaction was significant,f(2,22) = 10.72,p <.01(MSe =.37). In addition to the previously described interaction between Limb Type x Movement Axis, the differences in diameter were smallest for the homologous combination and largest for the homolateral combination, whereas the heterolateml condition was positioned in between the two aforementioned conditions. In order, mean diameters for the X-axis and Y-axis were 8.76 and 8.67 cm for the arm and 8.81 and 9.2 cm for the leg within the homologous condition, 9.07 and 8.32 cm for the arm and 9.58 and cm for the leg within the homolateral condition, and 8.88 and 8.38 cm for the arm Swlnnen et a1 361

15 and 9.27 and cm for the leg within the diagonal condition. The remaining interactions failed to reach the conventional levels of significance (p >.05). Variability of Circle Diameter The statistical analysis revealed that the SD's of the diameter of the circles drawn with the arm were significantly smaller than those drawn with the leg (M- =.77, Mleg = 1.14 cm), F( 1,ll) = 91.51,p c.01 (MSe = 0.11). The SD's were larger on the left side (M = 1.01 cm) than on the right side of the body (M =.9 cm), F(1,ll) = 16.17, p c.01 (MSe =.05). The main effect of movement axis was significant, F(1, 11) = 19.36,p c.01 (MSe =.04). The diameters were more variable along the X-axis (M = 1 cm) than along the Y-axis (M =.9 cm). Significant differences were also observed among the three limb combinations, F(2,22) = 47.05,p c.01 (MSe =.04). SD's for the homologous, homolateral, and heterolateral effector combinations were.8, 1.1, and.95 cm, respectively. The Limb Type x Effector Combination interaction was significant, F(2,22) = 3.86,p c.05 (MSe =.03). While SD's were generally smaller for the arm than for the leg, the between-limb differences were smaller during the homologous (Mam =.64 cm, Mteg =.96 cm) and heterolateral combination (M- =.79 cm, Mleg = 1.12 cm) than during the homolateral combination (M- =.87 cm, Mleg = 1.32 cm). In addition, the Limb Type x Effector Combination x Movement Axis interaction was significant, F(2, 22) = 8.09,p c.01 (MSe =.01). Across all effector Combinations, SD's for the arm were larger with respect to the X-axis than the Y-axis without exception. Mean SD's for the X- and Y-axis component were.72 and.57 for the homologous combination,.94 and.81 for the homolateral combination, and.87 and.71 for the heterolateral Combination, respectively. This was also the case for the SD's observed for the legs with respect to the homologous condition, whereas the differences between the X- and Y-axis SD scores were very similar for the homolateral and heterolateral limb combinations. Mean leg SD's for the X- and Y-axis diameters were 1.05 and.88 cm for the homologous combination, 1.35 and 1.3 cm for the homolateral combination, and 1.11 and 1.14 cm for the heterolateral combination, respectively. The remaining interactions failed to reach the conventional levels of significance (p >.05). Within Limb Relative Phase Analyses The Quality of Circle Drawing across the Three Effector Combinations. A 2 x 2 x 3 (Limb Type x Body Side x Effector Combination) repeated measures ANOVA was conducted on the relative phase error and variability scores separately. Relative phase was computed between the X- and Y-axis component within each limb. ASSOLUTE ERROR. With respect to relative phase error, the absolute deviation from a 90' phase offset between the X- and Y-axis component within a limb was computed. The larger the deviation from 90", the more disrupted the uniformity of the circle. The analysis of relative phase error revealed that the absolute deviation from the required relative phase of 90" was significantly smaller for circles drawn with the arm (M = 7.51') than with the leg (M = 13.28"),F(l, 11) = 65.28,p c.01 (MSe = 73.48). Relative phase error was also smaller for the right than for the left limbs, M = 9.48 and 11.3', respectively,f(l, 11) = 26.11,~ c.01 (MSe = 18.43).Signilicant differences were also observed among the three effector combinations, F(2, 22) = 7.83,p c.01 (MSe = 17.96). Circle drawing was performed most accurately in the homologous condition (M = 9.72") and least accurately in the homolateral condition (M = 11.35'), whereas the heterolateral condition was positioned in between the aforementioned conditions (M = 10.1 '). A posteriori tests revealed that the homologous and heterolateral conditions did not differ significantly from each other (p >.05). However, both effector combinations differed significantly from the homolateral combination (p c.01 and p c.05). None of the interactions reached significance (p >.05). STANDARDEVIATION. The analysis of SD's revealed that the variability of circle drawing was generally smaller for the arm (M = 7.02") than for the leg (M = 11.77"), F(1, 11) = ,p c.01 (MSe = 17.74).Variability scores for circles drawn with the right limbs were also smaller than those drawn with the left limbs, M's = 8.73 and lo.ob", respectively, F(1, 11) = 48.77, p c.01 (MSe = 5.29). Sigtllficant differences in SD were also observed among the three effector combinations,f(2,22) = 25.79,p c.01 (MSe = 8.6). Circle drawing was performed most consis tently in the homologous condition (M = 8.45') and least consistently in the homolateral condition (M = 10.56'), whereas the heterolateral condition was positioned in between the aforementioned conditions (M = 9.17"). A posteriori tests revealed that all three limb combinations differed from each other (p c.01). Two interaction effects were significant but since they are only of marginal interest, they will not be discussed any further. The Quality of Circle Drawing within Each Effector Combination. In addition to the overall ANOVA including all three limb combinations, the relative phase data were subsequently analyzed within each limb combination by means of a 2 x 4 (Coordination'Ifrpe x Coupling Task) repeated measures ANOVA. Coordination type consisted of two levels and referred to the coordination of both arms versus both legs within the homologous condition, to the left &eft leg versus right Wright leg coordination pattern within the homolateral condition, and to the left Wright leg and rat &eft leg pattern within the heterolateral condition. The coupling task consisted of four levels: X,,JYh, XmtJyin, Xin/Ymti, and Xmtdymti. 362 Journal of Cognitive Neuroscience Volume 9, Number 3

16 HOMOLOGOUS EFFECTOR COMBINATION. The absolute error scores as well as the SD scores were significantly lower for the homologous arm than for the leg combination,f(l, 11) = 83.49,p <.01 (MSe = 4.71),andF(1,11) = 208.3,p <.01 (MSe = 5.4), respectively. Mean absolute error and SD scores were 6.63 and 6.03" for the homologous arm and and 10.87' for the homologous leg pattern. The main effect for coupling task was significant for both absolute error and variability scores, F(3,33) = 9.25,p <.01 (MSe = 4.71), and F(3,33) = 3.57,p <.05 (MSe = 2.5). Mean error and SD scores for the Xh/Yi,, Xanti/Yh, XuJYanti, and XanJYanti patterns were 9.02 and 7.93",9.32 and 8.3",9.42 and 8.83",and and 8.63", respectively. The interaction effect was significant for absolute error but not for SD, F(3, 33) = 3.49,p <.05 (MSe = 6.2 l), F(3,33) = 2.69,p >.05 <MSe = 4.33). This effect indicated that the differences observed between the arm and leg patterns were larger in some of the four coupling patterns than in the others: It was largest for the Xanti/Yanti pattern. HOMOLATERAL EFFECTOR COMBINATION. The circles drawn with both right homolateral limbs (M = 10.65) were produced more accurately than those drawn with the left homolateral limbs (M = 12.06). This effect was significant,f(l, 11) = 23.10,p <.01 (MSe = 14.36). For SD, the effect just failed to reach significance (&fright = 10.33, Mlefi = 10.8),F(l, 11) < 3.73,p =.07 (MSe = 40.15).The main effect for coupling task was significant for both absolute error and variability scores, F(3,33) = 9.25,p <.01 (MSe = 4.71), and F(3, 33) = 24.5,p <.01 (MSe = 7.43). Mean error and SD scores for the XJY-,, Xanti/Yh, Xh/Ymti, and Xanti/Yanti patterns were 9.54 and 8.6", and 11.98", and 12.47", and 10.9 and 9.2", respectively. The interaction effect was not significant (p >.05J HETEROLATERAL EFFECTOR COMBINATION. NO significant differences were observed in the accuracy and consis tency of circle drawing between the right ameft foot and left arm/right foot combination (M = 8.74 and 10.2", MsD = 9.08 and 9.26"), F(1, 11) c 1 for both. The main effect for coupling task was significant for both absolute error and variability scores, F(3,33) = 3.38,p <.05 (MSe = 4.68), and F(3,33) = 3.57,p <.05 (MSe = 13.5). Mean error and SD scores for the XJYin,Xanti/Yh,Xh/Yanti, and Xanti/Yanti patterns were 8.88 and 8.75", and 9.63", and 9.71, and 9.74 and 8.6", respectively. The interaction effect was not significant (p >.05). Between Limb Relative Phase Analyses Graphical Representation of XtJyin and LntJYanti Patterns for the Three Effector Combinations. Typical coordination patterns of a representative subject are shown for the most and least stable experimental conditions (Figures 8a-8c). Performance of the XJYin coupling pattern, requiring the simultaneous activation of the ho- mologous leg muscle groups, is shown in the upper graph (Figure 8a-1 and 8a-2). The pattern of interlimb coordination is performed with a high degree of stability without any noticeable phase deviation or transition, and this was the case for all subjects. In addition, the amplitudes for both limbs are very similar and are produced with a high degree of consistency across cycles. This is not the case during the production of the Xanti/Yanti coupling pattern where the amplitudes display more variation across cycles. Even though the anti-phase pattern is successfuuy maintained in the present trial, the relative phase stability is lower than during the XilJYin pattern. The left homolateral pattern is displayed in Figures 8b-1 and 8b-2. Similar to the homologous limb combination, the Xh/Yh coupling pattern is produced with a high degree of stability as can be observed from the displacement-time profiles. This is not the case during the Xanti/Ymti coupling pattern where the required antiphase mode can only be maintained for a short time. Following the phase transition, the resulting coupling mode is close to in-phase whereby the leg pattern is a little bit offset with respect to the arm pattern. Phase transitions did not always occur early in the trial across all subjects. Examples of the heterolateral left leg/right arm combination are shown in Figures 8c-1 and 8c-2. The observations with respect to the Xi,,/&, coupling pattern are similar to those of the homolateral pattern. In-phase coordination is well preserved across the trial, and the right arm leads the left leg on the majority of the cycles, except the first ones. The form of the circle is less successful when drawn with the leg as compared to the arm. During the Xanti/Ymti coupling pattern, the required anti-phase mode is only maintained during the first three cycles, after which a transition is observed to the inphase mode (Figure 8c-2). In order to obtain insights into the differential stability of coordination patterns at the global level, the number of phase transitions that occurred across the four coupling patterns and within each limb combination were counted (Table 1). It is clear from a general inspection of the table that phase transitions were observed most frequently during homolateral coordination and least frequently during homologous coordination, with the heterolateral limb combination taking an intermediate position. No phase transitions were observed during the XJKn pattern across the three limb combinations. A low percentage of transitions was observed during the homologous and heterolateral XmJYh pattern, whereas 60 to 80% of the homolateral trials exhibited transitions. During the XJYanti pattern, transitions occurred on 20 to 30% of the homologous trials, whereas all homolateral and heterolateral trials exhibited transitions. A similar pattern was found for the XanJYanti condition, where the number of transitions in the homologous combination was a bit higher than in the previous condition. Swinnen et al 363

17 Figure 8a-1. Example of circle drawings pertaining to the Xi,/Yi, coupling condition as produced with the homob gous effector combination. Left Leg Figure 8 A1. X in - Y in Right Leg Displacement X-axis Displacement X-axis h v B 8-6 g 4-0 ; P a -2 4 X-axis 10 h 8 v E 2-0 ; ap 4-6 Y-axis THE ACCURACY AND CONSISTENCY OF RELATIVE PHASING MEASURES ACROSS THETHREE EFFECTOR COMBINATIONS. The statistical analysis was focused on the absolute deviations from the required relative phasing pattern (0 or 180') as well as on the SD's of relative phase. ABSOLUTERROR. A 2 x 2 x 3 (Relative Phase Pattern x Movement Axis x Effector Combination) repeated measures ANOVA was conducted on the absolute error scores. The two levels of relative phase pattern represented the in-phase and anti-phase mode. Movement axis pertained to the X- and Y-axis component and the three levels of effector combination were homologous, homolateral, and heterolateral. The in-phase pattern (M = 37.15') was performed signrficantly more accurately than the anti-phase pattern (M = 98.6'), F(1, 11) = ,p c.01 (MSe = ). The main effect of movement axis was also significant even though only small differences were observed between the X- (M = 68.77') and Y-axis component (M = 66.98'),F(l, 11) = 6.12,p c.05 (MSe = 18.8). Signrficant differences were also observed among the three effector combinations, F(2,22) = ,p c.01 (MSe = ). Errors for the homologous, homolateral, and heterolatera1 effector combination were 34.78,84.16, and 84.69', respectively (Figure 9, left side). The interaction between phase pattern and movement axis was highly significant and invites a reinterpretation of the main effect for movement axis, F(1,ll) = ,p c.01 (MSe = 53.53) (Figure 10, left side). While the in-phase pattern was performed more accurately along the y-axis than along the X-axis, the anti-phase pattern was performed more accurately along the X-axis than along the Y-axis.The Movement Axis x Effector Combination interaction was not significant, F(2, 22) = 1.34,p >.05 (MSe = 31.02). Finally, the Movement Axis x Phase Pattern X Effector Combination interaction was significant, F(2,22) = 45.67, p c.01 (MSe = ). This interaction is graphically decomposed into a two-factor interaction between movement axis and phase pattern at each level of effector combination (Figure 11). As can be observed, the in-phase patterns are produced more accurately along 364 Journal of Cognitive Neuroscience Volume 9, Number 3

18 Figure 8a-2. Example of circle drawings pertaining to the Xm,i/Ymti coupling condition as produced with hornole gous effector combination. Left Leg Figure 8 A2. X anti - Y anti Right Leg? e4 g, Displacement X-axis Displacement X-axis x-axis h 10 E z 8 ~6 Y-axis the Y-axis than along the X-axis across all effector combinations. Conversely, the anti-phase patterns are produced more accurately along the X- than along the Y-axis component. The three limb combinations mainly deviated from each other with respect to the shape of the interaction effect. Additional analyses revealed that the Movement Axis x Phase Pattern interaction was significant within each effector combination, but the effect was most pronounced with respect to the heterolateral pattern (allp's <.01). VARIABILITY OF RELATIVE PHASE. The in-phase pattern (M = 14.25') was performed with lower variability than the anti-phase pattern (M = 20.go),F(1, 11) = 75.35,p <.05 (MSe = 21.21). SD scores were lower with respect to the Y-axis (M = 16.96") than with respect to the X-axis component (M = 18.17"),F(1, 11) = 40.2,p <.01 (MSe = 1.29). Significant differences in SD were also observed among the three effector combinations, F(2,22) = 4.09, p <.05 (MSe = 82.71) (Figure 9, right side). SD scores were 14.5, 19, and 19.2" for the homologous, homolateral, and heterolateral effector combination, respectively. A posteriori tests revealed marginally swcant differences between the homologous and homolateral (p =.06) and significant differences between the homologous and heterolateral condition (p <.Ol) but not between the homolateral and heterolateral condition (p >.05). The interaction between phase pattern and movement axis was significantj(1,ll) = 29.59,p <.01(MSe = 24.18) (FW 10, right side). While the in-phase pattern was performed with lower variability along the Y-axis than along the X-axis, the anti-phase pattern was performed with higher variability along the Y-axis than along the X-axis. The Movement Axis x Effector Combination interaction was also significant, F(2,22) = 5.37,~ <.05 (MSe = 3.2). While SD scores for the X- and Y-axis component were very similar to each other in the heterolateral condition (Mx = 19.15", My = 19.2'), they showed larger differences within the homologous (Mx = 15.1", My = 13.9") and homolated condition (Mx = 20.2", MY = 17.85"). The Phase Pattern x Effector Combination interaction was not s@cant,f(2,22) = 1.53,p >.05(MSe = 21.48) nor was the Movement Axis x Phase Pattern x Effector Combination interaction, F(2,22) < 1. Swinnen et al. 365

19 Figure 8b-1. Example of circle drawings pertaining to the Xh/Yh coupling condition as produced with the homolatera1 effector combination. Right Leg Figure 8 B1. X in - Y in Right Arm Displacement X-axis Displacement X-axis x-axis Y-axis The Accuracy and Consistency of Relative Phasing Measures for Each of the Effector Combinations. In addition to the previous overall ANOVA, the absolute error and SD data were subsequently analyzed within each limb combination by means of a 2 x 4 (Coordination Qpe x Coupling Task) repeated measures ANOVA. Coordination type consisted of two levels and referred to the coordination pattern of the arms and the legs within the homologous condition, to the left versus right limb coordination pattern within the homolateral condition, and to the left arm/right leg and right arm/left leg pattern within the heterolateral condition. Coupling task consisted of four levels: XJYh, XantJYin, XJYanti, XantJYanti. HOMOLOGOUS EFFECTOR COMBINATION. No significant differences in accuracy and variability were observed between the bilateral arm (M = 39.55", MSD = 15.51") and bilateral leg patterns (M = 30.02", MSD = 13.5"), F(1, 11) = 3.37,~ >.05 (MSe = ) and F(1, 11) = 2.61,p > 366 Journal of Cognitive Neuroscience.05 (MSe = 74.36), respectively. A significant main effect for coupling task was observed with respect to absolute error F(3, 33) = 14.72,p <.01 (MSe = ) and variability, F(3, 33) = 31.89,p c.01 (MSe = 74.48). The Xdyin pattern was performed most successfully (M = 12.49", MSD = 6.75"), followed by the XmtJY-, (M = 23.88", MSD = 10.42"), XJYanti (M = 46.16", MSD = 19.59"),andXmtJYmti pattern (M = 56.6lo,Ms~ = 21.26"). The Coordination Qpe x Coupling Task interaction was not significant, F(3,33) c 1, for both absolute error and SD. HOMOLATERAL EFFECTOR COMBINATION. No significant differences in accuracy were observed between the coordination pattern performed on the left (M = 39.55") and the right side (M = 30.02") of the body, F(1, 11) c 1. However, the left homolateral coordination pattern was performed with lower variability than the right pattern, mean SD = and 22.36", respectively, F(1, 11) = 16.97,p >.01 (MSe = ). A significant main effect Volume 3, Number 3

20 Figure 8b-2. Example of circle drawings pertaining to the X,,i/Ymti coupling condition as produced with the homolatera1 effector combination. Right Leg Figure X anti - Y anti Right Arm Displacement X-axis Displacement X-axis 10 h e 4 32 i!; x-axis q a o i i 3 i 5 6 i i 4 I b i i l i i 3 i 4 1 ' 5 Y-axis for coupling task was observed with respect to absolute error F(3, 33) = 193.6,p <.01 (MSe = ) and variability, F(3, 33) = 16.94, p <.01 (MSe = ). Absolute error and SD scores for the X,,,/Yh, Xanti/Yh, Xh/Yanti, and XmtJYmti pattern were and 9.34", and 22.26",95.67 and 28.94",and and 15.5". The Coordination wpe x Coupling Task interaction was not significant for absolute error F(3, 33) = 1.4,p >.05 (MSe = ), but it was significant for SD, F(3, 33) = 6.62,~ <.01(MSe = 92.93).Across all coordination types, the SD scores were lower for the left side than for the right side, but this effect was more pronounced for the Xh/Yanti condition than for the other conditions. In order, mean SD scores for the X,,,/Ym, XanJYh, XJYanti, and Xanti/Yanti were 8.49, 19.83, 20.3 and 14" for the left he molateral coordination pattern and 10.19, 24.69, 37.57, and 17" for the right homolateral coordination pattern. HETEROLATERAL EFFECTOR COMBINATION. The right arm/ left leg pattern was generally performed more accurately than the left arm/right leg pattern,m = and 89.42", F(1, 11) = 5.87,p <.05 (MSe = 731.5). No significant differences in variability were observed between both coordination patterns, F(1, 11) = 1.22, p >.05 (MSe = ). Mean SD scores were 20" for the right &eft leg pattern and 18.38" for the left amright leg pattern. A significant main effect for coupling task was observed with respect to absolute error F(3,33) = ,p <.01 (MSe = ) and variability, F(3, 33) = 15.1,p <.01 (MSe = ). Mean absolute error and SD scores for the XilJYh, Xmti/Yh, X,,,/Yanti, and XmtJYmti pattern were and 11.65", and 15.73", and 23.18", and and 26.2O.The Coordination'I)pex Coupling Task interaction was not significant for both absolute error and SD, F(3, 33) < 1 and F(3, 33) = 2.34,p >.05 (MSe = 97.78). Signed Relative Phasing Measures. To investigate the potential existence of a phase lag between the limbs, the signed relative phasing scores were analyzed with respect to the X,,,/Yh conditions. This was the only condition free of any phase transitions. In the case of bilateral Swinnen et al. 367

21 Figure 8c-1. Example of circle drawings pertaining to the Xi,/Yh coupling condition as produced with the heterolatera1 effector combination. Left Leg Figure 8 C1. X in - Y in.- u1 gt------? Right Arm h v - q 10-8 : 5 4 p Displacement X-axis x-axis Displacement X-axis Y-axis coordination patterns (homologous, heterolateral), the phase difference between the right and left limb was computed whereby the former served as the reference limb. In the homolateral coordination patterns, the arm was used as the reference signal to compute phase lags between the upper and lower limb. The relative phase was calculated with respect to the reference interval [-n, +n]. This implies that a positive score suggested a phase lag of the left limb with respect to the right limb in the bilateral patterns and a phase lag of the leg with respect to the arm in the homolateral conditions. A 3 x 2 (Effector Combination x Movement Axis) repeated measures ANOVA revealed that the signed relative phase measures differed signrficantly among the three conditions, F(2, 22) = 5.69, p <.05 (MSe = ). The phase values were positive in both the homologous (M = 8.79) and heterolateral (M = 20.36) conditions and slightly negative in the homolateral condition (M = -2.27). Stated differently, the right limb led the left limb in the bilateral coordination patterns, whereas there was only a small phase offset for the total group of subjects in the homolateral coordination pattern. A posteriori tests revealed a significant difference between the homologous and homolateral (p c.05) and between the heterolateral and homolateral combination (p c.05) but not between the homologous and heterolateral coordination pattern (p >.05). Phase lagging was also found to be significantly smaller along the Y-axis (M = 7.30") than along the X-axis (M = 10.62O), F(1, 11) = 7.50, p <.05 (MSe = 53.11). The interaction between effector combination and movement axis was not significant, F(2,22) = 1.42,~ >.05 (MSe = 34.65). Subsequent analyses were performed within each effector combination to elucidate differences between each couple of coordination patterns. Within the homologous combination, phase offsets were larger between both upper limbs than between both lower ones, but this effect failed to reach significance,f(l, 11) = 3.69, p >.05 (MSe = 81.16). Means for the upper and lower limb phase offsets were and 6.29", respectively. The differences between the right (M = -3.92") and left homolateral pattern (M = -.61 ) also failed to reach 368 Journal of Cognitive Neuroscience Volume 9, Number 3

22 Pipre 8c-2. Example of circle drawings pertaining to the X,,i/Ymti coupling condition as produced with the hetere lateral effector combination. Left Leg Figure 8 C2. X anti - Y anti Right Arm Displacement X-axis Displacement X-axis x-axis h E 6 * Y-axis 8 B o P -2.- % 4 n significance, F(1, 11) < 1. Sigmficant differences were observed between the right armlleft leg (M = 7.22') and left armlright leg pattern (M = 33.51'), F(1, 11) = 5.57, p <.05 (MSe = ). Discussion The Accuracy and Consistency of Circle Drawing among Effector Combinations The quality of circle drawing differed among the limb combinations. With respect to the variability in timing and amplitude as well as the accuracy and consistency of intralimb coordination, circle drawing was most successful during homologous coordination and least successful during homolateral coordination, whereas the heterolateral effector combination was positioned in between the aforementioned conditions. The quality of circle drawing was also a function of the effectors used. Across all effector combinations, circles drawn with the dominant (right) limbs were pro- duced more accurately and consistently than circles drawn with the nondominant (left) limbs. These findings support previous evidence on the existence of functional asymmetries in the upper as well as in the lower limbs (Peters, 1988). Intralimb coordination, timing, and circle diameter measures were also more accurate in the arm than in the leg. This is not surprising in view of the privileged position that the arm and hand have occupied through evolution for fine manipulation and precision. Conversely, the legs are major instruments for support of the body and for locomotion. An additional observation worth mentioning is that right/left differences were more pronounced in the lower than in the upper limbs within the homologous condition. The Accuracy and Consistency of Interlimb Coordination among Effector Combinations The analyses of relative phase revealed differences among the effector combinations that were consistent with the differences observed with respect to the quality Swinnen et al. 369

23 Table 1. Phase Transition Counts for the Homologous, Homolateral, and Heterolateral Pattern Across the Four Coupling Modes. Homologous (%) Homolateral (%) Heterolateral (%h) Arms Legs Left Right Lefl LedRight Arm Right LedLefl Arm Xin/Yin Xantd Yin Xin/ Yant i XantiWanti Figure 9. Relative phase error (a) and SD of relative phase (b) with respect to the coordination of the homob gous, homolateral, and hetere lateral effectors. Mops Hcmidateral Hetemlareral Effector Combination (b) Figure 10. The interaction between phase pattern and movement axis with respect to relative phase error (a) and the standard deviation of relative phase (b). - 0 In-phase Anti-phase Phase Pattern (a) a" 15-." P $ 5- v Y-axis In-phase Anti-phase Phase Pattern (b) of circle drawing: Coupling between the homologous limbs was found to be more accurate and consistent than between the nonhomologous limbs, extending previous findings on unidimensional parasagittal joint actions (Kelso & Jeka, 1992; Serrien & Swinnen, in press a,b; Swinnen, Dounskaia et al., 1995). While the analyses of intralimb coordination distinguished between the homolateral and heterolateral effector combinations, the analysis of interlimb coordination did not. In previous work, two potential explanations for the observed differences among homologous and nonhomologous effector combinations have been provided: a neural and biophysical account (Swinnen, Serrien, Walter, & Philippaerts, 1995; Swinnen, Dounskaia et al., 1995). The biophysical account points to differences in eigenfrequencies between the upper and lower limb segments which give rise to larger variations in the coupling of these segments (see also Kelso & Jeka, 1992). The neural account mainly seeks explanations in terms of differential pathway strength. The supremacy of intragirdle (homologous) over intergrdle (nonhomologous) coupling has been documented in a variety of vertebrates (Cruse & Warnecke, 1992; Halbertsma, 1983; Wetzel & Stuart, 1977). Across all three effector combinations, in-phase movements were produced more accurately and consistently 3 70 Journal of Cognitive Neuroscience Volume 9, Number 3

24 Homologous 160, I Heterolateral Homolateral r In-phase Anti-phase PhasePattern In-phase Anti-phase Phase Pattern E ,. P d In-phase Anti-phase PhasePattern Figure 11. The interaction between phase pattern and movement axis with respect to relative phase error during the homologous, homolateral, and heterolateral effector combination. than anti-phase movements. This effect was evident with respect to both the X- and Y-axis dimension. Analysis of the four distinct coupling patterns revealed that patterns, characterized by in-phase coordination with respect to both the X- and Y-axis dimension, were found most accurate and consistent across the three effector combinations. Patterns characterized by anti-phase coordination with respect to one or both movement dimensions were produced less accurately. The Xanti/Ymti pattern was performed least accurately during homologous and homolateral coordination, whereas it shared the high error rates with the X,/Ymti pattern during heterolateral coordination. These findings underscore the importance of the egocentric and allocentric constraint. Interlimb Phase Lags The asynchrony observed in the previous experiment was also supported in the present experiment. In the homologous coordination patterns, the left arm lagged with respect to the right arm and the left leg lagged with respect to the right leg. In the heterolateral right armfleft leg pattern, the left leg lagged with respect to the right arm. In the left arm/right leg pattern, it was the left arm that lagged with respect to the right leg. Thus, the right limb led the left limb in both bilateral conditions, whereas no big phase offsets between limbs were observed for the total group of subjects in the homolateral coordination pattern. This does not imply that phase offsets between the homolateral limbs were absent in individual subjects. Rather, it appears that this phase offset was inconsistent in sign across individuals. In the homologous and heterolateral patterns, the majority of subjects showed a positive phase offset. It is hypothesized that the distinct asynchrony between the r at and left limb is a manifestation of the superior control of the dominant (right limb) as com- pared to the nondominant limb in right-handed subjects. It may be an expression of the preeminence of the left hemisphere with respect to the organization of complex coordination patterns with spatiotemporal requirements (Swinnen, Serrien et al., 1995). Even though decisive evidence is not available at this point, the possibility remains that the observed phase offset between the right and left limb is due to the transmission of timekeeping information at cortical or subcortical levels. What we do know from another study is that the asynchrony did not result from differential visual monitoring of the limbs because it was also observed during bimanual circle drawing under blindfolded conditions. Nevertheless, the phase offset increased when the subject visually monitored the dominant limb and decreased when monitoring the nondominant limb (Swinnen, Jardin, & Meulenbroek, 1996). GENERAL DISCUSSION The present experiments demonstrate that the human performer is faced with limitations when organizing coordination patterns. This is inferred from the observation that some coordination patterns can be produced successfully without practice, whereas others appear much more difficult. Moreover, during attempts to perform the more difficult patterns, there is a tendency to regress to the easier coordination modes. These differential difficulty levels are informative about the architecture of the CNS with respect to the organization and control of coordination patterns. In the present context, difficulty is hypothesized to refer to the degree of divergence from the egocentric and/or docentric constraints. It is justified to use the concept of constraints in view of the fact that not only differences in accuracy and consistency among coordination patterns are observed but also particular transition routes that ultimately result in Swlnnen et al. 371

25 patterns of coordination that conform to these constraints (for extensive work on transitions, see Kelso et al., 1986, Scholz & Kelso, 1989, etc.). The findings of both experiments provide converging evidence for the existence of two major coordination constraints. The egocentric or mirror-image symmetry constraint is dominant during the coordination of the homologous limbs. The allocentric constraint emerges during the coordination of nonhomologous limbs. Both constraints can be meaningfully distinguished. Evidence suggesting that they are neurally endowed is discussed next. Coordination Constraints During the Coordination of Homologous Limbs In spite of considerable evidence for the capability of the hands to assume different roles during the production of everyday goaldirected movements, the tendency to move both hands and/or arms in a symmetrical fashion has been documented extensively in the literature and dates back a long time (Meige, 1901; Westphal, 1873, Woodworth, 1899). Recent studies on the production of discrete as well as cyclical bimanual movements have more specifically drawn attention to the existence of temporal and/or spatial constraints (Franz et al., 1991; Kelso, Southard, & Goodman, 1979; Marteniuk et al., 1984; Sherwood, 1994; Swinnen, Walter, & Shapiro, 1988; Swinnen, Young et al., 1991; Walter & Swinnen, 1992). The present study confirmed and extended recent findings on preferred coordination modes during bimanual drawing of circular and elliptical endpoint trajectories (Semjen, Summers, & Cattaert, 1995; Stucchi & Viviani, 1993). While the latter studies only manipulated coordination modes with respect to the X-axis component, the present studies looked at in-phase and antiphase modes with respect to both the X- and Y-axis component of circle drawing in the homologous upper and lower limbs. This combination resulted in four coordination modes that allowed a more complete assess ment of coordination constraints during bimanual coordination. Irrespective of movement dimension and limb type, the in-phase mode was produced with a higher degree of accuracy and consistency than the anti-phase mode, underscoring the importance of the egocentric constraint (i.e., symmetrical bimanual movements involving the simultaneous activation of homologous muscle groups were produced with a greater degree of accuracy and stability than asymmetrical movements involving nonhomologous muscle groups). Furthermore, during the production of anti-phase movements, subjects frequently exhibited transitions to in-phase modes of coordination. In addition to the observed differences between in-phase and anti-phase coordination, the interaction between interlimb relative phasing and movement dimension reached signrficance in both experiments. More specifically, in-phase coordination was produced with higher accuracy and consistency along the Y-axis than along the X-axis component. Conversely, anti-phase coordination was produced more successfully along the X- than along the Y-axis component. While the reason for this finding remains to be discovered, this interaction was hypothesized to reflect the (albeit more subtle) influence of the allocentric constraint during homologous limb coordination. Indeed, both aforementioned conditions required the control of limb movements in the same direction according to extrinsic space coordinates. In other words, the allocentric constraint was subordinate to the egocentric constraint, but the effect of the latter was possibly superposed on that of the former. Even though the putative brain mechanisms underlying the aforementioned coordination constraints remain to be uncovered, there is converging evidence that the in-phase or symmetrical bimanual coordination mode is not easily disrupted as a result of brain lesions. As Wiesendanger, Wicki, and Rouiller (1 994) noted, symmetrical limb movements are relatively well preserved in the presence of cortical lesions outside the primary motor cortex. This is also the case with split-brain patients and patients suffering from a congenital or acquired deficiency of the interhemispheric connections. In spite of the considerable difficulties they encounter during the production of bimanual tasks, they remain largely successful in performing symmetrical arm movements (preilowski, 1975; Tbller & Kelso, 1989). Because interhemispheric communication is apparently hampered in the latter patients, these observations have led neun, scientists to underscore the role of the bilaterally distributed motor pathways for production of bimanual movements that allow the proximal musculature of both limbs to be controlled by one hemisphere under certain circumstances. This ventromedial brain stem pathway has been anatomically demonstrated in primates and is distinguished from the dorsolateral pathway. While the former is primarily responsible for proximal control of limb movements, the latter enables the finely differentiated control of distal movements (Kuypers, 1973; Shinoda, Kakei, & Sugiuchi, 1994). The existence of these pathways and the associated ipsilateral control they afford has also been confirmed by clinical evidence in humans (Benecke, Meyer, & Freund, 1991; Colebatch, Deiber, Passingham, Friston, & Frackowiak, 1991; Colebatch & Gandevia, 1989; Gazzaniga, Bogen, & Sperry, 1967; Jones, Donaldson, & Parkin, 1989; Jung & Dietz, 1975; Miiller, Kunesch, Binkofski, & Freund, 1991; Wassermann, Pascual-Leone, & Hallett, 1994). The previous evidence provides strong hints that symmetrical limb movements constitute one of the most archaic modes of interlimb coordination, largely preserved under different pathological conditions. Their presence even emerges in exaggerated form as a result of brain dysfunction, developmental abnormalities, or 372 Journal of Cognitive Neuroscience Volume 9, Number 3

26 hereditary influences, often referred to as (congenital) mirror movements. Such movements are more apparent in the distal than in the proximal muscles of the upper limbs during voluntary activation of the homologous contralateral muscles. Mirror movements have been observed in patients with Klippel-Feil syndrome, Kallmann s syndrome, agenesis of the corpus callosum, and congenital hemiparesis (Cohen et al., 1991; Forget, Boghen, Attig, & Lamarre, 1986; Gunderson, & Solitare, 1968; Nass, 1985; Regli, Filippa, & Wiesendanger, 1967; Schott & Wyke, 1981; Westphal, 1873; Woods & Teuber, 1978; Ziilch & Muller, 1969). The preponderance of such movements has been associated with an impaired decussation of the pyramidal tracts and/or a deficit in the inhibitory control exerted by the contralateral hemisphere. A recent study using motor evoked potentials through transcranial magnetic stimulation has supported the notion that fast conducting pathways connect the motor cortex with both contralateral and ipsilateral spinal motoneurones in patients who suffer from mirror movements (Concotta et al., 1994). In contrast to the considerable degree of persistence of symmetrical movements in the presence of various CNS deficits, deficits in asymmetrical movements or tasks requiring interdependent bimanual movements are relatively large as a result of brain dysfunctions. This has for example been reported in patients with a commissurotomy (Preilowski, 1975,1990; Zaidel & Sperry, 1977). Together with the occurrence of mirror movements described above, these observations suggest two general principles of normal CNS functioning. First, control of asymmetrical movements requires a more elaborate involvement from higher CNS structures than the more archaic symmetrical limb mwements. Second, normal brain function may be associated with suppression or inhibition of the symmetrical or in-phase movements whenever alternative movement patterns are required. This recruitment of inhibitory networks is possibly mediated by the corpus callosum. In this respect, it is worth noting that symmetrical movements occur quite frequently during the first decade of child development, after which they disappear. Some authors have associated the disappearance of these mirror movements at the age of 10 with the progressive myelination of the corpus callosum (Asanuma & Okamoto, 1959; Asanuma & Okuda, 1962; Ferbert et al., 1992; Nass, 1985). Coordination Constraints During the Coordination of Nonhomologous Limbs Studying ipsilateral (homolateral) arm and foot coordination in the parasagittal plane, Baldissera et al. (1982) contended that the level of difficulty of an association did not depend upon preferential innervation of specific pairs of muscle groups. They argued instead that a relevant factor appears to be the mutual direction of the movements, quite independently of the muscles in- volved (p. 98). Associations were easy when the segments rotated simultaneously in the same direction but were more difficult when the segments moved in opposite directions. Subsequent studies have supported this contention with respect to forearm and lower leg homolateral and heterolateral coordination patterns in the parasagittal plane (Kelso & Jeka, 1992; Serrien & Swinnen, in press a,b; Swinnen, Dounskaia et al., 1995). The present experiments confirmed and extended support for the important role of the allocentric constraint during interlimb coordination. While previous research was limited to unidimensional coordination patterns in the parasagittal plane, we studied two-dimensional movements in the paratransverse plane. Across both the homolateral and heterolateral coordination pattern, the in-phase (allocentric iso-directional) coordination mode was found more stable than the anti-phase (allocentric non-isodirectional) mode. These observations were further supported when separately analyzing the four coupling patterns within each effector combination. Coupling was most accurate and consistent when in-phase coordination was required with respect to both the X- and Y-axis component. The patterns deteriorated signrficantly when anti-phase coordination was introduced with respect to one or both dimensions. This was evident from the absolute error scores, which were highest for the Xm,i/Ymti pattern in the homolateral condition, followed closely by the heterolateral condition. With respect to variability, the Xanti/Ymti pattern showed the highest SD scores of all four coupling tasks in the heterolateral condition, whereas this was not the case for the homolateral condition. This small variation across findings is understandable in view of the observation that subjects often showed phase transitions from a more difficult (and less consistent) to a less difficult (but more consistent) coupling pattern. As a result, the absolute error scores are more revealing than the SD scores to assess the differential difficulty of coupling patterns. The analysis of the quality of circle drawing through assessment of the relative phasing between the X- and Y-axis components within each limb generally confirmed the previous reports with respect to between-limb relative phasing. The coupling modes requiring in-phase coordination with respect to both movement dimensions also resulted in the most successful circle drawings. As soon as anti-phase coordination was required with respect to one or both dimensions, circle drawing deteriorated signrficantly. Previous studies have shown that the isdirectional movements are better preserved under pathological conditions than are the non-iso-directional movements. This was shown by Baldissera et al. (1994) for homolateral coordination in the intact limbs of hemiplegic patients and by Swinnen, Van Langendonk et al. (in press) during homolateral and heterolateral coordination in parkinsonian patients. If it is assumed that the peripheral ma- Swinnen et al. 373

27 chinery in those populations is not severely affected, the source of these coordinative disorders needs to be sought again at the central level of movement organization and/or processing of response-produced (afferent) information. Both hypotheses are discussed next. The nature of movement parameters that are coded in the CNS is particularly relevant to the central locus regarding the preparation of movement commands. Pioneering singlecell recording in awake monkeys, Evarts (1968) suggested that activity of the nerve cells in the motor cortex of the monkey showed firing patterns that were closely associated with the amount and pattern of muscular contraction rather than with the displacement that was produced by the contraction. The possibility of the tuning of the cortical cells to movement direction was also suggested. This relation has been investigated intensively in subsequent years by Georgopoulos and colleagues (Georgopoulos, 1991 ; Georgopoulos, Kettner, & Schwartz, 1988; Georgopoulos, Taira, & Lukashin, 1993). They found that the majority of cells have a directional preference even though they are only broadly tuned to movement direction. Movement in a specific direction is then represented as a popular vector, which comprises the weighted sum of the directions signalled by a population of cells in the motor cortex (the population coding hypothesis). The idea that individual neurons in a population are active during a variety of movements and that the coding for a particular movement is represented by the weighted average activity of the population has inspired recent attempts to model the control of movement in animals and humans. Schwartz (1994) used the population vector method to visualize the motor cortical representation of a monkey s hand trajectory while drawing a spiral. He observed that hand path was accurately reflected by a series of population vectors that were calculated throughout the task. Schwartz (1994) concluded from these findings that the movement trajectory is critically dependent on motor cortical activity. Evidence for discharge rates of cells associated with movement direction in preparation for and during movement has not only been found in the primary motor cortex but also in the premotor cortex, the parietal association cortex, the supplementary motor area, the primary somatosensory cortex, the cerebellum, the putamen, globus pallidus, and possibly other brain structures (Alexander & Crutcher, 1990; Caminiti, Johnson, Galli, Ferraina, & Burnod, 1991; Crutcher & Alexander, 1990; Fortier, Kalaska, & Smith, 1989; Kalaska, Caminiti, & Georgopoulos, 1983; Kalaska, Cohen, Prud homme, & Hyde, 1990; Mitchell, Richardson, Baker, & DeLong, 1987; Prud homme & Kalaska, 1994). In view of this widely distributed discharge of cells in association with the spatial attributes of movement, it appears plausible that the central nervous system s capability for simultaneously speclfying efferent commands for limb movements in different directions is limited. As a consequence, the emergence of directional coordinative constraints is perhaps not surprising. These constraints are not irrevocable, however. Interactions between the population vectors that are set up simultaneously within a highly linked neural medium can be overcome with practice. Furthermore, simultaneously specifying distinct population vectors may be more successful when the activity patterns are distributed across functionally distant regions within the CNS. In addition to the hypothesized difficulties associated with organizing and preparing effmnt commands for the control of allocentric non-isdirectional movements, the processing of response-produced afferences may also be much more complex in non-isdirectional than in isdirectional movements. Baldissera and coworkers (1 991,1994) have defended this hypothesis for the specific case of unidimensional homolateral wrist and foot movements in the parasagittal plane. They argue that in-phase movements are associated with a quasi automatic feedback system, whereas anti-phase movements are associated with a more attentiondemanding feedback system. Consequently, brain damage affecting the central mechanisms that process kinesthetic inflow will impair the non-iso-directional patterns more than the iso-directional ones. Additional research is required to unravel the efferent and/or afferent locus of the constraints inherent to the coordination of limb movements. Whatever the most viable account may be, the convergent experimental findings suggest that movement direction is a primary parameter coded in the CNS, giving rise to coordination constraints. There is great merit in identifying global coordination constraints as well as the preferred coordination modes to which they give rise. On the one hand, this work is of theoretical relevance for (motor) neuroscience in that it invites hypotheses about the design of the neural networks or CNS substrates that subserve the complex organization of patterns of interlimb coordination. On the other hand, uncovering preferred coordination tendencies is also of substantial practical relevance because these may form the basis of biases or errors in motor performance during the acquisition of new skills, often requiring substantial amounts of practice to be overruled (Walter & Swinnen, 1994). Moreover, preferred movement patterns may suddenly emerge under stressful conditions or when severe temporal constraints are imposed on the motor control system, a phenomenon that is practically relevant to error-prone performance within an ergonomic context. The aforementioned coordination constraints are not to be considered as insurmountable hardware limitations. The bewildering variety of coordination patterns that humans perform during every day activities and in recreational and industrial contexts proves otherwise. Rather, these constraints are presumed to give rise to systematic coordination tendencies or biases in motor 374 Journal of Cognitive Neuroscience Volume 9, Number 3

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