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
0 1997 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$= 0') and anti-phasemode
($ = 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. 348-377
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 s u p
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
modes between the limbs with respect to both the Xand Y-axis component of the two-dimensional movements.
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.
EXPERIMENT 1
Method
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
Subjects
350
Journal of Cognitive Neuroscience
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
Volume 9, Number 3
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
CONDITION
LEFTHAND
viii
0
RIGHT HAND
Q
PHASE
PATTERN
ALLOCENTRIC
DIRECTION
X: in-phase
Y: in-phase
different direction
same direction
X: in-phase
Y: in-phase
different direction
same direction
X: anti-phase
Y: in-phase
same direction
same direction
X: anti-phase
Y: in-phase
same direction
same direction
X: in-phase
Y: anti-phase
different direction
different direction
X: in-phase
Y: anti-phase
different direction
different direction
X: anti-phase
Y: anti-phase
same direction
different direction
X: anti-phase
Y: anti-phase
same direction
different direction
I
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 1.
352
Journal of Cognitive Neuroscience
Volume 9, Number 3
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 O R refers to the phase of the right arm movement at each sample, X R 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
..........
0
1 7 ,
3
4
5
6
7
8
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
9 1 0 1 1 1 2 1 3 1 4 1 5
- 6 4 - 2 0 2 4 6
Time (s)
Displacement X-axis
(a)
(b)
Flguie 3. Displacement-timetraces of the X-and Y-axis Component (a) and the resulting circle drawing (b).
Swinnen et al.
353
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.
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) = 2 6 . 4 1 , <
~ .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).
Results
Cycle Duration
Within Limb Relative Phase Analyses
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 = 1010.61
msec, M = 1002.04 msec, respectively). The differences
in cycle duration between the four coupling patterns
were not significant, F(3, 33) < 1 (MSe = 10957.86).
Means for the four conditions were: M Xh/Yh = 1009.26
msec, M Xmti/Y, = 1010.67 msec,MXilJYmti= 1008.18
msec, and M Xmti/Ymti= 997.19 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, 1 1) = 4.37,p >
.05 (MSe = 141.92),coupling pattern, F(3, 33) < 1. The
interaction effect was not significant either (p > .05).
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 Xand 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
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).
354
Journal of Cognitive Neuroscience
Volume 9, Number 3
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 = . 5 1 )
(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-,/Ymcondition, followed by the Xanti/Yanti,Xanti/Y-,,
and
X,,,/Yanti
condition.
107
-ff
XantiIYin
+- XinIYanti
+- XantiIYanti
8
E "I
\ I
$ 7
I
d
n5
Left
Between Limb Relative Phase Analyses
Right
Body Side
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
Figure 5a. Circle drawings
produced in the left and right
limb for a representative
subject during the Xi,/Ya
coupling conditions.
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 5 A XinMin
Right Arm
Left Arm
.-
.z
6-.--------.
- I
I
i ; 4 - 2 0 2 4 6
& 4 - 2 0 2 4 6
Displacement X-axis
Displacement X-axis
x-axis
n
E
8
6
1:
0
Y
-
4
-9
-2
5 4
-6
Time (s)
Y-axis
n
E
8
6
s
-
4
[
o2
p
.n
-2
4
4
Time (s)
Swinnen et aL
355
Figure 5b. Circle drawings
produced in the left and right
limb for a representative subject during the XantJYanti
coupling conditions.
FIGURE 5 6: X a W a n t i
Lett Ann
Rlght Arm
6
'P
$.:
.g -4
-6
-6
-4
-2
0
2
4
-6
6
-4
-2
0
2
4
6
Displaeanentx-axis
Displacementx-axis
x-axis
1
0
2
3
4
5
6
7
8
9
1 0 1 1 1 2 1 3 1 4
Time ( 8 )
Y-axis
8
8
Y
6
- 4
1
2
o o
-F&
-2
a 44
Time (s)
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 pat356
Journal of Cognitive Neuroscience
tern, transitions were observed on 4 and 44% of the
trials,respectively.The largest number of transitions were
observed during the Xmti/Yanticoupling 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) =
4 4 . 4 9 , ~c .01 (MSe = 733.94). The in-phase pattern (M
= 29.5') was performed more accurately than the antiVolume 9, Number 3
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 = 514.85) (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 =
1869.6).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 = 115.02').
Analysis of the variability scores revealed a significant
main effect for coupling pattern, F(3, 33) = 12.35,p c
.01 (MSe = 113.36). 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
r a t 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
and asymmetrical (anti-phase) (Cohen, 1971;Kelso, 1984;
Finally, assessment of the quality of circle drawing by
means of relative phase analyses between the X- and
Kelso et al., 1986;Stucchi & Viviani, 1993). Moreover, it
Y-axis component within each limb further underscored
has generally been confirmed that the former mode is
that the most consistent circle drawings were produced
produced with higher degrees of stability than the latter.
The present experiment confirmed and extended these
interlimb coupling mode. The highest
under the Xh/yin
observations to two-dimensional drawing tasks in which
variability was observed in the Xin/Yanti
condition. The
remaining two coupling conditions were positioned in
interlimb coordination modes were manipulated with
between the aforementioned patterns and did not differ
respect to both the X-and Y-axis component, resulting
substantially from each other.
in four distinct coupling patterns. Analyses of interlimb
relative phasing confirmed that the in-phase mode (he
In summary, two principles appear to determine the
accuracy and stability of bimanual coordination patterns.
mologous muscle groups) was produced with a higher
Most important is the egocentric constraint, or the gendegree of accuracy and consistency than the anti-phase
eral preference to activate the homologous muscles simode (nonhomologous muscle groups), underscoring
the importance of the egocentric constraint in bimanual
multaneously: It results in symmetrical movements with
coordination.
respect to the longitudinal axis of the body. Of seconEven though the egocentric constraint dominated, the
dary importance is the allocentric constraint, or the
extrinsic spatial orientation of the limb movements also
general preference to move the limbs in the same direcappeared to affect bimanual coordination.This is inferred
tion according to extrinsic space coordinates. It appears
that the effects induced by the allocentric constraint are
from the significant interaction observed between cousuperposed on those exhibited by the egocentric conpling mode and movement dimension. While in-phase
movements were produced with higher accuracy and
straint during bimanual coordination.
consistency with respect to the Y-axis than with respect
While the limbs appeared tightly synchronized in the
to the X-axis, anti-phase movements were generated
Xh/Yh and Xmti/Y,
conditions, detailed analyses of the
more successfully along the X- than along the Y-axis signed relative phase scores revealed a small but distinct
asynchrony or phase offset between the right and left
component (Figure 6). This finding is possibly mediated
limb. The dominant right limb led the nondominant limb
by the allocentric constraint. More specifically,the couby 9.65" in the XJYh pattern and by 13.00" in the
pling patterns that were found to be most accurate and
consistent within the in-phase and anti-phase mode inXmtdYh pattern. Considering that subjects orbited
through a 360" phase angle in approximately 1 sec (i.e.,
volved limb motions in the same allocentric direction
(i.e., in-phase movements with respect to the Y-axis 1009 and 1010 msec), the aforementioned phase lags
represent temporal offsets of about 27 and 36 msec,
component and anti-phase movements with respect to
the X-aiiscomponent). Thus, while the egocentric conrespectively. These temporal offsets are close to those
straint was dominant, the effect of the allocentric conreported by Stucchi and Viviani (1993) with respect to
straint was possibly superposed on the effect of the
ellipse drawing. In agreement with their findings,we also
egocentric constraint.
observed larger offsets during anti-phase than during
The aforementioned account is also supported by the
in-phase coordination. Stucchi and Viviani (1 993) argued
statistical analysis involving the four levels of coupling
that this time delay between both limb motions was a
pattern. The analysis of relative phase error revealed that
consequence of the lateralization of timing commands
the Xh/Y, pattern (homologous muscle groups) was
for periodic bimanual movements, necessitating the
produced most accurately at all times. The XmtdYmti transmission of timekeeping information to the other
hemisphere.
pattern (nonhomologous muscle groups) was found to
While previous studies reporting performance differbe least accurate. The two remaining coupling patterns
ences between the dominant and nondominant hand
demonstrated intermediate accuracy: the XmtdYmpattern was produced more accurately than the XuJYmti have predominantly compared both limbs under unilateral performance conditions, the present study demonpattern. While the former involved iso-directional movestrated that the superior performance of the dominant
ments with respect to both dimensions according to
limb also became evident under bimanual performance
extrinsic space coordinates, the latter pattern involved
conditions. This was inferred from fhe within-hb relanon-iso-directional movements with respect to both ditive phase analysis between the x-and Y-axiscompomensions. The pattern of data observed with respect to
the SD of relative phase was similar, except that the
nent, showing a more successful production of the circle
variability of the X,,,/Ymti
in the right than in the left limb. Furthermore,the diamepattern was lower than that of
ter of the right limb circle was more consistent than the
pattern. This is not surprising because subthe XmtdYanti
diameter of the left limb circle. These observations open
jects, trying to perform the more difficult Xmti/Ymti
patinteresting perspectives for the assessment of hand
tern, exhibited more frequent phase transitions than in
dominance or manual lateralization under bimanual in
the remaining conditions.This resulted in the production
of incorrect but more stable in-phase coupling patterns.
addition to the conventional unirnanual performance
conditions.
Often, these transitions occurred early in the trial.
358
Journal of Cognitive Neuroscience
Volume 9, Number 3
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
~~
HOMOLOGOUS
HOMOLOCOUSARMS
HOMOLOCOUS LEGS
x-axis :
in-phase
left
right
arm
arm
Y-axis :
In-phase
0 0 0 0
X-axis :
anti-phase
arm
Y-axis :
In-phase
0 0 0 0
x-axis :
left
right
in-phase
arm
arm
Y-axis:
anti-phase
0 0 0 0
left
HETEROLATERAL
HETEROLATERAL
RIGHT ARM/
LEFTLFG
LEFT A R M I
RIGHT LEG
~~
~
HOMOLATERAL
HOMOLATERAL LEFT
HOMOLATEPAL RIGHT
right
arm
left
right
arm
I
x-axis :
anti-phase
Y-axis:
anti-phase
left
right
arm
arm
0
left
0 0
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
360
Journal of Cognitive Neuroscience
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
Volume 9, Number 3
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 v p e
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 , l l ) < 1,body side,
F(1,ll) < 1,effector combination,F(2,22) = 2.7,p > .05
(MSe = 4743.4). 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 =
170.99). 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, 11) < 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 significantlyfrom
each other (p < .Ol). None of the interaction effects were
significant (p > .05).
Diameter
A 2 x 2 x 2 x 3 (Limb v p e 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 . 8 6 , ~> .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
10.17 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 v p e 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 10.96 cm for the leg within the
homolateral condition, and 8.88and 8.38 cm for the arm
Swlnnen et a1
361
and 9.27 and 10.34 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 , l l )
= 91.51,p c .01 (MSe = 0.1 1). 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 .88cm 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.
ASSOLUTEERROR. With respect to relative phase error,
the absolute deviation from a 90' phase offset between
362
Journal of Cognitive Neuroscience
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) = 2 6 . 1 1 , ~
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).
STANDARD
DEVIATION.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) = 182.78,p c .01 (MSe = 17.74).Variabilityscores 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 W r i g h t leg
coordination pattern within the homolateral condition,
and to the left W r i g h t leg and r a t &eft
leg pattern
within the heterolateral condition.The coupling task consisted of four levels: X,,JYh, XmtJyin, Xin/Ymti,and
Xmtdymti.
Volume 9, Number 3
HOMOLOGOUS
EFFECTORCOMBINATION.
The absolute error scores as well as the SD scores were significantly
lower for the homologous arm than for the leg combination,F(l, 1 1 ) = 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 12.82 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",9.32and 8.3",9.42and 8.83",and 11.13 and 8.63",
respectively. The interaction effect was significant for
absolute error but not for SD, F(3, 33) = 3.49,p < .05
(MSe = 6.2l ) , 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/Yantipattern.
HOMOLATERAL
EFFECTORCOMBINATION.
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, 1 1 ) = 23.10,p < .01 (MSe = 14.36).For SD,
the effect just failed to reach significance (&fright = 10.33,
Mlefi = 10.8),F(l,1 1 ) < 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) = 2 4 . 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",
12.55 and 11.98",12.43 and 12.47",and 10.9 and 9.2",
respectively. The interaction effect was not significant
(p > .05J
HETEROLATERAL
EFFECTOR COMBINATION. N O significant
differences were observed in the accuracy and consis
tency of circle drawing between the right a m e f t foot
and left arm/right foot combination (M = 8.74 and 10.2",
MsD = 9.08 and 9.26"),F(1, 1 1 ) 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",11.18 and 9.63",
10.58 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 L n t J Y a n t i 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
Figure 8a-1. Example of circle drawings pertaining to the
Xi,/Yi, coupling condition as
produced with the h o m o b
gous effector combination.
-
Figure 8 A1 . X in Y in
Left Leg
Right Leg
4 - 2 0 2 4 6 8
4 - 2 0 2 4 6 8
Displacement X-axis
Displacement X-axis
X-axis
h
10
B
8
v
-
6
g
4
-0 ;
aP
-2
4
Time (s)
Y-axis
h
v
8
-
8
6
4
E ;2
-0P
a 4
-6
Time (s)
THEACCURACY 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.
ABSOLUTEERROR. A 2 x 2 x 3 (Relative Phase Pattern x
Movement Axis x Effector Combination) repeated meas-
ures 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) = 280.93,pc .01 (MSe = 483.34).
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,pc .05(MSe = 18.8).Signrficant
364
Journal of Cognitive Neuroscience
differences were also observed among the three effector
combinations,F(2,22)= 186.58,pc .01 (MSe = 21 1.33).
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)= 440.48,pc .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 = 149.68).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
Volume 9, Number 3
Figure 8a-2. Example of circle drawings pertaining to the
Xm,i/Ymti coupling condition
as produced with hornole
gous effector combination.
Figure 8 A2. X anti - Y anti
Right Leg
Left Leg
? 2
4 0
-0e4
-2
g,
4 - 2 0 2 4 6 8
Displacement X-axis
Displacement X-axis
x-axis
h
E
10
z
8
~6
Time (s)
Y-axis
Time (s)
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 RELATIVEPHASE.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 s w c a n t 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)
(
F
W 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
< .05 (MSe = 3.2).
was also significant,F(2,22) = 5 . 3 7 , ~
While SD scores for the X- and Y-axis component were
very similar to each other in the heterolateral condition
(Mx= 19.15", M y = 19.2'), they showed larger differences within the homologous (Mx = 15.1",M y = 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 A x i s x Phase Pattern x Effector
Combination interaction, F(2,22) < 1.
Swinnen et al.
365
Figure 8b-1. Example of circle drawings pertaining to the
X h / Y h coupling condition as
produced with the homolatera1 effector combination.
Figure 8 B1. X in - Y in
Right Leg
Right Arm
8 6 4 - 2 6 2 4 6
4 4 - 2 0 2 4 6 8
Displacement X-axis
Displacement X-axis
x-axis
0
1
2
3
4
5
6
7
8
9
1 0 1 1 1 2 1 3 1 4 1 5
Time (s)
Y-axis
Time (s)
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 Q p e 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: X J Y h , XantJYin, XJYanti,
XantJYanti.
HOMOLOGOUS
EFFECTORCOMBINATION.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, 1 1 )
= 3 . 3 7 ,>
~ .05 (MSe = 1296.97) and F(1, 1 1 ) = 2 . 6 1 , 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) = 1 4 . 7 2 , p < .01 (MSe = 1328.3) and
variability, F(3, 33) = 3 1 . 8 9 , 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"),andXmtJYmtipattern (M = 5 6 . 6 l o , M s =
~ 21.26").
The Coordination Q p e x Coupling Task interaction
was not significant, F(3,33) c 1 , for both absolute error
and SD.
No significant difHOMOLATERAL
EFFECTORCOMBINATION.
ferences 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, 1 1 ) c 1 .
However, the left homolateral coordination pattern was
performed with lower variability than the right pattern,
mean SD = 15.65 and 22.36", respectively, F(1, 1 1 ) =
16.97,p > .01 (MSe = 127.27). A significant main effect
Volume 3,Number 3
Figure 8b-2. Example of circle drawings pertaining to the
X,,i/Ymti coupling condition
as produced with the homolatera1 effector combination.
Figure 8 82. X anti - Y anti
Right Leg
Right Arm
8 4 4 - 2 0 2 4 6 8
Displacement X-axis
Displacement X-axis
x-axis
h
5
e
i!;
10
8
6
4
32
q
-2
3 4
5-6
a
o
i
i
3
i
5
6
i
i
4
I b i i l i i 3 i 4 1 ' 5
9
1 0 1 1
Time (s)
Y-axis
0
1
2
3
4
5
6
7
8
1 2 1 3 1 4
Time (s)
for coupling task was observed with respect to absolute
error F(3, 33) = 193.6,p < .01 (MSe = 772.34) and
variability, F(3, 33) = 16.94,p < .01 (MSe = 203.11).
Absolute error and SD scores for the X,,,/Yh, Xanti/Yh,
Xh/Yanti, and XmtJYmti pattern were 18.26 and 9.34",
70.18and 22.26",95.67and 28.94",and152.53 and 15.5".
The Coordination w p e x Coupling Task interaction was
not significant for absolute error F(3,33) = 1.4,p> .05
(MSe = 549.57),but it was significant for SD, F(3,33) =
6.62,~
< .01(MSe = 92.93).Acrossall 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/Yanticondition 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 h e
molateral coordination pattern and 10.19,24.69,37.57,
and 17" for the right homolateral coordination pattern.
F(1, 11) = 5.87,p< .05 (MSe = 731.5).N o significant
differences in variability were observed between both
coordination patterns, F(1, 11) = 1.22,p > .05 (MSe =
103.51). 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)= 201.67,p< .01
(MSe = 975.49)and variability, F(3,33) = 15.1,p< .01
(MSe = 141.81).Mean absolute error and SD scores for
the XilJYh, Xmti/Yh,X,,,/Yanti,and XmtJYmti pattern were
21.98 and 11.65",37.18 and 15.73",143.74 and 23.18",
and 135.87 and 26.2O.TheCoordination'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 reHETEROLATERAL
EFFECTOR COMBINATION.
The right arm/
spect to the X,,,/Yh conditions.This was the only condileft leg pattern was generally performed more accurately
than the left arm/right leg pattern,M = 79.96and 89.42", tion free of any phase transitions.In the case of bilateral
Swinnen et al.
367
Figure 8c-1. Example of circle drawings pertaining to the
Xi,/Yh coupling condition as
produced with the heterolatera1 effector combination.
Figure 8 C1. X in - Y in
Right Arm
Left Leg
.-u1
gT------?
44-202 4 6 8
44-202 4 6 8
Displacement X-axis
Displacement X-axis
x-axis
10
-q
h
v
5
-8p
4
:
-2
5 4
6
0
1
2
3
4
5
6
7
8
9
1 0 1 1 1 2 1 3 1 4 1 5
Time (s)
Y-axis
Time (s)
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 =
1080.56).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
368
Journal of Cognitive Neuroscience
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 = 53.1 1).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 11.29 and 6.29",respectively.
The differences between the right (M = -3.92") and left
homolateral pattern (M = -.61°) also failed to reach
Volume 9, Number 3
P i p r e 8c-2. Example of circle drawings pertaining to the
X,,i/Ymti coupling condition
as produced with the hetere
lateral effector combination.
Figure 8 C2. X anti - Y anti
Right Arm
Left Leg
8 6 4 - 2 0 2 4 6 8
Displacement X-axis
Displacement X-axis
x-axis
0
1
2
3
4
5
6
7
8
1 0 1 1
9
1 2 1 3 1 4 1 5
Time (s)
Y-axis
h
8
6
E
* 4
2
-.-BP
o
-2
% 4
n 4
8
0
1
2
3
4
5
6
7
8
9
1
0
1
1
1
2
1
3
1
4
1
5
Time (s)
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 = 1488.13).
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
Table 1. Phase Transition Counts for the Homologous, Homolateral,and Heterolateral Pattern Across the Four Coupling Modes.
Homologous (%)
Arms
Homolateral (%)
Legs
Heterolateral (%h)
Left
Right
Lefl LedRight A r m
Right LedLefl A r m
0
0
0
0
Xin/Yin
0
0
XantdYin
8.33
0
Xin/ Yant i
29.17
20.83
100
100
100
100
XantiWanti
37.5
20.83
100
100
100
100
83.33
62.5
12.5
16.67
Figure 9. Relative phase error (a) and SD of relative
phase (b) with respect to the
coordination of the h o m o b
gous, homolateral, and hetere
lateral effectors.
M o p s 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).
6
220-
0
a" 15."3P 10-
$
5-
-0- Y-axis
v1
-
0
In-phase
Anti-phase
Journal of Cognitive Neuroscience
In-phase
Anti-phase
Phase Pattern
Phase Pattern
(a)
(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,
3 70
0
& 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
Volume 9, Number 3
Homologous
Heterolateral
Homolateral
160, I
160-
.2140-
3 120-
E 10.,.P
-3
d
806040-
2 20In-phase
Anti-phase
PhasePattern
In-phase
Anti-phase
Phase Pattern
r”
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-phasemovements. 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/Ymtipattern 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 a t 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
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
372
Journal of Cognitive Neuroscience
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 Xthan 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
Volume 9, Number 3
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-axiscomponent. 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-axiscomponents 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-directionalmovements. 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 maSwinnen et al.
373
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 “popularvector,’’ 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
374
Journal of Cognitive Neuroscience
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
Volume 9, Number 3
performance to which the human performer is naturally
drawn.When these tendencies do not converge with the
task requirements, they need to be overruled.The intact
CNS is endowed with the capability to overcome or
suppress these tendencies and to sculpture differentiated patterns of activity as a result of practice.
Acknowledgment
Support for the present study was provided through a grant
from the Research Council of K.U. Leuven, Belgium (Contract
No. OT/94/30) and the National Fund for Scientific Research
in Belgium (Project S 2/5 - ND.E 112). Dr. N. Dounskaia was
supported by a fellowship from the Research Council of K. U.
Leuven (Contract No. F/93/100).
Reprint requests should be send to S. €? Swinnen, Motor Control Laboratory, Dept. of Kinesiology, FLOK, Group Biomedical
Sciences, K. U. Leuven, Tervuurse Vest 101, 3001 Heverlee,
Belgium, or via e-mail to: [email protected].
AC.BE.
REFERENCES
Asanuma, H., & Okamoto, K. (1959). Unitary study on evoked
activity of callosal neurones and its effect on pyramidal
tract cell activity on cats.Japanese Journal of Physiology,
9, 473-483.
Asanuma, H., & Okuda, 0.(1962). Effects of transcallosal volleys on pyramidal tract cell activity of cat.Journal of
Neumpbysiology,25, 198-208.
Alexander, G. E., & Crutcher, M. D (1990). Preparation for
movement: neural representations of intended direction in
three motor areas of the monkey.Journal of NeumpbysiolOW, 64, 133-150.
Baldissera, E,Cavallari, I?, & Civaschi, I? (1982). Preferential
coupling between voluntary movements of ipsilateral
limbs. Neuroscience Letters, 34, 95-100.
Baldissera, E, Cavallari, I?, Marini, G., & Tassone, G. (1991). Differential control of in-phase and anti-phase coupling of
rhythmic movements of ipsilateral hand and foot. Experimental Brain Research, 83, 375-380.
Baldissera, E, Cavallari, I?, & Tesio, L. (1994). Coordination of
cyclic coupled movements of hand and foot in normal subjects and on the healthy side of hemiplegic patients. In
S. I? Swinnen, H. Heuer, J. Massion, & I? Casaer (Eds.), Znterlimb Coordination:Neural, Dynamtcal, and Cognitive
Constraints (pp. 229-242). San Diego: Academic Press.
Benecke, R., Meyer, B. U., & Freund, H.J. (1991). Reorganization of descending motor pathways in patients after hemispherectomy and severe hemispheric lesions
demonstrated by magnetic brain stimulation. Experimental Brain Research, 83, 419-426.
Bernstein, N. (1967). The co-ordination and regulation of
movement. Oxford: Pergamon Press.
Caminiti, R., Johnson, €? B., Galli, C., Ferraina, S., & Burnod, Y.
(1991). Making arm movements within different parts in
space: the premotor and motor cortical representation of
a coordinate system for reaching to visual targets.Journal
of Neumscience, I I , 1182- 1197.
Carson, R. G., Byblow, W. D., & Goodman, D. (1994). The dynamical substructure of bimanual coordination. In S I!
Swinnen, H. Heuer, J. Massion, & €? Casaer (Eds.), Znterlimb
coordination:neural, dynamical, and cognitive constraints (pp. 319-337). San Diego: Academic Press.
Cincotta, M., Ragazzoni, A,, Descisciolo, G., Pinto, E,Maurri,
S., & Barantoni, E (1994). Abnormal projection of corticospinal tracts in a patient with congenital mirror movements. Neumpbysiologie Clinique-Clinical
Neuropbysiology, 24, 427-434.
Cohen, L. (1971). Synchronous bimanual movements performed by homologous and non-homologous muscles. Perceptual and Motor Skills, 32, 639-644.
Cohen, L. G., Meer, J., T e a I., Bierner, S., Leiderman, D. B.,
Dubinsky, R. M., Sanes,J. N., Jabbari, B., Branscum, B., &
Hallett, M. (1991). Congenital mirror movements. Abnormal organization of motor pathways in two patients.
Brain, 114, 381-403.
Colebatch, J. G., & Gandevia, S. C. (1989). The distribution of
muscular weakness in upper motor neuron lesions affecting the arm. Brain, 112, 749-763.
Passingham, R. E,Friston, K. J.,
Colebatch, J. G., Deiber, M. €?,
& Frackowiak, R. S. J. (1991). Regional cerebral blood flow
during voluntary arm and hand movements in human subjects. Journal of Neuropbysiology, 65, 1392- 1401.
Cruse, H., & Warnecke, H. (1992). Coordination of the legs of
a slow-walking cat. Experimental Brain Research, 89,
147- 156.
Crutcher, M. D., & Alexander, G E. (1990). Movement-related
neuronal activity selectively coding either direction or
muscle pattern in three motor areas of the monkey.Journal of Neumpbysiology, 64, 151- 163.
Evarts, E. V. (1968). Relation of pyramidal tract activity to
force exerted during voluntary movement.Journal of
Neuropbysiology, 3 1, 14-27.
Ferbert, A., Priori, A,, Rothwell,J. C., Day, B. L., Colebatch,
J. G., & Marsden, C. D. (1992). Interhemispheric inhibition
of the human motor cortex. Journal of Pbysiology, 453,
525-546.
Forget, R., Boghen, D., Attig, E.,& Lamarre, Y. (1986). Electromyogmphic studies of congenital mirror movements.
Neurology, 36, 1316-1322.
Fortier, I? A., Kalaska,J. E,& Smith, A. M. (1989). Cerebellar
neuronal activity related to whole-arm reaching movements in the monkey.Journal of Neuropbysiology, 62,
198-21 1.
Franz, E. A., Zelaznik, H. N., & McCabe, G. (1991). Spatial
topological constraints in a bimanual task. Acta Psychologica, 77, 137- 151.
Gazzaniga, M. S., Bogen,J. E., & Sperry, R. W. (1967).
Dyspraxia following division of the cerebral commissures.
Archives of Neurology, 16, 606-612.
Georgopoulos, A. I? (1991). Higher order motor control. Annual Review of Neumscience, 14, 361-377.
Georgopoulos, A. I?, Kettner, R. E.,& Schwartz, A. B. (1988).
Primate motor cortex and free arm movements to visual
targets in three-dimensional space. II.Coding of the direction of movement by a neuronal population. Journal of
Neuroscience,8, 2928-2937.
Georgopoulos, A. I?, Taira, M., & Lukashin, A. (1993). Cognitive neurophysiology of the motor cortex. Science, 260,
47-52.
Gunderson, C. H., & Solitare, G. B. (196s).Mirror movements
in patients with the Klippel-Feil syndrome. Archives of
Neurology, 18, 675-679.
Halbertsma, J. (1983). The stride cycle of the cat: the modelling of locomotion by computerized analysis of automatic
recordings. Ada Pbysiologica Scandinavica fSuppl.J,521,
1-75
Haken, H., Kelso,J. A. S., Bunz, H. (1985). A theoretical model
of phase transitions in human bimanual coordination. Bie
logical Cybernetics, 51, 347-356.
Heuer, H. (1985). Intermanual interactions during simultaneSwinnen et al.
375
ous execution and programming of finger movements.
Journal of Motor Behaviol; 17, 335-354.
Jones, R. D., Donaldson, I. M., Parkin, I? J. (1989). Impairment
and recovery of ipsilateral sensory-motor function following unilateral cerebral infarction. Brain, 112, 113-132.
Jung, R., & Dietz, V (1975). Venogerter Start der Willkiirbewegung bei Pyramidenlasionen des Menschen. Archiven
Psychiatrischen Nervenkranken, 221, 87- 109.
Kalaska,J. E, Caminiti, R., & Georgopoulos, A. I? (1983). Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and
comparison with motor cortex. Experimental Brain Research, 51, 247-260.
Kalaska,J. E, Cohen, D. A. D., Prud’homme, M., & Hyde, M. L.
(1990). Parietal area 5 neuronal activity encodes movement kinematics, not movement dynamics. Experimental
Brain Research, 80, 351-364.
Kelso,J. A. S. (1984). Phase transitions and critical behavior
in human bimanual coordination. American Journal of
Pbysiology: Regulatory, Integrative, and Comparative
Pbysiology, 15, 1000-1004.
Kelso,J. A. S., & Jeka, J. J. (1992). Symmetry breaking dynamics of human interlimb coordination. Journal of Experimental Psychology:Human Perception and Performance,
18, 3,645-668.
Kelso,J. A. S., Scholz,J. I?, & Schoner, G. (1986). Nonequilibrium phase transitions in coordinated biological motion:
critical fluctuations. Pbysics Letters, A1 18, 279-284.
Kelso,J. A. S., Southard, D. L., & Goodman, D. (1979). On the
coordination of two-handed movements. Journal of Experimental Psychology:Human Perception and Performance,
2, 229-238.
Kuypers, H. G. J. M. (1973). The anatomical organization of
the descending pathways and their contributions to motor control especially in primates. In J. E. Desmedt (Ed.),
New developments in electmmyograp/y and clinical
neuropbysiology,Vol I11 (pp. 38-68). Basel, Switzerland:
Karger.
Marteniuk, R. G, MacKenzie, C. L., & Baba, D. M. (1984). Bimanual movement control: information processing and interaction effects. The Quarterly Journal of Experimental
Psychology, 36A, 335-365.
Meige, H. (1901). Les mouvements en miroir; leurs applications pratiques et therapeutiques. Revue Neurologique,
19, 780-782.
Mitchell, S. J., Richardson, R. T., Baker, E H., & DeLong, M. R.
(1987). The primate globus pallidus: neuronal activity related to direction of movement. Experimental Brain Research, 68, 491-505.
Muller, E, Kunesch, E., Binkofski, E, & Freund, H. J. (1991). Residual sensorimotor functions in a patient after right-sided
hemispherectomy. Neuropsychologia, 29, 125-145.
Nass, R. (1985). Mirror movement asymmetries in congenital
hemiparesis: The inhibition hypothesis revisited. Neurol00,
35, 1059-1062.
Peters, M. (1988). Footedness: Asymmetries in foot preference and skill and neuropsychological assessment of foot
movement. Psychological Bulletin, 103, 179- 192.
Preilowski, B. (1975). Bilateral motor interaction: Perceptualmotor performance of partial and complete “split-brain”patients. In K. S. Zulich, 0.Creutzfeldt, & G. C. Galbraith
(Eds.), Cerebral localization (pp. 115-132). Berlin:
Springer.
Preilowski, B. (1990). Intermanual transfer, interhemispheric
interaction and handedness in man and monkeys. In C. Trevarthen (Ed.), Brain circuits and functions of the mind
3 76
Journal of Cognitive Neuroscience
(pp. 168- 180). Cambridge, England: Cambridge University
Press.
Prud’homme, M. J. L., & Kalaska,J. E (1994). Proprioceptive
activity in primate primary somatosensory cortex during
active arm reaching movements.Journal of Neuropbysiol00,
72, 2280-2301.
Regli, E, Filippa, G., & Wiesendanger, M. (1967). Hereditary
mirror movements. Archives of Neurology, 16, 620-623.
Scholz,J. I?, & Kelso,J. A. S. (1989). A quantitative approach
to understanding the formation and change of coordinated movement patterns.Journal of Motor Behauiot; 21,
122-144.
Schott, G. D., & Wyke, M. A. (1981). Congenital mirror movements. Journal of Neurology, Neurosurgery, and Psychiatry, 44, 586-599.
Schwartz, A. B. (1994). Direct cortical representation of drawing. Science, 265, 540-542.
Semjen, A., Summers,J. J., & Cattaert, D. (1995). Hand coordination in bimanual circle drawing.Journal of Experimental Psychology;Human Perception and Performance, 21,
1139- 1157.
Serrien, D. J., & Swinnen, S. I? (in press a). Coordination constraints induced by effector combination under isofrequency and multi-frequency conditions. Journal of
Experimental Psychology:Human Perception and Performance.
Serrien, D. J., & Swinnen, S. F! (in press b). The production of
iso-frequency and multi-frequency coordination patterns
as a function of the planes of motion. Quarterly Journal
of Experimental Psychology.
Sherwood, D. E. (1994). Hand preference, practice order, and
spatial assimilations in rapid bimanual movement. Journal
of Motor Behaviol; 26, 123-134.
Shinoda, Y., Kakei, S., & Sugiuchi, Y. (1994). Multisegmental
control of axial and limb muscles by single long descending motor tract axons. Lateral versus medial descending
motor systems. In S. I? Swinnen, H. Heuer, J. Massion, & I?
Casaer (Eds.), Interlimb coordination: neural, dynamical,
and cognitive constraints (pp. 31-47). San Diego: Academic Press.
Stucchi, N., & Viviani I? (1993). Cerebral dominance and asynchrony between bimanual two-dimensional movements.
Journal of Experimental Psychology:Human Perception
and Performance, 19, 1200-1220.
Swinnen, S. I?, Dounskaia, N., Verschueren S., Serrien, D. J., &
Daelman, A. (1995). Relative phase destabilization during interlimb coordination: The disruptive role of kinesthetic afferences induced by passive movement. Experimental
Brain Research, 105,439-454.
Swinnen, S . I?,Jardin, K., & Meulenbroek, R. (1996). Betweenlimb asynchronies during bimanual coordination: effects
of manual dominance and attentional cueing. Neuropsychologia, 34, 1203-1213.
Swinnen, S . I?, Serrien, D. J., Walter, C. B., & Philippaerts, R.
(1995). The organization of patterns of multilimb coordination as revealed through reaction time measures. Experimental Brain Research, 104, 153-162.
Swinnen, S. I?,Van Langendonk, H., Verschueren, S., Peeters,
G., Dom, R., & De Weerdt, W. (in press). Interlimb coordination deficits in Parkinson patients during the production
of two-joint oscillations in the sagittal plane. Movement
Disorders.
Swinnen, S. I?, Walter, C. B., Beirinckx, M. B., & Meugens, I? E
(1991). Dissociating the structural and metrical specifications of bimanual movement. Journal of Motor Behaviol;
23, 263-279.
Volume 9, Number 3
Swinnen, S. I?, Walter, C. B., Lee, T. D., & Serrien, D. J. (1993).
Acquiring bimanual skills: Contrasting forms of information feedback for interlimb decoupling.Journal of Experimental Psychology:Learning, Memoly, C Cognition, 19,
1328-1344.
Swinnen, S., Walter, C. B., & Shapiro, D. C. (1988). The coordination of limb movements with different kinematic patterns. Brain and Cognition, 8, 326-347.
Swinnen, S. I?, Young, D. E., Walter, C. B., & Serrien, D. J.
(1991). Control of asymmetrical bimanual movements. Experimental Brain Research, 85, 163- 173.
Tuller, B., & Kelso, J. A. S. (1989). Environmentally-specified
patterns of movement coordination in normal and splitbrain subjects. Experimental Brain Research, 75, 306316.
Turvey, M. T. (1990). Coordination. American Psychologtst,
45, 938-953.
Walter, C. B., & Swinnen, S. I? (1990). Kinetic attraction during bimanual coordination.Journal of Motor Behaviol;
22, 451-473.
Walter, C. B., & Swinnen, S. I? (1992). Adaptive tuning of interlimb attraction to facilitate bimanual decoupling. Journal
of Motor Behaviol; 24, 95-104.
Walter, C. B., & Swinnen, S. I? (1994). The formation and dissolution of “bad habits” during the acquisition of coordination skills. In S. I? Swinnen, H. Heuer,J. Massion, & I?
Casaer (Eds.), Interlimb coordination: neural, dynamical,
and cognitive constraints (pp. 491-513). San Diego: Academic Press.
Wassermann, E. M., Pascual-Leone,A., & Hallett, M. (1994).
Cortical motor representation of the ipsilateral hand and
arm. Experimental Brain Research, 100,121-132.
Westphal, C. (1873). ijber einige Bewegungsercheinungen an
geliihmten Gliedern. Archiv fur Psychiatrischen Nervenkrankheiten, 4, 747-759.
Wetzel, M. C., & Stuart, D. G. (1977). Activation and coordination of vertebrate locomotion. In R. M. Alexander & G.
Goldspink (Eds.), Mechanics and Ene?getics of Animal Locomotion @p. 115-152). New York: Wiley.
Wiesendanger, M., Wicki, U., & Rouiller, E. (1994). Are there
unifying structures in the brain responsible for interlimb
coordination? In S. I? Swinnen, H. Heuer,J. Massion, & I?
Casaer (Eds.), Interlimb coordination: neural, dynamical,
and cognitive constraints (pp. 179-207). San Diego: Academic Press.
Woodworth, R. S. (1899). The accuracy of voluntary movement. Psychological Review, 3 (Suppl. 2).
Woods, B. T., & Teuber, H. L. (1978). Mirror movements after
childhood hemiparesis. Neurology, 28, 1152- 1158.
Zaidel, D., & Sperry, R. W. (1977). Some long-term effects of
cerebral commissurotomy in man, Neuropsychologia, 15,
193-204.
Ziilch, K. J., & Miiller, N. (1969). Associated movements in
man. In I? J. Vinken & G. W. Bruyn (Eds.), Handbook of
clinical neurology, Vol. I , Disturbances of nervous function (pp. 404-426). Amsterdam: North-Holland.
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