Full text of DOI:10.1093/geronb/55.5.P295

Journal of Gerontology: PSYCHOLOGICAL SCIENCES
Copyright 2000 by The Gerontological Society of America
2
000, Vol. 55B, No. 5, P295–P303
Age-Related Deterioration of Coordinated
Interlimb Behavior
1
1
2
Deborah J. Serrien, Stephan P. Swinnen, and George E. Stelmach
1Motor Control Laboratory, Department of Kinesiology, K.U. Leuven, Belgium.
2Motor Control Laboratory, Arizona State University, Tempe.
Younger and older participants performed two-limb coordination patterns of homologous (similar) and nonho-
mologous (dissimilar) effectors during 1:1 synchronization, according to the in-phase or anti-phase mode. The
aim of the study was to examine age-related changes during the production of these basic movement patterns and
their relative stability difference. The findings revealed that the aging process modulated the coordination dy-
namics as a function of effector system characteristics. Whereas the homologous system was resistant to age-
related deficits, movements of the nonhomologous system showed coordinative degradation that was most appar-
ent during execution of the anti-phase mode. The latter performance regression is argued to be an expression of
age-dependent declines in cognitive regulation and afferent information processing. This implies that deteriora-
tion in coordinated behavior across the life span may be strongly task dependent because of a combined effect of
cognitive and sensory components.
GING is often associated with a deterioration in motor
performance. One predominant characteristic is age-
life as well as social and recreational activities is a prototype
of a complex task that demands attentional regulation and
sensory monitoring of various sources. Therefore, it can be
hypothesized that coordinated actions impose an additional
load on older as compared with younger adults because of
age-related declines in cognitive processing (Clark, 1996;
Hasher & Zacks, 1988; McDowd, Vercruyssen, & Birren,
1991) and deterioration in sensory structures and function
(Skinner, Barrack, & Cook, 1984; Schaumburg, Spencer, &
Ochoa, 1983; Stelmach & Sirica, 1986).
Previously, research on coordinated interlimb behavior
has demonstrated that certain movement patterns represent
preferred modes of coordination that express the intrinsic
behavior of the motor system (Kelso, 1984; Turvey, 1990).
One such configuration is moving segments rhythmically with
equal tempo according to the in-phase or anti-phase mode.
When performed in the sagittal plane, these coordination
modes can be associated with the directional requirements
of the action pattern. In particular, segments move in the
same direction in extrinsic space during in-phase, whereas
they move in different directions during anti-phase (Baldissera,
Cavallari, Marini, & Tassone, 1991).
Even though interlimb synchronization represents a primary
constraint, it has been noticed that the movement dynamics
depend on the type of coordination mode (in-phase vs. anti-
phase) as well as the type of limb combination (homologous
vs. nonhomologous). First, in-phase movements are produced
more successfully than anti-phase movements (e.g., Kelso,
1984). Commonly, this performance difference has been il-
lustrated as an increased instability of the anti-phase mode
when cycling frequency is increased until it can no longer
be continued and a transition toward the inphase mode occurs.
Applying an identical frequency scaling when moving ac-
cording to the in-phase mode does not give rise to transitions.
Second, isofrequency coordination is more successful for
homologous (similar) than for nonhomologous (dissimilar)
A
related slowing in cognitive and motor processes (Birren,
Woods, & Williams, 1980; Cerella, Poon, & Williams, 1980),
which is reflected in longer reaction and movement execution
times. There are various hypotheses concerning age-related
slowing (Spirduso, 1995). One of them is that slowing occurs
because of increased neural noise (i.e., signals are less well
detected in the central nervous system), resulting in a reduced
signal-to-noise ratio (Salthouse, 1982). Central and/or periph-
eral factors underlie this lowered signal-to-noise ratio and
more time is needed to examine signals and discard neural
noise, leading to increased processing demands. Age-related
slowing in the execution of movement patterns has been an
extensively investigated topic and an abundance of literature
is available (for reviews, see Diggles-Buckles, 1993; Spirduso,
1
995; Welford, 1984).
Clearly, behavioral slowing that refers to a modification in
absolute timing represents an important feature of movement
performance in older adults. Another temporal issue represents
relative timing, that is, the ability to synchronize movement
patterns. Not much is known about modifications in the quality
of interlimb behavior across the life span. Inherent changes
in the underlying coordination process due to degeneration
of central or peripheral components may have significant
functional consequences. Previously, studies involving pos-
tural requirements and manual actions have revealed that
aging leads to declines in coordinated activities (Bennett &
Castiello, 1994; Greene & Williams, 1996; Pohl, Winstein, &
Fisher, 1996; Spirduso & Choi, 1993; Stelmach, Amrhein,
Goggin, 1988; Woollacott, Shumway-Cook, & Nashner,
986). In addition, movement complexity represents a
meaningful factor that contributes to motor deficits with age
Light & Spirduso, 1990). However, the control of rhythmical
multilimb behavior and modifications due to age have not
been explored in detail. This type of action that underlies daily
&
1
(
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SERRIEN ET AL.
effectors. That 1:1 synchronization is less stringent for non-
homologous than for homologous limbs has been interpreted
to result from natural frequency dissimilarities between the
upper and lower limbs and from differences in afferent and/or
efferent command structures (Kelso & Jeka, 1992; Serrien
&
Swinnen, 1997, 1998; Swinnen, Dounskaia, Verschueren,
Serrien, & Daelman, 1995).
Provided that in-phase and anti-phase coordination are
spontaneously generated movement patterns in human be-
havior, the question arises of how accurate and stable these
configurations remain across the life span. The aim of the
present study was to investigate age-related modifications
in the production of these elementary coordination modes
and their relative stability difference. In addition, because of
the observed performance differences between homologous
and nonhomologous conditions in young adults, it was also
of interest to examine whether these dissimilarities remain
present to the same degree in older adults. Accordingly, an
experimental paradigm was set up in which two-limb coor-
dination patterns were compared across younger and older
participants. Our aim was to describe age-related changes in
movement performance and to identify potential determi-
nants that might be responsible for the reduced quality of
coordinated interlimb behavior due to aging.
Figure 1. Side view of the experimental apparatus.
The task required cyclical flexion and extension move-
ments with a 1:1 frequency ratio. There were six perfor-
mance conditions: homologous (upper limbs, lower limbs),
homolateral (right side, left side), and heterolateral (right
arm/left leg, left arm/right leg). The coordination modes in-
cluded in-phase (isodirectional) and anti-phase (nonisodi-
rectional) movements.
METHODS
Participants
A group of eight younger (mean age ϭ 24 years; 5
women and 3 men) and eight older (mean age ϭ 75 years; 5
women and 3 men) adults participated in the study. All were
right-handed and had no history of neurological disease or
skeletomotor dysfunction. None of the participants was tak-
ing any medication at the time of testing. The older adults
were in good health, ambulatory, and lived independently
either in the general community or in a retirement commu-
nity. They were all involved in daily activities and hobbies.
A variety of socioeconomic classes and educational levels
were represented. Participants had not been involved in a sim-
ilar experiment and were naive with respect to the purpose
of the experiment. Informed consent was obtained from all
participants.
Procedure
The participants were seated in the chair and their limbs
were attached to the levers. Shoes were removed to avoid
additional loading of the legs. In the start position, the joint
angle was approximately 90Њ in the lower limbs and 110Њ in
the upper limbs. Before the experiment started, the partici-
pants were informed about the goal of the test. They were
instructed to make cyclical two-limb movements across the
total duration of a trial (15 s) at the pace provided by a met-
ronome (60 beats/min). Participants were asked to preserve
spatial and temporal requirements of the movement patterns
within and between trials. Order of the trials was counter-
balanced across participants, between and within limb com-
binations and coordination modes. Two trials per condition
were performed, resulting in a total of 24 trials. Following a
Apparatus and Task
Participants were seated in a chair that allowed indepen-
dent motion of the forearms and lower legs in the sagittal
plane (Figure 1). The chair consisted of a welded steel
frame, a wooden back support, and a seat that could be ad-
justed in the forward–backward direction. The upper and
lower limbs were attached to levers which were 45 cm (18
in.) in length for the upper limbs and 65 cm (26 in.) for the
lower limbs. Participants performed flexion and extension
movements around the elbow and knee joints. The setup
was built such that the horizontal axes of rotation of the le-
vers could be aligned with the center of rotation of the el-
bow and knee joints. Joint angles were registered through
built-in shaft encoders (Tamagawa, 4096 bits/revolution),
mounted at the axis of rotation of each joint. The data were
sampled at 150 Hz.
“
ready” command, a 400-Hz tone was presented that led to
initiation of a trial.
Measures
Phase synchronization.—Interlimb coordination was
quantified by means of relative phase that represents the dif-
ference in phase angle between two segments moving con-
currently. The phase angles for each segment were esti-
mated from the phase plane trajectories that refer to position
versus velocity at each instant. Normalizing both coordi-

AGING AND INTERLIMB COORDINATION
P297
nates to the unit circle, the individual phase angles (⌽) were
obtained through the following formula: ⌽ ϭ tan ([dx/dt]/
x), whereby x refers to the normalized position and dx/dt to
the normalized instantaneous velocity (Scholz & Kelso,
ance (ANOVAs), with repeated measures on the last two
factors. The first factor included the younger and older
adults, whereas the second factor represented the coordina-
tion modes: in-phase and anti-phase. The third factor re-
ferred to the homologous, homolateral, and heterolateral
limb combinations.
Additional phase analyses were conducted to examine
coordination differences within effector combination. These
consisted of separate 2 (group) ϫ 2 (coordination mode) ϫ
2 (limb condition) ANOVAs, with repeated measures on the
last two factors. The first factor referred to the younger and
older participants, whereas the second factor represented the
in-phase and anti-phase coordination modes. The third fac-
tor included the conditions for the different limb combina-
tions: upper versus lower limbs, right versus left side, right
arm/left leg versus left arm/right leg.
The analyses for cycle duration and amplitude consisted
of 2 (group) ϫ 2 (coordination mode) ϫ 3 (limb combina-
tion) ANOVAs, with repeated measures on the last two fac-
tors. The first factor represented the younger and older
adults, whereas the second factor included the coordination
modes: in-phase and anti-phase. The third factor referred to
the homologous, homolateral, and heterolateral limb combi-
nations.
Ϫ1
1
989). Velocity was obtained by differentiation of the dis-
placement data. Amplitude rescaling was done for each half
cycle: Positive amplitudes were divided by their peak posi-
tive amplitude, and negative amplitudes were divided by
their respective peak negative amplitude score. The phase
angles were subtracted for each data sample, resulting in a
continuous estimate of relative phase, that is, ␾ ϭ ⌽ Ϫ ⌽ .
1
2
In addition, the absolute deviation from the intended rela-
tive phase (0Њ and 180Њ) was extracted at the two peak posi-
tions of flexion and extension, providing a measure of rela-
tive phase accuracy. The within trial standard deviation
around the mean relative phase represented relative phase
variability and is indicative of the stability with which the
coordination pattern is executed. Moreover, a high degree
of pattern stability (low variability) can be associated with a
preferred behavioral state, whereas a decrease in pattern sta-
bility occurs when moving away from it. Mean deviation
and variability scores were calculated for each trial and av-
eraged across experimental condition.
Cycle duration and amplitude.—To examine the tem-
poral and spatial parameters of movement organization, the
cycle duration and amplitude of the limb trajectories were
determined. Cycle duration was obtained by measuring the
time that elapsed between two consecutive positive peaks.
Amplitude was determined by calculating the absolute
value of the peak-positive to peak-negative amplitude. For
both timing and amplitude, within trial standard deviation
was calculated to assess temporal and spatial variability, re-
spectively. Mean and variability scores were calculated per
trial and subsequently averaged for each segment across ex-
perimental condition.
RESULTS
Phase-Synchronization
The mean deviation scores from the required relative
phase showed a significant main effect of group, F(1,14) ϭ
30.4, p Ͻ .0001, coordination mode, F(1,14) ϭ 11.5, p Ͻ
.01, and limb combination, F(2,28) ϭ 35.4, p Ͻ .0001. All
two-way interactions were significant: Group ϫ Coordina-
tion Mode, F(1,14) ϭ 5.7, p Ͻ .05; Group ϫ Limb Combi-
nation, F(2,28) ϭ 21.7, p Ͻ .0001; and Coordination Mode ϫ
Limb Combination, F(2,28) ϭ 9.3, p Ͻ .001. The Group ϫ
Coordination Mode ϫ Limb Combination interaction also
reached significance, F(2,28) ϭ 9.8, p Ͻ .001. Figure 2
demonstrates that phasing accuracy did not differ between
younger and older adults for homologous conditions (p Ͼ
Data Analyses
The main phase analyses consisted of 2 (group) ϫ 2 (co-
ordination mode) ϫ 3 (limb combination) analyses of vari-
Figure 2. The absolute deviation (AD) of relative phase for the different effector combinations during in-phase and anti-phase coordination
for younger and older adults.

P298
SERRIEN ET AL.
.
05). Conversely, it deteriorated for the older adults during
whereas it deteriorated for the older adults during anti-phase
movements (M ϭ 64.3Њ) as compared with in-phase move-
ments (M ϭ 25.9Њ). The Group ϫ Limb Condition interac-
tion was also significant, F(1,14) ϭ 5.3, p Ͻ .04. This inter-
action suggested that relative phase accuracy was similar
for the younger adults on both sides of the body (M ϭ 13.7Њ
for the left side, M ϭ 12.3Њ for the right side), whereas qual-
ity of performance decreased on the left side (M ϭ 53.6Њ) as
compared with the right side (M ϭ 36.7Њ) for the older
adults. Relative phase variability demonstrated a significant
main effect of group, F(1,14) ϭ 18.5, p Ͻ .001, and coordi-
nation mode, F(1,14) ϭ 24.1, p Ͻ .001. The Group ϫ Coor-
dination Mode interaction was significant, F(1,14) ϭ 15.9,
p Ͻ .01. This interaction revealed that phasing variability
was similar across coordination modes for the younger
adults (M ϭ 7.1Њ for in-phase, M ϭ 9.1Њ for anti-phase),
whereas it increased for anti-phase movements (M ϭ 27.9Њ)
as compared with in-phase movements (M ϭ 9.2Њ) for the
older adults.
For the heterolateral limbs, relative phase accuracy
showed that the older adults (M ϭ 25.0Њ) were less success-
ful than the younger adults (M ϭ 14.3Њ), F(1,14) ϭ 6.9, p Ͻ
.02. Relative phase variability demonstrated significant
main effects of group, F(1,14) ϭ 5.4, p Ͻ .05, and coordi-
nation mode, F(1,14) ϭ 9.9, p Ͻ .01. The main effect of
limb condition was also significant, indicating that the right
arm/left leg condition (M ϭ 7.9Њ) was produced with higher
stability than the left arm/right leg condition (M ϭ 13.0Њ),
F(1,14) ϭ 8.6, p Ͻ .02. The Group ϫ Coordination Mode
interaction reached significance, F(1,14) ϭ 4.8, p Ͻ .05.
This interaction suggested that the younger adults per-
formed the coordination modes with virtual equal degree of
variability (M ϭ 7.6Њ for in-phase, M ϭ 9.2Њ for anti-phase),
whereas it deteriorated during anti-phase movements (M ϭ
16.9Њ) as compared with in-phase movements (M ϭ 8.4Њ)
for the older adults.
homolateral and heterolateral conditions and more strongly
for anti-phase than in-phase coordination.
Relative phase variability revealed a significant main ef-
fect of group, F(1,14) ϭ 16.4, p Ͻ .01, coordination mode,
F(1,14) ϭ 51.5, p Ͻ .0001, and limb combination, F(2,28) ϭ
2
0.1, p Ͻ .0001. All two-way interactions were significant:
Group ϫ Coordination Mode, F(1,14) ϭ 21.1, p Ͻ .001,
Group ϫ Limb Combination, F(2,28) ϭ 9.6, p Ͻ .001, and
Coordination Mode ϫ Limb Combination, F(2,28) ϭ 7.0, p Ͻ
.
01. The Group ϫ Coordination Mode ϫ Limb Combina-
tion interaction was also significant, F(2,28) ϭ 7.2, p Ͻ .01.
Figure 3 shows that coordinative stability of the younger
and older participants did not differ during homologous
conditions. Conversely, relative phase variability increased
for the older adults during homolateral and heterolateral
conditions, especially during anti-phase movements.
Additional analyses of relative phase were conducted to
examine differences within the limb combinations. For the
homologous limbs, relative phase accuracy showed that
younger adults (M ϭ 8.3Њ) were more successful than older
adults (M ϭ 12.9Њ), F(1,14) ϭ 5.8, p Ͻ .05. Also, in-phase
coordination (M ϭ 9.1Њ) was more accurate than anti-phase
coordination (M ϭ 12.1Њ), F(1,14) ϭ 20.3, p Ͻ .001. In ad-
dition, upper limb movements (M ϭ 6.8Њ) were performed
with a higher degree of accuracy than lower limb move-
ments (M ϭ 14.4Њ), F(1,14) ϭ 5.2, p Ͻ 05. The latter find-
ing confirms previous data with the same task (Serrien &
Swinnen, 1997). Relative phase variability revealed a main
effect of coordination mode, F(1,14) ϭ 41.8, p Ͻ .0001.
The mean scores were 5.6Њ and 6.7Њ for in-phase and anti-
phase movements, respectively.
For the homolateral limbs, relative phase accuracy
showed a significant main effect of group, F(1,14) ϭ 43.4,
p Ͻ .0001, coordination mode, F(1,14) ϭ 12.5, p Ͻ .01, and
limb condition, F(1,14) ϭ 7.3, p Ͻ .02. The Group ϫ Coor-
dination Mode interaction was significant, F(1,14) ϭ 10.5,
p Ͻ .01. This interaction indicated that phasing accuracy
was similar across coordination modes for the younger
adults (M ϭ 12.1Њ for in-phase, M ϭ 13.8Њ for anti-phase),
Cycle Duration
Mean cycle duration revealed that older adults (M ϭ
1136.5 ms) produced slower cycles than younger adults (M ϭ
Figure 3. The standard deviation (SD) of relative phase for the different effector combinations during in-phase and anti-phase coordination
for younger and older adults.

AGING AND INTERLIMB COORDINATION
P299
1
002.0 ms) who complied more successfully with the im-
limbs, respectively. In addition, in-phase movements (M ϭ
5.7Њ) were less variable than anti-phase movements (M ϭ
6.6Њ), F(1,14) ϭ 9.4, p Ͻ .01.
posed metronome pacing, F(1,14) ϭ 6.9, p Ͻ .02. The main
effect of limb combination was also significant, F(2,28) ϭ
3
.4, p Ͻ .05. The mean scores were 1015.0 ms, 1116.2 ms,
and 1076.5 ms for the homologous, homolateral, and hetero-
lateral limbs, respectively.
Phase Transitions
Even though in-phase and anti-phase movements are pre-
ferred coordination modes, fluctuations around their mean
states are inevitable because of the systems’ inherent noisi-
ness. In this respect, relative phase variability is a relevant
parameter to conceptualize coordinative stability and to ef-
fect phase transitions between patterns (Kelso, 1995). The
smaller the fluctuations, the more stable the coordination
mode and the more solid the coherence between the underly-
ing components. Conversely, when coordinative variability
is strongly increased, a phase transition is likely to occur to-
ward a pattern with a relatively lower degree of fluctuations.
In view of the previously described differential level of
stability between in-phase and anti-phase coordination and
between both groups of adults, trials were counted in which
phase transitions occurred. The results were consistent with
the hypothesis that high variability underlies coordinative
change. In particular, no transitions were observed for the
younger adults or, during homologous conditions, for the
older adults. During homolateral conditions, 25% of the tri-
als produced by the older adults were characterized by a
transition. The latter always occurred in trials during which
the anti-phase mode was initially adopted, resulting in a
change toward the in-phase mode. Moreover, older partici-
pants always started off appropriately in the anti-phase pat-
tern, whereas a transition to the in-phase pattern was made
after a few seconds of practice. All elderly adults except one
participant experienced a pattern change in one or more tri-
als. Therefore, it can be suggested that transitory events
characterize coordinated behavior of older adults when task
constraints become too demanding. During heterolateral
conditions, phase transitions were noted in 3% of the older
adults’ trials. Also in this case, coordinative change always
took place from an initially controlled anti-phase pattern to-
ward an in-phase pattern.
Temporal variability revealed a significant main effect of
coordination mode, F(1,14) ϭ 10.0, p Ͻ .01, and limb com-
bination, F(2,28) ϭ 5.0, p Ͻ .02. The two-way interactions
of Group ϫ Limb Combination, F(2,28) ϭ 3.4, p Ͻ .05, and
Coordination Mode ϫ Limb Combination, F(2,28) ϭ 6.6, p Ͻ
.
01, were significant. The Group ϫ Coordination Mode ϫ
Limb Combination interaction was also significant, F(2,28) ϭ
.4, p Ͻ .05. Figure 4 shows that temporal variability in-
3
creased substantially for the older as compared with the
younger adults during nonhomologous conditions when
anti-phase coordination was required.
Amplitude
Mean amplitude showed a significant main effect of co-
ordination mode, F(1,14) ϭ 31.7, p Ͻ .01. The Group ϫ
Coordination Mode interaction was significant, F(1,14) ϭ
1
1.8, p Ͻ .01. This interaction indicated that younger adults
increased their amplitude during anti-phase coordination (M ϭ
1
1
10.0Њ) as compared with in-phase coordination (M ϭ
02.6Њ), whereas older adults maintained their amplitude
during both configurations (M ϭ 123.8Њ for in-phase, M ϭ
24.3Њ for anti-phase). The Coordination Mode ϫ Limb
Combination interaction was significant, F(2,28) ϭ 6.0, p Ͻ
01. This interaction suggested that amplitude was equal for
both coordination modes during homologous conditions (M ϭ
15.4Њ for in-phase, M ϭ 114.1Њ for anti-phase), whereas it
1
.
1
was dissimilar during homolateral conditions (M ϭ 111.1Њ for
in-phase, M ϭ 118.3Њ for anti-phase) and heterolateral condi-
tions (M ϭ 133.1Њ for in-phase, M ϭ 119.2Њ for anti-phase).
Spatial variability was lower for the younger (M ϭ 5.2Њ)
than for the older adults (M ϭ 7.1Њ), F(1,14) ϭ 8.9, p Ͻ .01.
The main effect of limb combination was also significant,
F(2,28) ϭ 10.9, p Ͻ .001. The mean scores were 5.6Њ, 6.6Њ,
and 6.3Њ for the homologous, homolateral, and heterolateral
The age-related deterioration during homolateral coordi-
Figure 4. The standard deviation (SD) of cycle duration for the different effector combinations during in-phase and anti-phase coordination
for younger and older adults.

P300
SERRIEN ET AL.
nation is exemplified in Figure 5. Displacement time pro-
files of right arm/right leg movements and the orthogonal
plot of both displacement patterns (Lissajous figure) are
displayed for a young and older participant. When in-
phase and anti-phase movements are performed correctly
erence to move effectors rhythmically with equal tempo
(Kelso, 1995; Swinnen, Jardin, Meulenbroek, Dounskaia,
& Hofkens-Van Den Brandt, 1997). Little is known about
the extent to which these constraints change or become
more challenging across the life span due to modifications
in central or peripheral factors. The aim of this experiment
was to investigate age-related changes in the coordination
dynamics of homologous versus nonhomologous limbs
during the production of 1:1 synchronization, according to
the in-phase and anti-phase mode. The data revealed per-
formance differences between younger and older partici-
pants that depended both on limb combination and coor-
dination mode. These modifications due to aging are
hypothesized to result from a conjunction of (a) deficits in
afferent information processing for steering coordinated
behavior and (b) declines in cognitive regulation, emerg-
ing from a deterioration of inhibitory mechanisms and a
reduced optimal (attentional) monitoring of sensory feed-
back information.
(
i.e., relative phases of 0Њ or 180Њ), the Lissajous figures
result in a straight (diagonal) line configuration, oriented
to the right or left. It can be observed that the plots of the
young adult show consistent behavior during in-phase as
well as anti-phase movements. Conversely, the relative
motion plot of the older adult is more diffuse during the
in-phase mode and is highly scattered and irregular during
the anti-phase mode. In the latter case, there is no coordi-
native consistency and a transition from anti-phase to in-
phase is apparent.
DISCUSSION
Past research has shown that explicit constraints emerge
during coordinated interlimb behavior, resulting in a pref-
Figure 5. Displacement time series and relative motion plots of homolateral coordination for a young (A) and older (B) participant.

AGING AND INTERLIMB COORDINATION
P301
Age-Related Changes in Coordinated Behavior
Depend on Limb Combination
data on bimanual coordination (Greene & Williams, 1996;
Serrien, Teasdale, Bard, & Fleury, 1996). A more pro-
nounced performance regression became apparent when ex-
ecuting the anti-phase mode with a combination of the up-
per and lower limbs. Older adults experienced a great deal
of difficulty during nonhomologous anti-phase as compared
with in-phase movements. We hypothesize that this finding
can be explained by a compound effect of loosely coupled
nonhomologous effectors (as discussed previously) and dis-
similar feedback mechanisms subserving in-phase and anti-
phase patterns. In particular, Baldissera and colleagues
(1991) examined nonhomologous coordination and sug-
gested that in-phase movements require limited feedback
control, whereas anti-phase movements undergo refined
processing, relying on increased monitoring and attentional
resources.
The latter statement is supported by recent functional
imaging data. In particular, it has been demonstrated that
anti-phase movements demand more pronounced neural
processing than in-phase movements (Goerres, Samuel,
Jenkins, & Brooks, 1998; Sadato, Yonekura, Waki, Ya-
mada, & Ishii, 1997; Stephan et al., 1999). Also, the anti-
phase mode necessitates a suppression of the elementary in-
phase mode (Sadato et al., 1997). Consequently, anti-phase
coordination requires selective attention to inhibit conflict-
ing neural commands. As the capacity of the attentional sys-
tem to suppress patterns of interference and/or dominant
responses becomes deficient with age (Clark, 1996; Demp-
ster, 1992; Hasher & Zacks, 1988; West, 1996), it is reason-
able to assume that the performance of the anti-phase mode
will deteriorate as a function of age. Because of reduced in-
hibitory control, a bias toward the more basic in-phase
mode emerges. In this respect, phase transitions from anti-
phase to in-phase were regularly observed for the older
adults during nonhomologous conditions, especially when
homolateral effectors were involved. The diminished capac-
ity to repress intrinsic coordination tendencies as a function
of age was also noticed in a learning experiment in which a
90Њ out of phase pattern was to be acquired with the upper
limbs (Swinnen et al., 1998).
Weakened inhibitory mechanisms in older participants
may also contribute to impaired sustained attention (Chao &
Knight, 1997). In the present context, this suggests that cog-
nitive processing that is required to produce coordinated ac-
tions will be subject to age-related declines. Less capacity
can be directed to monitoring the trajectories of the coordi-
native task, resulting in a greater vulnerability to inefficient
behavior. The latter is likely to be more prominent for anti-
phase than in-phase movements because of the higher men-
tal effort that is required, a distinction that can be associated
with the concepts of controlled or effortful processing ver-
sus automatic processing (Hasher & Zacks, 1979; Schneider
& Shiffrin, 1977). Furthermore, Summers, Byblow, By-
south-Young, and Semjen (1998) examined the cognitive
demands during bimanual isofrequency coordination by in-
cluding a supplementary task. The authors noticed that sec-
ondary task performance did not affect in-phase movements
but resulted in a deterioration of anti-phase movements
when cycling at high frequencies. This discrepancy of cog-
nitive requirements between both coordination modes has
All participants produced the required coordination modes
more successfully with their homologous than with their
nonhomologous limbs, confirming and extending previous
findings in young adults (Serrien & Swinnen, 1997, Swin-
nen et al., 1995). This performance difference as a function
of limb combination may be related to a distinction in orga-
nizational/control processes. In particular, it has been dem-
onstrated that homologous segments form a tight synergy
characterized by a high degree of converging afferent sig-
nals, an informational input which is of primary importance
for realizing interlimb synchronization. Therefore, the capa-
bility to detect deviations from the required relative motion
pattern through continuous kinesthetic monitoring is highly
efficient during homologous conditions, securing the pres-
ervation of in-phase and anti-phase coordination. Con-
versely, nonhomologous effectors are associated with a less
stringent type of synergy for which sensory information is
less congruent. This may reduce optimal monitoring of af-
ferent information and subsequent detection of errors in the
ongoing movement pattern, affecting the quality of synchro-
nized interlimb behavior (Serrien & Swinnen, 1998; Swin-
nen et al., 1995).
Because of the fact that aging induces an overall deterio-
ration of sensory functions (Skinner et al., 1984; Stelmach
&
Sirica, 1986), it is suggested that a decline in the quality
of afferent information from the periphery and/or an in-
crease in threshold for its detection will change the avail-
able contextually related input for calibrating and steering
coordinated behavior in an optimal manner. In the present
study, age-related deficits were rather specific to nonhomol-
ogous conditions. This indicates that deficient sensory in-
formation processing has a stronger effect on loosely cou-
pled control structures for which the ability to monitor
afferent input is attenuated. In addition, it is likely that a de-
cline in the processing of afferences is associated with an
increased cognitive load for task production, that is, more
conscious control and mental effort is required for the con-
trol of movement. The latter statement is supported by data
from a deafferented patient. During dual task performance,
the patient experienced more interference than controls and
commented that combined tasks such as speaking and a
manual action demanded substantial cognitive resources
(Teasdale et al., 1994).
Complexity of the Coordination Mode:
In-Phase Versus Anti-Phase Movements
In support of previous work, the present findings indi-
cated that directional requirements determine the quality of
interlimb synchronization. In particular, in-phase (isodirec-
tional) movements were easier to execute than anti-phase
(
non-isodirectional) movements and resulted in superior
motor behavior (Kelso & Jeka, 1992; Serrien & Swinnen,
997; Swinnen et al., 1995). The intrinsic nature of in-phase
1
coordination was especially noted during homologous
movements that were produced with a similar degree of suc-
cess in both groups of participants. During homologous
anti-phase movements, an age-related deterioration in syn-
chronization capabilities was noticed, supporting earlier

P302
SERRIEN ET AL.
received support from functional imaging work. In particu-
lar, it has been shown that neural activation in the prefrontal
cortex and midbrain occurs during anti-phase patterns that
does not emerge during in-phase patterns. Sadato and col-
leagues (1997) stated that this extra activation is indicative
of additional attentional requirements, reflecting on-line
monitoring due to augmented spatial attention and spatial
working memory during anti-phase coordination. However,
Fink and colleagues (1999) claimed that this prefrontal acti-
vation can be specifically related to sensory(motor) integra-
tion. The authors suggested that frontal monitoring serves
an executive function, allowing active supervision of the
task. The observation that the prefrontal cortex appears to
be more sensitive to age-related deterioration than other ar-
eas of the cortex (Mielke et al., 1998; Raz et al., 1997) is
likely to contribute to cognitive processing deficits in older
adults. As stated previously, extra attentional resources are
probably required because of insufficient sensory regula-
tion, suggesting that an impairment in cognitive monitoring
as a function of age may play a determining factor in the
quality of multilimb coordination. This is in line with earlier
data that have demonstrated that cognitive declines due to
age may introduce significant consequences for motor be-
havior (Kluger et al., 1997).
The coordinative difficulties that were observed during
two-limb motion patterns were supported by the cycle dura-
tion data. Whereas movements of homologous limbs and
nonhomologous limbs according to the in-phase mode were
produced in harmony with the tempo of the metronome,
movements of nonhomologous limbs in the anti-phase mode
were performed with a high degree of temporal variability.
Increased kinematic variability due to aging has been ob-
served repeatedly, a finding that can be associated with age-
related neuromuscular changes (Cooke, Brown, & Cunning-
ham, 1989; Seidler & Stelmach, 1995; Spirduso, 1995). In
addition, older as compared with younger participants pro-
duced large delays from the target tempo provided by the
metronome. It is hypothesized that the older persons slowed
their motion patterns as an adaptive strategy to cope more
successfully with the task requirements. Behavioral slowing
may also be related to the fact that the older participants de-
pended more on visual feedback to guide their movement
patterns because of a reduced reliance on proprioceptive in-
formation. Therefore, the temporal constraints associated
with the visual feedback’s detection or adjustment processes
might necessitate a reduction in movement speed.
ment of Neurology, Inselspital, BHH M-133, CH-3010 Berne, Switzerland.
E-mail: debbie.serrien@insel.ch
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Acknowl edgment s
Address correspondence to Deborah Serrien, who is now at the Depart-
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Received April 5, 1999
Accepted November 24, 1999
Decision Editor: Toni C. Antonucci, PhD