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Interlimb Coordination From A Psychological Perspective: JPFSM: Review Article
Interlimb Coordination From A Psychological Perspective: JPFSM: Review Article
DOI: 10.7600/jpfsm.5.349
Abstract During coordination of the movement of two limbs, the movements often interfere
with each other, i.e., interlimb coordination is constrained. Many movement-related param-
eters such as movement direction, movement frequency, the coupling of limbs, neural network
among limbs, and muscle homology are considered constraints of interlimb coordination, and
they are roughly consolidated into two constraints, a neuromuscular constraint, and a percep-
tual-cognitive constraint. Interlimb coordination is considered to be governed by a coalition of
neuromuscular and perceptual-cognitive constraints. On the other hand, spontaneous interlimb
coordination is considered purely perceptual in nature. In this review, we focused on an influ-
ential study on interlimb coordination published in Nature by Mechsner et al. (2001), which
supported the latter psychological approach. Thorough verification of the paper with reference
to related studies revealed that no studies have yet proposed decisive contrary evidence against
the psychological approach. Rather, investigation of interlimb coordination with perceptual-
cognitive perspective has uncovered new findings. As a next psychological approach, the
proposal of a unified and predictive explanation for movements is required. In addition, neural
mechanisms that connect perceptual-cognitive representation to an appropriate motor com-
mand, if any, should be addressed.
Keywords : interlimb coordination, psychology, sparse coding, salience
1B and 1D)] are defined as 0˚ and 180˚, respectively. The ture”44). Because their claims seemed to be too extreme
movements with these relative phases can be performed (e.g., purely perceptual, no need of translation between a
stably without a lot of practice compared to cases of other motor and a perceptual representation)11,44-47), many subse-
relative phases such as 90˚37,38). An anti-phase movement quent publications tried to propose contrary evidence (e.g.,
unintentionally changes to an in-phase movement with a special issue in J Mot Behav48-61)). Surprisingly, although
increasing movement frequency, and the opposite phase 15 years have passed and many papers on interlimb co-
transition from an anti-phase to an in-phase movement ordination have been published since the Mechsner et
rarely occurs. Moreover, the critical fluctuation39) and al. article in Nature, there still has been no consensus
critical slowing down40), one of the key features for self- whether interlimb coordination is governed by a coalition
organization, are observed in association with the phase of neuromuscular and perceptual-cognitive constraints or
transition. As shown above, it has been experimentally if the control principle of interlimb coordination is purely
and theoretically clarified that interlimb coordination is perceptual. The present review, therefore, tries to verify
constrained by spatiotemporal parameters of movement41). Mechsner’s claims and the arguments against them along
Possible constraints of interlimb coordination can be with a description of the three experiments in Mechsner’s
roughly consolidated into two constraints2,41-43): “a neu- article in Nature44), and attempts to predict the next psy-
romuscular constraint” and “a perceptual-cognitive con- chological approach to interlimb coordination.
straint”. Most researchers originally thought that interlimb
coordination was governed by a coalition of neuromus-
Experiment 1: Index finger abduction-adduction in mir-
cular and perceptual-cognitive constraints. However, in
ror/parallel directions with different forearm postures
2001, Mechsner et al. published a revolutionary article
in Nature, which claimed that “(t)he symmetry tendency Subjects performed cyclical abduction and adduction
in bimanual movements is independent of muscular and of both index fingers in the horizontal plane either in a
motoric constraints and is thus purely perceptual in na- mirror (Fig. 1A) or in a parallel (Fig. 1B) direction. The
Figure 1
A B
C D
time time
posture of the forearm was maintained either in a pro- is perceptually conceived as the most salient or accentu-
nated (i.e., palm down) or in a supinated (i.e., palm up) ated subevent (c.f. anchoring75-78)), the sequences of the
position. When the forearm position is congruent for both most salient subevents prefer to go together in concur-
limbs, co-contraction of the homologous muscles will re- rent two event streams. The results of the sensorimotor
sult in a mirror directional movement. When the forearm coordination between repetitive sound (i.e., metronome)
position is incongruent for both limbs (e.g., the right limb and cyclical extension-flexion of the index finger of one
in the pronated position and the left limb in the supinated hand showed that flexion on the beat was more stable
position), co-contraction of the homologous muscles will compared to extension on the beat, and a less stable pat-
result in a parallel directional movement. Hence, it is pos- tern of extension on the beat abruptly changed to a more
sible to investigate whether interlimb coordination has a stable pattern of flexion on the beat2,79-82). Since repetitive
tendency toward co-activation of the homologous muscles sound is conceived as a more salient event compared to
or toward perceptual, spatial symmetry. pause between sounds, the results of the sensorimotor
The results were very clear that a mirror directional coordination (i.e., stable pattern of flexion on the beat)
movement was more stable compared to a parallel direc- can be explained by the relative salient hypothesis with
tional movement independent of the forearm posture, and an assumption that flexion is the most salient subevent in
that an involuntary phase transition from a parallel to a a stream of extension-flexion. Similarly, coordination of
mirror directional movement occurred at high movement extension-flexion of both index fingers can be explained
frequency. Mechsner et al. concluded that “the symme- by the relative salience hypothesis as follows: flexion, the
try tendency in the bimanual finger oscillation model is most salient subevent, of the right and left fingers prefer
a tendency towards perceptual, spatial symmetry, rather to go together. Moreover, the following studies indirectly
than towards co-activation of homologous muscles”44). In support the relative salience hypothesis. In the case that
order to clarify whether interlimb or interjoint coordina- the salience of finger extension is greater than that of fin-
tion is constrained by co-activation of the homologous ger flexion due to haptic sensation coupled with extension
(or iso-functional) muscles or by perceptual, spatial sym- (i.e., tapping by extension), extension on the beat became
metry, several experiments, in which subjects performed more stable than flexion on the beat, and the phase tran-
coordinated movements with two different postures, sition from extension on the beat to flexion on the beat
were conducted utilizing extension-flexion of both index occurred81). When introducing the auditory and haptic
fingers62-64), extension-flexion of both wrists65), radial- stimuli coupled with finger flexion for each side, the anti-
ulnar flexion of both wrists66,67), extension-flexion of the phase (e.g., extending the right finger while flexing the
ipsilateral wrist and elbow68,69), extension-flexion of the left finger) became stable83) because the coordination of
ipsilateral wrist and ankle10,70-72), pronation-supination of both fingers could be conceived as a dual task paradigm
the forearm and internal-external rotation of the ipsilat- of stable sensorimotor coordination of each finger. The in-
eral leg73), and extension-flexion of the ipsilateral finger phase of extension-flexion of both wrists was conceived
and toe74). Some studies showed similar results as that as a repetition of a single unit (i.e., a synchronized subev-
of experiment 1 that interlimb coordination only had a ent of both wrists), whereas the anti-phase was conceived
tendency toward perceptual, spatial symmetry (i.e., mir- as two units (i.e., the alternate occurrence of subevent of
ror direction in the horizontal plane or the same direction each wrist)84). Double metronome for one extension-flex-
in the sagittal plane)10,68,69,71,72). On the other hand, there ion cycle of the index finger results in flexion on the beat
are studies showing that interlimb coordination was gov- for each finger even during the anti-phase, and hence, the
erned by both neuromuscular and perceptual-cognitive anti-phase became more stable with the help of a double
constraints2,62,65-67,70,73,74) or by only neuromuscular con- metronome compared to a single metronome85).
straint63,64). Although the relative-salience hypothesis seems to be
Based on the results that interlimb coordination had plausible, it is criticized as a post hoc rationalization49) be-
a tendency toward co-activation of the homologous cause it may be able to produce an ad hoc psychological
muscles63,64), and not toward perceptual, spatial symmetry, explanation for any coordination phenomenon. For exam-
which was completely opposite to the results of experi- ple, if the results of experiment 1 had shown a tendency
ment 1, it was pointed out that the conclusion obtained by toward co-activation of abductors, it could have been
the psychological approach to interlimb coordination was explained as the coordination of index finger abduction-
incorrect56,61,63). As a rebuttal to this, Mechsner claimed adduction having a tendency toward synchronization of
that the coordination of extension-flexion of both index abduction, because abduction was more salient compared
fingers, used in those studies, could be explained well to adduction for some psychological or neuromuscular
by the relative-salience hypothesis, one of the perceptual reasons. To sum up, experiment 1 investigated whether
grouping principles45,46). In the relative-salience hypothe- bimanual coordination could be described by a psycho-
sis, 1) cyclical joint movements such as flexion-extension logical approach, not whether bimanual coordination was
of the index finger tend to be conceived as a stream of a governed by a neuromuscular constraint.
unified event, and 2) if a single point in a unified event
352 Figure 2 JPFSM : Muraoka T, et al.
A B
C D
muscles. Because there might be a hierarchy in the con- stable. In other words, neural crosstalk is not suitable as
trollability among fingers in the order of I > M > R91-93), the main constraint for interlimb coordination, which is
Riek and Woolley proposed the hypothesis that “the more consistent with the results of experiments 1 and 2.
controllable finger in each pair are synchronized”. On the
other hand, Mechsner explained the two-finger tapping of
Experiment 3: Bimanual cycling at a non-harmonic
both hands as a tendency toward perceptual, spatial sym-
frequency ratio under symmetric visual feedback
metry in a hand-centered reference frame11). In the hand-
centered reference frame, sequence tapping in the order Subjects were instructed to circle two visible flags by
of I and M has the same directional characteristic as se- way of two cranks without visual information of the mov-
quence tapping in the order of M and R irrespective of the ing arms. The flags moved in accordance with the move-
forearm posture. Indeed, a hand-centered reference frame ment of the cranks, but each crank had different gear ratios
is used in the premotor and posterior parietal cortices for so that a 4:3 frequency ratio in the cranks resulted in an
the representation of the space surrounding the hands iso-frequency in the flags. Subjects practiced the in-phase
for grasping94-97). The results obtained using bimanual (i.e., flags revolve in a counter direction at the same speed,
4-finger tapping98) could be explained both by a tendency both flags starting at the 12 o’clock position) and anti-
toward symmetry in the hand-centered reference frame phase (i.e., flags revolve in a counter direction at the same
and by the synchronization of a more controllable finger. speed, one flag starting at the 12 o’clock position and the
Although it is unknown which explanation is appropriate, other flag starting at the 6 o’clock position) flag coordina-
the results of experiment 2 and some above-mentioned tion for 15 to 20 min. If the bimanual coordination tends
studies showed no tendency toward co-activation of the toward perceptual, spatial symmetry, the in-phase in the
homologous muscles in bimanual finger tapping. flags should be more stable compared to the anti-phase in
Neural crosstalk is considered a possible neuromuscu- the flags, and the phase transition from the anti-phase to
lar constraint for movements41,42). It is well known that the in-phase in the flags should occur irrespective of the
the activity (contraction and relaxation of muscles) of activation timing of the muscles of both limbs.
one limb affects not only the corticospinal (or motoneu- The results showed that the in-phase in the flags was
ron) excitability of the muscles employed in the activity, more stable compared to the anti-phase in the flags, and
but also the excitability of the resting muscles of other that a phase transition from the anti-phase to the in-phase
limbs99-109). This kind of influence from the activity of one in the flags occurred. Almost the same coordination phe-
limb to the resting muscles in other limbs is most pro- nomenon was observed when the left flag was circled by
nounced between the homologous muscles110), but often an experimenter and the right flag was circled by a sub-
spread to the non-homologous muscles111,112). This kind of ject. Since the bimanual movements with a non-harmonic
influence is highly task-dependent104). The influence of a frequency relationship (i.e., 4:3), which is considered
cyclical movement on other resting limbs in terms of neu- to be almost impossible to perform for naïve subjects116)
ral crosstalk enhances the preferred coordination pattern could be performed under the visual feedback of flags
when moving both limbs cyclically99,100,113-115), and it is with the simplest frequency relationship (i.e., 1:1), Mech-
flexibly tuned in accordance with a change in posture99). sner concluded that the “symmetry and antiphase in the
In addition, it was shown that the extent of modulation of flags can be achieved in visual space even though there
corticospinal excitability in a resting wrist muscle, which is no specific translation of characteristic body activity
enhances the preferred coordination pattern of the wrist patterns into these characteristic perceptual patterns”44).
and ankle (i.e, in-phase; same directional movement), was He regarded the course of practice to circle the cranks for
correlated with the time to transition from the anti-phase the in- and anti-phase in the flags as “figuring out and sta-
(i.e., opposite directional movement) to the in-phase102). bilizing a more and more suitable and economic way of
At first glance, this correlation between the neural cross- representing the practiced movements rather than estab-
talk and performance of interlimb coordination proved lishing body-defined movement patterns by way of rep-
that interlimb coordination was mainly governed by the etition”46), which suggests that the Body-World is sparsely
neuromuscular constraint, which is contrary to the results coded (the sparse coding principle, the economical coding
of experiments 1 and 2. It should be noticed here that the principle)45,46). The sparse coding principle means that
anti-phase, as well as in-phase, is a stable coordination “many movement features that may be perceptible in
pattern in a variety of phase relationships between 0˚ and principle are neither addressed nor perceived”45). Similar
180˚. In addition, Fig. 6 of the study by McIntyre-Robin- to the results of experiment 3, several studies showed
son and Byblow102) showed that the neural crosstalk that that difficult bimanual movements with a non-harmonic
enhanced anti-phase coordination was seen in four out of frequency relationship could be performed easily with the
17 subjects, but phase transition from the anti-phase to help of visual feedback that integrates kinematic informa-
the in-phase was seen in “all” subjects. Therefore, neural tion of both hands (relative angle as Lissajous curve117),
crosstalk may be able to explain the stable in-phase coor- relative velocity as a line118,119)). These studies used bi-
dination, but not why the anti-phase coordination is also manual circling produced by a relatively complicated
354 JPFSM : Muraoka T, et al.
muscle activation pattern compared to a single joint recip- clearly stated that “evidence for body-related control can-
rocating movement (e.g., extension-flexion produced by not be taken as evidence against a perceptual-cognitive
alternate activation of the extensors and flexors), which approach”45). Therefore, it seems quite difficult to propose
might hide the possible effect of co-activation of the ho- contrary evidence against Mechsner’s claim, which may
mologous muscles on bimanual coordination. However, be a serious issue from the viewpoint of falsifiability pro-
even when using a single joint reciprocating movement, posed by Karl Popper.
a visual feedback that integrates kinematic information It is important to note that Mechsner’s study published
of both arms enabled naïve subjects to perform a diffi- in Nature was not conducted in order to determine whether
cult relative phase other than 0˚ and 180˚ (e.g., 90˚) with movements were founded upon a coalition of neuromus-
ease120-126), though non-integrated visual feedback (i.e., two cular and perceptual-cognitive constraints. It is wrong to
flags move symmetrically or iso-directionally during anti- consider that his article proposed a dichotomy between
phase) could not contribute to, or even destabilized coor- perceptual-cognitive constraint and neuromuscular con-
dination18,127,128). Therefore, it is plausible that movements straint. He considered that the perceptual-cognitive and
rely on the sparse coding principle. Some studies showed neuromuscular accounts of movements represent different
that a bimanual discrete movement was constrained in levels of explanation and that a psychological approach
response to an identified movement’s goal43,129-131), which originally includes (takes into account) neuromuscular
is consistent with the sparse coding principle. Thus, it can factors as tools to execute movements. The relevance of
be said that the interlimb coordination phenomenon origi- neuromuscular factors would not contradict a perceptual-
nates at the level of how movement is perceptually and cognitive approach because perception and cognition
cognitively conceived in its environment, and not at the have been evolving to cope with neuromuscular factors.
level of how movement is described in terms of kinetics This means that perception and cognition interact with
and kinematics (c.f., internal and external focus in motor the economy and efficiency at the neuromuscular level90)
learning132,133)). (e.g., efficient neural control using co-activation of the ho-
mologous muscles is coupled with the feeling of ease and
comfort). His article tried to clarify whether constraints of
Mechsner’s psychological approach
movements were perceived and considered on a psycho-
Based on thorough verification of experiments 1, 2 logical level of perception, cognition, emotion, and so on.
and 3, it may be safe to say that interlimb coordination Therefore, it is a wrongly posed problem whether or not
is, at least partly, constrained at the perceptual-cognitive movements are founded upon a coalition of neuromuscular
level. This is also supported by some studies that showed and perceptual-cognitive constraints. On the other hand,
the characteristics of interlimb coordination (e.g., two a psychological approach in the future should propose a
stable modes of the in-phase and anti-phase, more stable unified and predictive explanation for movements instead
in-phase compared to anti-phase) appearing even when of an ad hoc and post hoc explanation. “The issue of how
the neuromuscular factors were partly or completely re- and why appropriate motor patterns directly correspond to
moved by means of investigating bimanual coordination perceptual-cognitive representations”54) has to be resolved.
of patients without somatosensory feedback bimanually
or unimanually134), motor imagery of bimanual coordina-
Conclusion
tion135,136), coordination between active limb movement
and passively moving limb137-140), coordination between In this review, we focused on an influential study on
active limb movement and phantom limb141), interlimb co- interlimb coordination published by Mechsner et al. Al-
ordination between persons74,142-149), coordination between though not many researchers agree with their claim that
active limb movement and visual stimulus142,147,150-152), and the control principle of interlimb coordination is purely
perception of interstimulus coordination153-155). perceptual, several studies have been conducted to inves-
The unsettled problem is whether the control principle tigate interlimb coordination from a perceptual-cognitive
of interlimb coordination is purely perceptual. Because perspective. Thus, it can be said that the psychological
the connection between movements and perception- approach has achieved certain success in the field of mo-
cognition is very tight, it seems impossible to remove tor control research. In future studies, a psychological ap-
the perceptual-cognitive factor from movements as proach needs to propose a unified and predictive explana-
the above-mentioned studies did. Mechsner stated that tion for movements. In addition, neural mechanisms that
“(m)any bodily movement characteristics are perceptible, connect perceptual-cognitive representation to appropriate
in the first place, by vision as well as by proprioception, motor command, if any, should be addressed.
and, in part, by way of other sensory modalities such as
audition. Thus, by definition, they are open to inclusion
Conflict of Interests
in a perceptual-cognitive control scheme”45). That is, any
neuromuscular constraint can be replaced by an ad hoc The authors declare that there is no conflict of interests
perceptual-cognitive constraint. In addition, Mechsner regarding the publication of this article.
JPFSM : Interlimb coordination from a psychological perspective 355
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