Interactions between interlimb and intralimb coordination during the performance of bimanual multijoint movements

The simultaneous performance of movements involving different effectors gives rise to neural and biomechanical interactions between and within limbs. The present study addressed the role of interlimb and intralimb constraints during the control of bimanual multijoint movements. Thirteen participants performed eight tasks involving the bilateral elbows and wrists under different coordination conditions. With respect to interlimb coordination, coordination patterns referred to the in-phase and anti-phase coordination modes, involving the simultaneous timing of homologous versus non-homologous muscles, respectively. With respect to inter-segmental (intralimb) coordination, the isodirectional mode referred to simultaneous flexions and extensions in the ipsilateral wrist and elbow joints, whereas the non-isodirectional mode involved simultaneous flexion in one joint together with extension in the other joint, or vice versa. The analysis of the data focused upon measures of relative phasing between proximal and distal joints within a limb as well as between the homologous joints of both limbs. With respect to interlimb coordination, findings revealed that adoption of the in-phase mode resulted in a higher quality of interlimb coordination than the anti-phase mode. However, the mode adopted in the distal joints had a larger impact on the quality of interlimb coordination than the mode adopted in the proximal joints. More specifically, in-phase coordination of the distal joints had a positive, and anti-phase coordination a negative, influence on the global coordinative behavior of the system. Minor effects of intralimb coordination modes on interlimb coordination were observed. With respect to intralimb coordination between the ipsilateral elbow and wrist, the isodirectional mode was performed with higher stability than the non-isodirectional mode. The mode of interlimb coordination also affected the quality of intralimb coordination, such that generating anti-phase coordination patterns in the distal joints had a negative influence on the accuracy and stability of intralimb coordination. Taken together, the present findings suggest a hierarchical structure whereby interlimb coordination constraints have a stronger impact on the global coordinative behavior of the system than intralimb coordination constraints. Moreover, the global coordinative state of the system is more affected by the coordination between the distal than between the proximal joints. Overall, the findings suggest that the mirror-image symmetry constraint has a powerful influence on bimanual multijoint coordination.     

The identification of coordination constraints across planes of motion

Two dominant coordination constraints have been identified during isofrequency conditions in previous work: the egocentric constraint, i.e., simultaneous activation of homologous muscle groups, and the allocentric constraint, i.e., moving the segments in the same direction in extrinsic space. To verify their generalization, bimanual drawing movements were performed in different planes of motion (transverse, frontal, sagittal, frontal-transverse) according to the in-phase and anti-phase mode along the X- and Y-axes. Convergent findings were obtained across the transverse, frontal, and frontal-transverse planes. The in-phase mode along both axes was performed most accurately/consistently, whereas the anti-phase mode resulted in a deterioration of the coordination pattern and this effect was most pronounced when the latter mode was introduced with respect to both dimensions. For sagittal plane motions, the in-phase mode was again superior but the second most optimal configuration was the anti-phase mode along both axes. This finding was hypothesized to result from the familiarity with the pattern since it resembles cycling behavior. It illustrates how cognitive mapping is superimposed onto the dynamics of interlimb coordination. Overall, these results support the presence of both the egocentric and allocentric constraint during bimanual movement production. Received: 21 August 1998 / Accepted: 12 February 1999     

Spatial constraints in bimanual coordination: influences of effector orientation

Two experiments are reported that examined the influence of spatial orientation of the upper limbs in bimanual coordination. In both experiments, the upper limbs were oriented in either parallel, orthogonal, or obtuse spatial configurations and participants were asked to move their limbs continuously in temporal (1:1) synchrony, prepared in either in-phase or anti-phase modes of coordination. Bimanual coordination trials in Experiment 1 were paced by a metronome at one of four frequencies (1.0, 1.5, 2.0 or 2.5 Hz). Measures of relative phase accuracy and stability both revealed that, as metronome frequency increased, in-phase coordination dominated for the parallel spatial orientation, anti-phase coordination dominated for the orthogonal spatial orientation, and neither pattern dominated for the obtuse spatial orientations. In Experiment 2, an intentional switch method replicated and extended these influences of spatial orientation. The time to voluntarily switch from an anti-phase pattern to an in-phase pattern was faster than an in-phase to anti-phase switch (confirming support for the dominance of the in-phase pattern), but this was true only for the parallel spatial orientation. The reverse was true for the orthogonal spatial orientation (i.e., faster from in-phase to anti-phase), and no difference in switch times was observed for an obtuse spatial orientation. These findings support and extend previous research regarding the influence of spatial orientation in bimanual coordination and may be attributed to the role of, and potential interactions between, egocentric, allocentric, and mechanical constraints during action.     

Coordinative and limb-specific control of bimanual movements in patients with Parkinson's disease and cerebellar degeneration

The present study examined the effects of basal ganglia and cerebellar pathology on bimanual coordination using patients with Parkinson's disease (PD) and cerebellar dysfunction (CD). Twenty patients with idiopathic PD (10 untreated early and 10 advanced PD), 10 patients with cerebellar degeneration, and 11 normal subjects were instructed to perform in-phase and anti-phase bimanual coordination movements. The results indicated that while the quality of coordinated bimanual movements in untreated early PD and CD patients was not significantly different from that of normal controls, advanced PD patients exhibited reduced synchronized coordination during the faster anti-phase mode. This suggests that the observed bimanual coordination abnormalities in PD are not an early sign of the pathophysiology of the disease, and cerebellar degeneration may have minimal consequences on synchronized coordination between the limbs. In terms of the parameterization of individual limb movements, CD patients showed a tendency for hypermetric impairments with more irregular movements, while PD patients exhibited relatively slower limb movements and lower amplitudes than normal controls. Overall, the current data provide evidence of the specific functions of different neural structures involved in the pathological process of PD and CD on bimanual coordination.     

Unraveling interlimb interactions underlying bimanual coordination

Three sources of interlimb interactions have been postulated to underlie the stability characteristics of bimanual coordination but have never been evaluated in conjunction: integrated timing of feedforward control signals, phase entrainment by contralateral afference, and timing corrections based on the perceived error of relative phase. In this study, the relative contributions of these interactions were discerned through systematic comparisons of five tasks involving rhythmic flexion-extension movements about the wrist, performed bimanually (in-phase and antiphase coordination) or unimanually with or without comparable passive movements of the contralateral hand. The main findings were the following. 1) Contralateral passive movements during unimanual active movements induced phase entrainment to interlimb phasing of either 0 degrees (in-phase) or 180 degrees (antiphase). 2) Entrainment strength increased with the passive movements' amplitude, but was similar for in-phase and antiphase movements. 3) Coordination of unimanual active movements with passive movements of the contralateral hand (kinesthetic tracking) was characterized by similar bilateral EMG activity as observed in active bimanual coordination. 4) During kinesthetic tracking the timing of the movements of the active hand was modulated by afference-based error corrections, which were more pronounced during in-phase coordination. 5) Indications of in-phase coordination being more stable than antiphase coordination were most prominent during active bimanual coordination and marginal during kinesthetic tracking. Together the results indicated that phase entrainment by contralateral afference contributed equally to the stability of in-phase and antiphase coordination, and that differential stability of these patterns depended predominantly on integrated timing of feedforward signals, with only a minor role for afference-based error corrections.     

Effects of interlimb and intralimb constraints on bimanual shoulder-elbow and shoulder-wrist coordination patterns

The present study addressed the interactions between interlimb and intralimb constraints during the control of bimanual multi-joint movements. Participants performed eight coordination tasks involving bilateral shoulder-elbow (expt I) and shoulder-wrist (expt II) movements. Three principal findings were obtained. First, the principle of muscle homology (in-phase coordination), giving rise to mirror symmetrical movements with respect to the midsagittal plane, had a powerful influence on the quality of interlimb coordination. In both experiments, the accuracy and stability of inter- and/or intralimb coordination deteriorated as soon as the antiphase mode was introduced in one or both joint pairs. However, the mutual influences between bilateral distal and proximal joint pairs varied across coordination tasks and effectors. Second, the impact of intralimb coordination modes on the quality of intralimb coordination was inconsistent between adjacent (expt I) and non-adjacent joint (expt II) combinations. Third, the mode of interlimb coordination affected the quality of intralimb coordination, whereas strong support for the converse effect was not obtained. Taken together, these observations point to a hierarchical control structure whereby interlimb coordination constraints have a stronger impact on the global coordination of the system than intralimb constraints, whose impact is substantially dependent on effector and task. The finding that intralimb coordination is subordinate to interlimb coordination during the production of bimanual multi-joint coordination patterns indicates that symmetry is a major organizational principle in the neural control of complex movement.     

Using scanning trials to assess intrinsic coordination dynamics

Bimanual 1:1 coordination patterns other than in-phase (0°) and anti-phase (180°) have proven difficult to perform even with extended practice. The difficulty has been attributed to phase attraction that draws the coordination between the limbs towards the bimanual patterns of in-phase and anti-phase and variability associated with the activation of non-homologous muscles via crossed and uncrossed cortical pathways. We found participants could very effectively produce a large range of supposedly unstable coordination patterns (between 0° and 180° in 30° increments) after only 3 min of practice when integrated feedback (Lissajous plots) was provided and other perceptual and attentional distractions were minimized. These findings clearly indicate that the perception-action system is fully capable of producing a wide range of bimanual coordination patterns and that the reason for the failure to produce these patterns in previous experiments reside in the perceptual information and attentional requirements typically found in experimental testing environments.     

Coordination of coupled hand and foot movements during childhood

To acquire further insight into the neural mechanisms governing the association of voluntary oscillations of ipsilateral hand and foot we investigated when and how coordination of such coupling develops in children 7-10 years old. Sixty-six children were asked to rhythmically oscillate their right hand and foot, paired in-phase or anti-phase (i.e. rotating in the same or in the opposite angular direction). Angular displacement was monitored by a potentiometric technique, and EMGs from extensor carpi radialis (ECR) and tibialis anterior (TA) were recorded. All subjects were able to couple in-phase oscillations, but 13 of them failed to perform the anti-phase task. Maximal frequency of oscillation was found to be positively correlated with age. Phase-relations between hand and foot oscillations and between onsets of the EMG activity in hand and foot movers were measured in 37 of the children. During in-phase coupling limb oscillations were kept in an almost perfect synchrony by three different modalities of muscle recruitment. Ten of the youngest children activated TA before ECR, while 13 of the oldest subjects activated ECR before TA, as do adults. The remaining 14 children (7-8 years old) activated the two muscles almost synchronously. During anti-phase coupling, most of the younger children (20) showed a strict phase-opposition between both EMG onsets and movements. The remaining 10 (9-10 years old) activated the ECR first. The hand frequency-response (i.e. the phase-relation between the onset of the EMG and the related movement) showed age-related changes, corresponding to the behaviour of a mass-spring model (with lumped parameters) decreasing its resonant frequency. Instead, the foot frequency-response remained unchanged. The age-related modifications of the hand frequency-response adequately explain the changes of the interlimb relations described above. These results show that central structures controlling hand and foot coupling are still immature before 10 years of age and reinforce the view that in-phase and anti-phase coupling require separate neural controls.     

Cerebral midline structures in bimanual coordination

In six healthy right-handed volunteers, we compared the cerebral activation pattern related to unimanual right- and left-hand movements and to bimanual in-phase and anti-phase movements using functional magnetic resonance imaging (fMRI). Internally paced unimanual finger-to-thumb opposition movements led to a strong contralateral activation of primary sensorimotor areas in all six subjects. Midline activity was lateralized to the left side during right-hand movements, but to both sides during left-hand movements. Activity patterns of bimanual in-phase movements resembled the combined activity patterns of the two unimanual conditions: right and left hemispheric activations of the primary sensorimotor cortices and predominantly left-sided medial frontal activity. In contrast, during anti-phase movements, we observed a clear increase in activity, in both right and left frontal midline areas and in right hemispheric, mainly dorsolateral premotor areas compared to in-phase movements. These results indicate that frontal midline activity is not specific for bimanual movements per se. It can already be involved during simple unimanual movements but becomes progressively more involved during more complex aspects of movement control. Received: 20 September 1998 / Accepted: 24 February 1999     

Characteristics of instructed and uninstructed interpersonal coordination while walking side-by-side

We examined how people synchronize their leg movements while walking side-by-side on a treadmill. Walker pairs were either instructed to synchronize their steps in in-phase or in antiphase or received no coordination instructions. Frequency and phase analysis revealed that instructed in-phase and antiphase coordination were equally stable and independent of walking speed and the difference in individually preferred stride frequencies. Without instruction we found episodes of frequency locking in three pairs and episodes of phase locking in four pairs, albeit not always at (or near) 0 degrees or 180 degrees. Again, we found no difference in the stability of in-phase and antiphase coordination and no systematic effects of walking speed and the difference in individually preferred stride frequencies. These results suggest that the Haken-Kelso-Bunz model for rhythmic interlimb coordination does not apply to interpersonal coordination during gait in a straightforward manner. When the typically involved parameter constraints are relaxed, however, this model may largely account for the observed dynamical characteristics.     

Proprioceptive regulation of interlimb behavior: interference between passive movement and active coordination dynamics

The coordination of homolateral effectors (right arm/right leg) according to the in-phase or anti-phase mode was perturbed through passive movement of a third segment (left arm or left leg) imposed by the experimenter. The manipulated parameters of the passive segment were frequency and amplitude along with their degree of scaling. Results showed that passive movement degraded anti-phase patterns more than in-phase patterns. Furthermore, the anti-phase mode deteriorated profoundly during frequency manipulation, but scaling did not induce additional effects, whereas a linear association was observed between anti-phase deterioration and amplitude manipulation. Together, these data indicate that passive movement disturbed the coordination dynamics of an actively performed task. The fact that interference depended on the manipulated parameter suggests a distinction in the degree of intrusiveness of the irrelevant afferent information induced by the passive limb. It is concluded that sensory discrimination between irrelevant and relevant input is critical in performing a coordinated task adequately under perturbed conditions.     

Relative phase destabilization during interlimb coordination: the disruptive role of kinesthetic afferences induced by passive movement

The disruption of three patterns of two-limb coordination, involving cyclical flexion-extension movements performed in the same or in different directions, was investigated through application of passive movement to a third limb by the experimenter. The three patterns referred to the homologous, homolateral, and heterolateral (diagonal) limb combinations which were performed in the sagittal plane. The passive movement involved a spatiotemporal trajectory that differed from the movements controlled actively. Even though subjects were instructed to completely ignore the passive limb movement, the findings of experiment 1 demonstrated a moderate to severe destabilization of the two-limb patterns, as revealed by analyses of power spectra, relative phase, cycle duration, and amplitude. This disruption was more pronounced in the homolateral and heterolateral than in the homologous effector combinations, suggesting stronger coupling between homologous than nonhomologous limb pairs. Moreover, passive mobilization affected antiphase (nonisodirectional) movements more than inphase (isodirectional) movements, pointing to the differential stability of these patterns. Experiment 2 focused on homolateral coordination and demonstrated that withdrawal of visual information did not alter the effects induced by passive movement. It was therefore hypothesized that the generation of extra kinesthetic afferences through passive limb motion was primarily responsible for the detriment in interlimb coordination, possibly conflicting with the sensory information accompanying active movement production. In addition, it was demonstrated that the active limbs were more affected by their homologous passive counterpart than by their non-homologous counterpart, favoring the notion of specific interference. The findings are discussed in view of the potential role of kinesthetic afferences in human interlimb coordination, more specifically the preservance of relative phasing through a kinesthetic feedback loop.     

Error correction in bimanual coordination benefits from bilateral muscle activity: evidence from kinesthetic tracking

Although previous studies indicated that the stability properties of interlimb coordination largely result from the integrated timing of efferent signals to both limbs, they also depend on afference-based interactions. In the present study, we examined contributions of afference-based error corrections to rhythmic bimanual coordination using a kinesthetic tracking task. Furthermore, since we found in previous research that subjects activated their muscles in the tracked (motor-driven) arm, we examined the functional significance of this activation to gain more insight into the processes underlying this phenomenon. To these aims, twelve subjects coordinated active movements of the right hand with motor-driven oscillatory movements of the left hand in two coordinative patterns: in-phase (relative phase 0°) and antiphase (relative phase 180°). They were either instructed to activate the muscles in the motor-driven arm as if moving along with the motor (active condition), or to keep these muscles as relaxed as possible (relaxed condition). We found that error corrections were more effective in in-phase than in antiphase coordination, resulting in more adequate adjustments of cycle durations to compensate for timing errors detected at the start of each cycle. In addition, error corrections were generally more pronounced in the active than in the relaxed condition. This activity-related difference was attributed to the associated bilateral neural control signals (as estimated using electromyography), which provided an additional reference (in terms of expected sensory consequences) for afference-based error corrections. An intimate relation was revealed between the (integrated) motor commands to both limbs and the processing of afferent feedback.

The behavioural and electrophysiological effects of visual task difficulty and bimanual coordination mode during dual-task performance

The difficulty of a visual three stimulus and a bimanual coordination task was manipulated by varying discrimination difficulty (easy, hard) and coordination mode (in-phase, anti-phase) respectively. Electroencephalographic activity was recorded from 32 sites whilst participants (n = 16) completed four dual-task conditions in counterbalanced order. Longer reaction time and lower accuracy were found for the hard relative to the easy visual task and, for the hard visual task, accuracy was lower under anti-phase relative to in-phase conditions. Amplitude and latency of event-related potential components P3a and P3b were recorded and measured. There was a reduction in P3b amplitude and increase in P3a amplitude for the hard visual task overall and a further reduction in frontal P3b amplitude under the more demanding anti-phase condition. For the easy visual task, however, P3b and P3a amplitude were greater under the anti-phase relative to in-phase coordination condition at left hemisphere frontal sites. These findings suggest that the attentional cost of stabilising anti-phase bimanual coordination is largely associated with top-down automatic processes subserved by the frontal attentional network.     

Effects of plantar flexor muscle fatigue induced by electromyostimulation on postural coordination

The aim of the present study was to investigate the influence of a modification of an intrinsic capacity (plantar flexor strength) on the implementation of in-phase and anti-phase mode of coordination. Analysis of hip and ankle relative phases during fore-aft tracking task was done before and after an electromyostimulation fatigue protocol on the soleus muscles. Results showed participants used exclusively in-phase and anti-phase modes of coordination, with a sudden switch from one to the other with target frequency increase. Regarding tracking tasks, fatigue induces a decrease of performance for lower frequencies, and a significant decrease of switch frequency (−0.08 Hz) for each subject. In conclusion, changes in mode of coordination implementation suggest that the in-phase mode implementation is highly linked to the strength production capacity at the ankle joint.     

Dynamical changes in corticospinal excitability during imagery of unimanual and bimanual wrist movements in humans: a transcranial magnetic stimulation study

This study explored the dynamical changes in corticospinal excitability during the imagination of cyclical unimanual and bimanual wrist flexion-extension movements. Transcranial magnetic stimulation was applied over the left motor cortex to evoke motor evoked potentials in the right wrist flexor and extensor muscles. Findings provided evidence for increased reciprocal excitability changes during imagery of symmetrical in-phase movements as compared to asymmetrical (anti-phase) or unimanual movements. This suggests that in-phase movements may reinforce whereas anti-phase movements may reduce the temporal representation of the task in the corticospinal motor networks of the brain.     

Let your feet do the walking: constraints on the stability of bipedal coordination

In this paper we consider whether the behaviour of the neural circuitry that controls lower limb movements in humans is shaped primarily by the spatiotemporal characteristics of bipedal gait patterns, or by selective pressures that are sensitive to considerations of balance and energetics. During the course of normal locomotion, the full dynamics of the neural circuitry are masked by the inertial properties of the limbs. In the present study, participants executed bipedal movements in conditions in which their feet were either unloaded or subject to additional inertial loads. Two patterns of rhythmic coordination were examined. In the in-phase mode, participants were required to flex their ankles and extend their ankles in synchrony. In the out-of-phase mode, the participants flexed one ankle while extending the other and vice versa. The frequency of movement was increased systematically throughout each experimental trial. All participants were able to maintain both the in-phase and the out-of-phase mode of coordination, to the point at which they could no longer increase their frequency of movement. Transitions between the two modes were not observed, and the stability of the out-of-phase and in-phase modes of coordination was equivalent at all movement frequencies. These findings indicate that, in humans, the behaviour of the neural circuitry underlying coordinated movements of the lower limbs is not constrained strongly by the spatiotemporal symmetries of bipedal gait patterns.     

Instabilities during antiphase bimanual movements: are ipsilateral pathways involved?

The spatial and temporal coupling between the hands is known to be very robust during movements which use homologous muscles (in-phase or symmetric movements). In contrast, movements using nonhomologous muscles (antiphase or asymmetric movements) are less stable and exhibit a tendency to undergo a phase transition to in-phase movements as movement frequency increases. The instability during antiphase movements has been modeled in terms of signal interference mediated by the ipsilateral corticospinal pathways. In this study we report that participants in whom distal ipsilateral motor-evoked potentials could be elicited with transcranial magnetic stimulation (TMS), exhibited higher variability during a bimanual circling task than participants whose ipsilateral pathways could not be transcranially activated. These results suggest that ipsilateral control of the limb affects the level of bimanual coupling, and may contribute to uncoupling phenomena observed during asymmetric coordination.     

High-frequency transcranial magnetic stimulation of the supplementary motor area reduces bimanual coupling during anti-phase but not in-phase movements

Previous electrophysiological and neuroimaging studies have provided evidence that the supplementary motor area (SMA) has an important role in the control of bimanual coordination. The present experiment investigated the effects of high-frequency repetitive transcranial magnetic stimulation (rTMS) over the SMA region on kinematic variables during cyclical bimanual coordination, with a particular focus on the quality of coordination. Subjects performed metronome-paced trials of in-phase and anti-phase bimanual index-finger movements at near-maximal cycling frequency. During movement execution, rTMS (20 Hz, 0.5 s, 120% hand motor threshold) was applied over one of three positions in the sagittal midline 2.0, 4.0 and 6.0 cm anterior to the primary motor leg area. Sham rTMS was included as a control condition. After rTMS, the mean relative phase error between hands increased, but only in the anti-phase trials. The maximum increase in phase error occurred immediately after rather than during the rTMS train. The effect was largest after stimulation 4 or 6 cm anterior to the leg area of the primary motor cortex. We did not observe any changes in the variability of relative phase or in cycle duration or movement amplitude. Findings are discussed in light of recent functional models on the role of the SMA in bimanual movement control.     

Load compensation during homologous and non-homologous coordination

Two-limb coordination of homologous and non-homologous effectors was examined during isofrequency (1:1) and multifrequency (2:1) conditions. The coordination patterns involved flexion and extension movements in the sagittal plane and were performed under unloaded and single-limb (right arm) loaded conditions. Previous studies suggested that the lower degree of 1:1 synchronization observed during nonhomologous as compared to homologous coordination results from natural differences in biophysical (inertial) properties. Elaborating on this idea, adding weight to the right arm was hypothesized to modulate its inertial characteristics, rendering homologous limbs more dissimilar and nonhomologous limbs more similar by enhancing and decreasing their inertial differences, respectively. Therefore, the observations made during unloaded conditions were predicted to be completely reversed during loaded conditions. Findings revealed that during 1:1 coordination (experiment 1) single-limb loading resulted in a decreased relative phase stability, whereas relative phase accuracy depended upon the limb combination. In particular, phase-locking was more accurately maintained for loaded homologous than for nonhomologous limbs, whereas loading the nonhomologous limbs resulted in a deterioration of the quality of synchronization. These findings suggest that there is an additional explanation of differential coordination capabilities among limb combinations. It is hypothesized that the neural networks subserving the control centers of the homologous limbs are more tightly connected than those of the nonhomologous effectors, allowing 1:1 synchronization to be more successfully preserved in the face of (load) perturbations. During 2:1 coordination (experiment 2), the loading procedure disturbed the coordination dynamics across all limb combinations. That no differential effect of loading on effector combination was observed is possibly a result of the fact that only an initial level of practice was studied in which optimal relative phase dynamics are still being explored for both homologous and nonhomologous limbs. Received: 7 May 1997 / Accepted: 16 January 1998