The metabolic and cognitive energy costs of stabilising a high-energy interlimb coordination task

Kinematic (relative phase error), metabolic (oxygen consumption, heart rate) and attentional (baseline and cycling reaction times) variables were measured while participants practised a high energy-demanding, intrinsically unstable 90 degrees relative phase coordination pattern on independent bicycle ergometers. The variables were found to be strongly inter-correlated, suggesting a link between emerging performance stability with practice and minimal metabolic and attentional cost. The effects of practice of 90 degrees relative phase coordination on the performance of in-phase (0 degrees-phase) and antiphase (180 degrees-phase) coordination were investigated by measuring the relative phase attractor layouts and recording the metabolic and attentional cost of the three coordination patterns before and after practice. The attentional variables did not differ significantly between coordination patterns and did not change with practice. Before practice, the coordination performance was most accurate and stable for in-phase cycling, with antiphase next and 90 degrees-phase the poorest. However, metabolic cost was lower for antiphase than either in-phase or 90 degrees-phase cycling, and the pre-practice attractor layout deviated from that predicted on the basis of dynamic stability as an attractor state, revealing an attraction to antiphase cycling. After practice of 90 degrees-phase cycling, in-phase cycling remained the most accurate and stable, with 90 degrees-phase next and antiphase the poorest, but antiphase retained the lowest metabolic energy cost. The attractor layout had changed, with new attractors formed at the practised 90 degrees-phase pattern and its symmetrical partner of 270 degrees-phase. Considering both the pre- and post-practice results, attractors were formed at either a low metabolic energy cost but less stable (antiphase) pattern or at a more stable but higher metabolic energy cost (90 degrees-phase) pattern, but in neither case at the most stable and accurate (in-phase) pattern. The results suggest that energetic factors affect coordination dynamics and that coordination modes lower in metabolic energy expenditure may compete with dynamically stable modes.     

To Switch or Not to Switch: Recruitment of Degrees of Freedom Stabilizes Biological Coordination

Recruitment and suppression processes were studied in the swinging-pendulum paradigm (cf. P. N. Kugler & M. T. Turvey, 1987). The authors pursued the hypothesis that active recruitment of previously unmeasured degrees of freedom serves to stabilize an antiphase bimanual coordination pattern and thereby obviates the need for pattern switching from an antiphase to an in-phase coordination pattern, a key prediction of the H. Haken, J. A. S. Kelso, and H. Bunz (1985) model. In Experiment 1, 7 subjects swung single hand-held pendulums in time with an auditory metronome whose frequency increased. Pendulum motion changed from planar (2D) to elliptical (3D), and forearm motion (produced by elbow flexion-extension) was recruited with increasing movement rate for cycling frequencies typically above the pendulum's eigenfrequency. In Experiment 2, 7 subjects swung paired pendulums in either an in-phase or an antiphase coordinative mode as movement rate was increased. With the systematic increase in movement rate, the authors attempted to induce transitions from the antiphase to the in-phase coordinative pattern, with loss of stability the key mechanism of pattern change. Transitions from the antiphase to the in-phase coordinative mode were not observed. Pattern stability, as defined by the variability of the phase relation between the pendulums, was affected only a little by increasing movement rate. As in the single-pendulum case, pendulum motion changed from planar to elliptical, and forearm motion was recruited with increasing cycling frequency. Those results reveal a richer dynamics than previously observed in the pendulum paradigm and support the hypothesis that recruitment processes stabilize coordination in biomechanically redundant systems, thereby reducing the need for pattern switching.     

One-to-one and polyrhythmic temporal coordination in bimanual circle tracing

The authors manipulated movement amplitude in a bimanual circle-tracing task to alter the natural tracing frequency of the arms. Participants (N = 14) traced different-diameter circles simultaneously with the two arms in either in-phase (0 degrees) or antiphase (180 degrees) coordination, using the index fingers or plastic styli. Movement amplitude altered the natural tracing frequency of the arms, as demonstrated by the following 2 findings: (a) The larger the difference in circle diameter, the larger was the shift from the fixed-point values of 0 degrees and 180 degrees, and the shift increased as movement frequency increased. Those results are consistent with the manipulation of delta omega in the bimanual pendulum paradigm. (b) Increasing movement frequency induced transitions from 1:1 to non-1:1 coordination, contrary to findings in previous investigations of polyrhythmic coordination. Tactile feedback played a minimal role in stabilizing bimanual coordination in the current tasks.     

Dynamics of 1:2 Coordination: Temporal Scaling, Latent 1:1, and Bistability

The simplest interlimb multifrequency coordination of 1:2 can be performed at different speeds and in at least two different styles or modes. The effects of speed and mode (in-phase or antiphase) were evaluated in a bimanual 1:2 rhythmic task in which participants (N = 8) oscillated hand-held pendulums with identical or different uncoupled frequencies. A motion equation in relative phase that captures the asymmetries of components and task predicted the 1:2 coordination equilibria resulting from temporal scaling. According to the experimental results, both coordination modes proved to be equally stable. More detailed analyses of individual trials showed signs that the more fundamental 1:1 coordination intruded into the 1:2 coordination.     

Dynamics of learning new postural patterns: influence on preexisting spontaneous behaviors

In stance, rotations around the hips and ankles typically exhibit a relative phase close to 20 degrees or 180 degrees . In 2 experiments, the authors studied the reciprocal influence of those coordination tendencies with learning an ankle-hip relative phase of 135 degrees . Before, during, and after learning a new mode of coordination, they assessed participants' (N = 24 in each experiment) spontaneous postural patterns with a tracking task in which no specific coordination was required. Learning the 135 degrees phase relation led to persistent modifications of the spontaneous in-phase and antiphase modes. Contrary to the theoretical predictions of the dynamical approach, the initial stability of the preexisting patterns did not influence the difficulty of producing the new mode or the improvement in performance during learning. Initial stability did, however, influence the rate and type of modification of spontaneous patterns. The authors discuss the results in relation to conclusions drawn from bimanual studies.     

The efficacy of the Microsoft Kinect<Superscript>TM</Superscript> to assess human bimanual coordination

The Microsoft Kinect has been used in studies examining posture and gait. Despite the advantages of portability and low cost, this device has not been used to assess interlimb coordination. Fundamental insights into movement control, variability, health, and functional status can be gained by examining coordination patterns. In this study, we investigated the efficacy of the Microsoft Kinect to capture bimanual coordination relative to a research-grade motion capture system. Twenty-four healthy adults performed coordinated hand movements in two patterns (in-phase and antiphase) at eight movement frequencies (1.00–3.33 Hz). Continuous relative phase (CRP) and discrete relative phase (DRP) were used to quantify the means (mCRP and mDRP) and variability (sdCRP and sdDRP) of coordination patterns. Between-device agreement was assessed using Bland–Altman bias with 95 % limits of agreement, concordance correlation coefficients (absolute agreement), and Pearson correlation coefficients (relative agreement). Modest-to-excellent relative and absolute agreements were found for mCRP in all conditions. However, mDRP showed poor agreement for the in-phase pattern at low frequencies, due to large between-device differences in a subset of participants. By contrast, poor absolute agreement was observed for both sdCRP and sdDRP, while relative agreement ranged from poor to excellent. Overall, the Kinect captures the macroscopic patterns of bimanual coordination better than coordination variability.     

The effect of volition on the stability of bimanual coordination

The authors investigated how the intention to passively perform a behavior and the intention to persist with a behavior impact upon the spatial and temporal properties of bimanual coordination. Participants (N = 30) were asked to perform a bimanual coordination task that demanded the continuous rhythmic extension-flexion of the wrists. The frequency of movement was scaled by an auditory metronome beat from 1.5 Hz, increasing to 3.25 Hz in.25-Hz increments. The task was further defined by the requirement that the movements be performed initially in a prescribed pattern of coordination (in-phase or antiphase) while the participants assumed one of two different intentional states: stay with the prescribed pattern should it become unstable or do not intervene should the pattern begin to change. Transitions away from the initially prescribed pattern were observed only in trials conducted in the antiphase mode of coordination. The time at which the antiphase pattern of coordination became unstable was not found to be influenced by the intentional state. In addition, the do-not-intervene set led to a switch to an in-phase pattern of coordination whereas the stay set led to phase wandering. Those findings are discussed within the framework of a dynamic account of bimanual coordination.     

Coordination Dynamics of the Bipedal Galloping Pattern

A motion equation in relative phase was developed that incorporates the spatial-temporal pattern of the bipedal gallop along with the more commonplace patterns of the bipedal jump and walk-run. In 3 experiments, human participants (N = 6 per experiment) simulated the bipedal gait patterns through the rhythmic motions of hand-held pendulums. Predictions of the motion equation for coordination equilibria and their respective degrees of stability were confirmed. In particular, the gallop pattern was less stable than the fundamental in-phase and antiphase patterns but changed in qualitatively similar ways to those gaits as a function of limb asymmetry and movement frequency. The relation between the modeled coordination dynamics and the kinematic characteristics of real bipedal galloping is discussed     

Attentional loads associated with interlimb interactions underlying rhythmic bimanual coordination

Studies of rhythmic bimanual coordination under dual-task conditions revealed (1) a dependence of secondary task performance on the stability of coordinative tasks, in that secondary task performance was better during in-phase than antiphase coordination, and (2) a shift in the mean relative phasing between the limbs compared to single-task conditions. The present study aimed to account for these phenomena by dissociating three qualitatively different interactions between the limbs that govern this motor behavior, related to movement planning, error correction, and interlimb reflex activity. The experiment probed the cognitive demands associated with each interlimb interaction by examining the attentional load under dual-task conditions, indexed by reaction times of the secondary task and kinematic changes in the coordinative tasks relative to single-task conditions. First, only in the condition that involved interlimb interactions at the level of movement planning reaction times were shorter for in-phase than for antiphase coordination, highlighting an intimate relation between movement planning and attentional processes. Second, under dual-task conditions a shift in the mean relative phase was observed relative to single-task conditions, but only for the interlimb interactions that depend directly on sensory feedback (error correction and interlimb reflex activity). These observations qualified the effects of attentional load reported in previous studies. Third, reaction times varied systematically over the movement cycle. These variations revealed a dynamical signature of the attentional load that differed between the three interlimb interactions.     

Dynamics of 1:2 Coordination: Temporal Scaling,Latent 1:1, and Bistability

The simplest interlimb multifrequency coordination of 1:2 can be performed at different speeds and in at least two different styles or modes. The effects of speed and mode (in-phase or antiphase) were evaluated in a bimanual 1:2 rhythmic task in which participants (N = 8) oscillated hand-held pendulums with identical or different uncoupled frequencies. A motion equation in relative phase that captures the asymmetries of components and task predicted the 1:2 coordination equilibria resulting from temporal scaling. According to the experimental results, both coordination modes proved to be equally stable. More detailed analyses of individual trials showed signs that the more fundamental 1:1 coordination intruded into the 1:2 coordination.     

Dual-Finger Preferred-Speed Tapping: Effects of Coordination Mode and Anatomical Finger and Limb Pairings

Interlimb and interfinger coordination were examined in a dual-finger tapping paradigm in which 16 subjects performed at preferred frequencies. Three bimanual finger combinations, in random order (2 index; 2 middle; and 1 index and 1 middle), were performed in in-phase and antiphase coordination modes, in addition to 1 unimanual combination (antiphase index-middle). Relative phase means were within 3&percent; accuracy for all conditions. A lower tapping frequency was found in all antiphase vs. in-phase conditions, accompanied by lower phasing variability and lower intrafinger consistency in the antiphase. When frequency was changed from the preferred rate, the 2 coordination modes became more alike in variability and, within the same frequency range, demonstrated no significant differences. The bimanual mixed-fingers tapping tended to have significantly lower phasing values (a small fixed point drift) and higher tapping frequencies than the symmetric conditions. The unimanual task was similar to all other antiphase conditions. Changes in preferred frequency with different coordination modes may be related to differing perceptual informational constraints. Current models addressing natural frequencies of coupled oscillators do not account for the present data.     

Coordination Dynamics of the Bipedal Galloping Pattern

A motion equation in relative phase was developed that incorporates the spatial-temporal pattern of the bipedal gallop along with the more commonplace patterns of the bipedal jump and walk-run. In 3 experiments, human participants (N = 6 per experiment) simulated the bipedal gait patterns through the rhythmic motions of hand-held pendulums. Predictions of the motion equation for coordination equilibria and their respective degrees of stability were confirmed. In particular, the gallop pattern was less stable than the fundamental in-phase and antiphase patterns but changed in qualitatively similar ways to those gaits as a function of limb asymmetry and movement frequency. The relation between the modeled coordination dynamics and the kinematic characteristics of real bipedal galloping is discussed.     

Concurrent cognitive task modulates coordination dynamics

Does a concurrent cognitive task affect the dynamics of bimanual rhythmic coordination? In‐phase coordination was performed under manipulations of phase detuning and movement frequency and either singly or in combination with an arithmetic task. Predicted direction‐specific shifts in stable relative phase from 0° due to detuning and movement frequency were amplified by the cognitive task. Nonlinear cross‐recurrence analysis suggested that this cognitive influence on the locations of the stable points or attractors of coordination entailed a magnification of attractor noise without a reduction in attractor strength. An approximation to these findings was achieved through parameter changes in a motion equation in relative phase. Results are discussed in terms of dual‐task performance as limited resources, dynamics rather than chronometrics, and reparameterization rather than degradation.     

Age-related differences in the integration of sensory information during the execution of a bimanual coordination task

Young (n = 7) and elderly (n = 7) subjects performed bimanual coordination patterns in the transverse plane according to the in-phase or antiphase mode. Sensory information was manipulated through visual (with or without vision of the limbs) and proprioceptive input (with or without vibratory stimuli on one limb). Movement patterns with vibrations showed higher deviations from the intended relative phase than did those without vibrations. This finding suggests that the proprioceptive information induced by the vibrations and the movement interfered, leading to a disruption of the coordination patterns. In addition, as compared with the elderly, the young subjects performed more stable movements under normal circumstances but were more strongly affected by vibratory stimuli during the performance of in-phase movements. During antiphase movements, both age groups experienced a decrease of pattern stability. Furthermore, the absence or presence of visual feedback influenced the performance of the young subjects more than that of the elderly. The presence of vision led to stable in-phase movements, whereas a decrease of pattern stability was observed for antiphase movements. In general, these results demonstrate that manipulation of feedback sources affects young subjects more than elderly ones, and this can be related to a reduced sensory sensitivity as a function of aging.     

Intentional Switching Between Bimanual Coordination Patterns

Previous theoretical and empirical work indicates that intentional changes in a bimanual coordination pattern depends on the stability of the bimanual coordination pattern (Kelso, Schotz, & Schöner, 1988; Scholz & Kelso, 1990). The present experiments retest this notion when online Lissajous displays are provided. Switching to and from in-phase and antiphase and to and from 90° and 270° were tested in Experiment 1. Participants were able to very effectively produce the 180°, 90°, and 270° coordination patterns although performance of the in-phase coordination task was even more stable. The data indicated that switching to in-phase from antiphase was more rapid than vice versa and that switching times between 90° to 270° were similar. Experiment 2 investigated switching between 1:2 and 2:1 bimanual coordination patterns. The results indicated that switching time was similar between the 2:1 and 1:2 coordination tasks and that increases in stability over practice resulted in additional decreases in switching times. This provides additional evidence that the attractor landscape is fundamentally different dependent on the type of information provided the performer. What remains to be done is to reconcile these results with the various theories/perspectives currently used to describe and explain bimanual coordination.     

Environmental coupling modulates the attractors of rhythmic coordination

A simple instance of coupling behavior to the environment is oscillating the hands in pace with metronome beats. This environmental coupling can be weaker (1 beat per cycle) or stronger (2 beats per cycle). The authors examined whether strength of environmental coupling enhanced the stability of in-phase bimanual coordination. Detuning by manipulanda that produced different left and right eigenfrequencies shifted the relative phase angle from 0 degrees, with the size of the shift larger for higher movement frequencies. Stronger environmental coupling was found to decrease this relative-phase shift, with accompanying increase and reduction, respectively, in recurrence quantification measures related to coordination stability and coordination noise. Stronger environmental coupling also increased oscillation amplitude. Results are considered from the perspective of parametric stabilization.     

Metabolic and attentional energy costs of interlimb coordination

The authors investigated metabolic and attentional energy costs as participants (N = 6) practiced in-phase, antiphase, and 90 degrees -phase cycling (order counterbalanced) on independent bicycle ergometers, with resistance (40 W/ergometer) and frequency (40 rpm) held constant. Coordination stabilized and became more accurate for all 3 cycling modes, as shown by measures of relative phase, but that collective variable could not account for other relevant attributes of the multifaceted motor behavior observed across the 3 coordination modes. In-phase and antiphase cycling were similar in stability and accuracy, but antiphase had the lowest metabolic and attentional energy costs. Because both homologous muscle action and perceptually symmetrical oscillations coincided in the in-phase mode, the absence of predominance of the inphase pattern showed that neither of those musculoskeletal and perceptual factors exclusively determined the strongest attractor of the coordination dynamics. Both metabolic and attentional costs declined with practice, consistent with the hypothesis that adaptive motor behavior is guided by sensory information concerning the energy demands of the task. Attentional cost was influenced not only by the information-processing demands of kinematic stability but also by the metabolic energy demands. Metabolic energy cost appeared to be the crucial determinant of the preferred solution for this coordination task.     

An event-based account of coordination stability

Constraints underlying bimanual coordination have traditionally been explained by dynamic interactions between the effectors. However, the present experiments demonstrate that a fundamental constraint on bimanual performance is the manner in which task goals are represented. In Experiment 1, participants vocalized during in-phase and anti-phase bimanual movements. As expected, most participants spontaneously exhibited temporal coupling between the manual and vocal responses. However, the form of coupling differed for the in-phase and anti-phase conditions. For anti-phase movements, there was a strong bias to produce two vocalizations per cycle; for in-phase movements, participants were equally likely to produce one or two vocalizations per cycle. We hypothesized that the spontaneous vocalizations probed the cognitive representation of the task, and the results indicated that anti-phase movements did entail a more complex event structure than in-phase movements did. In Experiment 2, we manipulated the event structure by having participants vocalize either once or twice per hand cycle. As predicted, coordination stability was reduced when the event structure was more complex.     

Bimanual finger tapping: effects of frequency and auditory information on timing consistency and coordination

The authors' goal in this study was to probe the basis for an earlier, unexpected finding that preferred-frequency finger tapping tends to have higher frequencies and to be less stable for in-phase than for antiphase tasks. In follow-up experiments, 3 protocols were employed: a preferred-frequency replication in both coordination modes, a metronome-driven matching of the preferred frequencies to each of the coordination modes, and a frequency scaling of both modes. The original findings were affirmed for preferred frequency. Tapping to a metronome had a differential effect on in-phase and antiphase: A more stable coupling across frequencies was exhibited during in-phase. Under frequency scaling, the antiphase pattern decomposed at lower frequencies than did in-phase, but no phase transitions were observed. The loss of stable coordination in both modes was attended by sudden increases in frequency differences between fingers and by phase wandering. The emergence of those effects is discussed in light of asymmetric modifications to the Haken-Kelso-Bunz model (H. Haken, J. A. S. Kelso, & H. Bunz, 1985) and the task constraints of tapping.     

Bimanual Finger Tapping: Effects of Frequency and Auditory Information on Timing Consistency and Coordination

The authors' goal in this study was to probe the basis for an earlier, unexpected finding that preferred-frequency finger tapping tends to have higher frequencies and to be less stable for in-phase than for antiphase tasks. In follow-up experiments, 3 protocols were employed: a preferred-frequency replication in both coordination modes, a metronome-driven matching of the preferred frequencies to each of the coordination modes, and a frequency scaling of both modes. The original findings were affirmed for preferred frequency. Tapping to a metronome had a differential effect on in-phase and antiphase: A more stable coupling across frequencies was exhibited during in-phase. Under frequency scaling, the antiphase pattern decomposed at lower frequencies than did in-phase, but no phase transitions were observed. The loss of stable coordination in both modes was attended by sudden increases in frequency differences between fingers and by phase wandering. The emergence of those effects is discussed in light of asymmetric modifications to the Haken-Kelso-Bunz model (H. Haken, J. A. S. Kelso, & H. Bunz, 1985) and the task constraints of tapping.