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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.

Adult↗

Interlimb coordination: real constraints and false dichotomies.

Despite the recent advances in the field of coordination dynamics addressing the interplay of constraints of different natures in the emergence of human coordination, F. Mechsner (2004) invites us to revive hierarchical and dichotomous thinking b y offering again his exclusive position that coordinated movements are (purely) perceptual-cognitive/psychological in nature. In this comment, the authors address a number of theoretical and methodological issues that might potentially puzzle the readers of Mechsner's article. They contend that the dichotomy proposed by Mechsner (i.e., perceptual-cognitive vs. motor) constitutes a restrictive framework for understanding human coordination.

Hand↗

Interlimb coordination of posture in patients with spastic paresis. Impaired function of spinal reflexes.

Activation of leg musculature on both sides following a unilateral displacement was studied during stance on separate see-saws, or on stable force-measuring platforms, in patients with spastic hemiparesis and paraparesis. During balancing the movements on the spastic side were damped and the degree of muscle activation reduced. Whereas in healthy subjects the tibialis anterior muscles of both sides were activated, following a unilateral displacement, with the same strength and latency (see-saws 55 ms, platforms 85 ms), in hemispastic patients the EMG responses were delayed (by about 20 to 30 ms) and of reduced strength on the spastic leg, irrespective of whether the unaffected or the spastic side was displaced. In addition, the compensatory movements on the spastic side were damped in both conditions, although the amplitude of displacement was the same bilaterally. Although there was no correlation between the delay and the reduction in EMG response, the latter was correlated with the severity of paresis. In patients with spastic paraparesis quite similar results were obtained with delayed and reduced EMG responses on both sides. It is concluded that in spasticity the impaired regulation of quick compensatory movements is due to a dysfunction of a spinal interneuronal system by which the early EMG responses are mediated. This could be explained by loss of supraspinal control. In addition to the impaired neural activation of leg muscles, changes in the mechanical properties of muscle can be assumed to contribute to the damped movements on the spastic side.

Adult↗

Aging effects on the metabolic and cognitive energy cost of interlimb coordination.

Many everyday motor tasks have high metabolic energy demands, and some require extended practice to learn the required coordination between limbs. Eight older (73.1 +/- 4.4 years) and 8 younger (23.3 +/- 5.9) men practiced a high-energy two-hand coordination task with both 180 degrees and 90 degrees target relative phase. The older group showed greater performance error in both conditions, and performance at 90 degrees was strongly attracted to antiphase coordination (180 degrees). In a retention test one week following the acquisition trials, the older group had learned the 180 degrees condition but did not learn the 90 degrees condition. Metabolic energy cost was not different between groups, but the older men showed higher heart rate and both conditions imposed greater cognitive demands as revealed in auditory probe reaction time. Older adults' motor learning may be inhibited by elevated heart rate at the same oxygen cost, increased cognitive cost, and an attraction toward more established low-energy in-phase or antiphase coordination.

Adult↗

The locomotion of the low spinal cat. II. Interlimb coordination.

The interaction of the two hindlimbs were investigated by an analysis of the muscular activity and the movements in 14 chronic spinal kittens during treadmill locomotion (i.e. in kittens subjected to a transection of the spinal cord (Th10--12)) one or two weeks after birth). At low speed the limbs were alternating (walk or trot). At higher they were activated more simultaneous, as during gallop. The two limbs could walk at different velocities, as during walking in a circle, when the two belts of the treadmill were driven at different speeds. The duration of the support phases was mainly influenced by the speed of the belt on which the limb was walking. The limbs could still maintain a common rhythm up to a two or three fold speed difference, as the flexion or the first extension phase of the limb walking on the "fast" belt was prolonged and the flexion phase of "slow limb" was shortened. At extreme speed differences the limb on the "fast belt" performed 2, 3 and even 4 steps during one stepcycle of the "slow limb". The placement of the feet was found to maintain the most stable relationship during alternating gaits at different speed differences. It is concluded that all phases of the step cycle are modifiable and that there are several mechanisms coordinating the limbs within the spinal cord.

Animals↗

On the nature of human interlimb coordination.

Movement time varies as a function of amplitude and requirements for precision, according to Fitts' law, but when subjects perform two-handed movements to targets of widely disparate difficulty they do so simultaneously. The hand moving to an "easy" target moves more slowly to accommodate its "difficult" counterpart, yet both hands reach peak velocity and acceleration synchronously. This result suggests that the brain produces simultaneity of action not by controlling each limb independently, but by organizing functional groupings of muscles that are constrained to act as a single unit.

Adult↗

Interlimb coordination of leg-muscle activation during perturbation of stance in humans.

1. Electromyographic (EMG) responses were recorded in both legs, along with corresponding joint movements, after uni- and bilateral perturbations during stance on a treadmill with split belts. Displacements were directed forward, backward, or in opposing directions. They were induced by randomly timed ramp impulses at one of four different rates of treadmill acceleration. 2. Unilateral perturbations directed backward were followed by a bilateral gastrocnemius-EMG response, forward-directed perturbations by a bilateral tibialis anterior-EMG response. The amplitude of these responses was dependent on the rate of treadmill acceleration. Relative to the response of the displaced leg, the amplitude of the EMG response on the nondisplaced side was smaller when a gastrocnemius EMG response was induced, and about equal when the tibialis anterior muscle was activated. The onset latencies were shorter on the displaced side (displaced leg 75-96 ms, non-displaced leg 93-112 ms). 3. Bilateral perturbations in one direction were followed by larger EMG responses in both legs (in the gastrocnemius for backward-directed impulses, in the tibialis anterior for forward-directed impulses). For a given acceleration rate, their amplitude was about equal to the sum of the EMG amplitude of the displaced leg and that of the nondisplaced leg obtained during unilateral displacement. The inverse result was obtained when the legs were simultaneously displaced in opposite directions: EMG responses in both legs were significantly smaller than those obtained after unilateral displacement. 4. It is concluded that a unilateral displacement evokes reflex EMG responses in the synergistic muscles of both legs, which are graded according to the size of the proprioceptive input from the primarily displaced joint. During bilateral displacements, the activity induced by the respective contralateral leg is linearly summed or subtracted, depending on whether the legs are displaced in the same or in opposite directions. In view of the short latencies of these bilateral responses, it would seem that they are mediated by a spinal mechanism. 5. Distinct differences in the behavior of the antagonistic leg muscles were observed: 1) the coactivation of the contralateral leg muscle was significantly smaller when the gastrocnemius was stretched unilaterally, whereas it was about equal for the tibialis anterior; and 2) the gastrocnemius EMG responses were closely correlated with the displacement velocity, whereas the tibialis anterior response was more closely correlated with acceleration, i.e., the tibialis anterior response was more dynamic in nature.(ABSTRACT TRUNCATED AT 400 WORDS)

Adult↗

Interlimb coordination deficits during cyclic movements in cerebellar hemiataxia.

The authors report a 35-year-old man whose unilateral cerebellar lesion resulted in marked deficits in coordinating simultaneous cyclic movements of the arm and leg on his ipsilesional side. He exhibited no such deficits when making simultaneous movements of the contralesional limbs or when moving paired left and right limbs. Thus, the cerebellum, which is already known to underlie within-limb interjoint coordination, also contributes to coordination between limbs.

Adult↗

Mass perturbation of a body segment: 2. Effects on interlimb coordination.

The shifts in relative phase that are observed when rhythmically coordinated limbs are submitted to asymmetric mass perturbations have typically been attributed to the induced eigenfrequency difference (delta omega) between limbs. Modeling the moving limbs as forced linear oscillators, however, reveals that asymmetric mass perturbations may induce a difference not only in eigenfrequency (i.e., delta omega not equal 0) but also in the covarying low-frequency control gains (i.e., delta k not equal 0). Because the inverse of the low-frequency control gain (k) reflects the level of muscular torque (input) required for a particular displacement from equilibrium (output), asymmetric mass perturbations may result in an imbalance in the muscular torques required for task performance (related to delta k not equal 0). Thus, it is possible that the effects attributed to delta omega were in fact mediated by delta k. In 2 experiments, the authors manipulated delta k and delta omega separately by applying mass perturbations to the lower legs of 9 participants. The relative phasing between the legs was not affected by delta k, but manipulation of delta omega (while delta k remained approximately 0) induced systematic relative phase shifts that were more pronounced for antiphase than for in-phase coordination. That indication that the coordination dynamics is indeed influenced by an imbalance in eigenfrequency is discussed vis-a-vis the question of how such a merely peripheral property may affect the underlying coordination process.

Extremities↗

The developmental origins of bimanual coordination: a dynamic perspective.

Patterns of interlimb coordination associated with infant reaching fluctuate frequently over developmental time. This study investigated whether these fluctuations are related to coordination tendencies. Interlimb patterns were studied in reaching and nonreaching movements in 4 infants, which were followed through their 1st year. Each week, reaching and nonreaching endpoint kinematics were recorded in both arms during multiple 14-s trials. It was found that patterns of interlimb coordination in reaching matched coordination tendencies in nonreaching. Reaching fluctuated between uni- and bimanual periods. During the bimanual periods, nonreaching interlimb activity tended to be synchronous. During the unimanual periods, nonreaching activity revealed no predominant form of interlimb coordination. It is argued that changing coordination tendencies may influence the organization of specific goal-oriented behaviors from early in life.

Female↗

Prism aftereffects disrupt interlimb rhythmic coordination.

The authors examined effects of prism-induced proprioceptive aftereffects on coordination of 95 participants and compared interlimb rhythmic coordination performed before versus after exposure to prisms of varying optical displacements. The observed steady states of relative phase for postprism exposure coordination were shifted by a small but significant amount, but not across all prism conditions. Phase-shift direction was not specific to the direction of optical displacement and was not, across all conditions, proportional to the magnitude of optical displacement. Prism exposure was associated with increased relative phase variability for all prism conditions. A no-prism control group showed no changes in interlimb rhythmic coordination. The results suggest that prism-induced proprioceptive aftereffects have general, disruptive effects on interlimb rhythmic coordination.

Adaptation, Physiological↗

Experimental study of coordination patterns during unsteady locomotion in mammals.

A framework to study interlimb coordination, which allowed the analysis of all the symmetrical and asymmetrical gaits, was recently proposed. It suggests that gait depends on a common basic pattern controlling the coordination of the forelimbs (fore lag, FL), the coordination of the hindlimbs (hind lag, HL) and the relationship between these two pairs of limbs (pair lag, PL) in an anteroposterior sequence of movement (APS). These three time parameters are sufficient for identifying all steady gaits. We assumed in this work that this same framework could also be used to study non-steady locomotion, particularly the transitions between symmetrical and asymmetrical gaits. Moreover, as the limbs are coordinated in time and also in space during locomotion, we associated three analogous space parameters (fore gap, FG; hind gap, HG and pair gap, PG) to the three time parameters. We studied the interlimb coordination of dogs and cats moving on a runway with a symmetrical gait. In the middle of the runway, the gait was disturbed by an obstacle, and the animal had to change to an asymmetrical coordination to get over it. The time (FL, HL, PL) and space (FG, HG, PG) parameters of each sequence of the trials were calculated. The results demonstrated that the APS method allows quantification of the interlimb coordination during the symmetrical and asymmetrical phases and during the transition between them, in both dogs and cats. The space and time parameters make it possible to link the timing and the spacing of the footfalls, and to quantify the spatiotemporal dimension of gaits in different mammals. The slight differences observed between dogs and cats could reflect their morphological differences. The APS method could thus be used to understand the implication of morphology in interlimb coordination. All these results are consistent with current knowledge in biomechanics and neurobiology, therefore the APS reflects the actual biological functioning of quadrupedal interlimb coordination.

Animals↗

Prism exposure affects the proprioceptive frames of reference for interlimb rhythmic coordination.

Adaptation to prisms can produce a change in felt arm position, termed proprioceptive shift. We studied the effects of prism-induced proprioceptive shift on interlimb rhythmic coordination performed under proprioceptive guidance, in the absence of vision. Relative to interlimb rhythmic coordination performed before prism exposure, the observed steady states of relative phase for postexposure coordination were shifted by a small but reliable amount. The shift was in the direction expected, given the direction of optical displacement. The amount of variability of interlimb rhythmic coordination was unaffected by prism exposure. The results suggest that the same spatial frames of reference altered by prism adaptation are involved in the production of interlimb rhythmic coordination patterns.

Adult↗

Conjugate limb coordination after experience with an interlimb yoke: evidence for motor learning in the rat fetus.

This study investigated the capacity of the E20 rat fetus to adaptively alter patterns of interlimb coordination in a prenatal model of motor learning. Fetal limb movement was manipulated with an interlimb yoke, consisting of a fine thread attached at the ankles, which created a physical linkage between two limbs. Exposure to the yoke resulted in a gradual increase in conjugate movements of the yoked limbs during a 30-min training period, which persisted after removal of the yoke. Training effects were evident when the yoke was applied to two hindlimbs, two forelimbs, or a homolateral forelimb-hindlimb pair. A savings in the rate of acquisition also was observed when fetuses experienced yoke training in a second session. These data argue that the rat fetus can respond to kinesthetic feedback resulting from variation in motor performance, which suggests that experience contributes to the development of coordinated motor behavior before birth.

Analysis of Variance↗

Effects of tendon vibration on the spatiotemporal characteristics of human locomotion.

The present study addressed the involvement of proprioceptive input of the muscle spindles in the spatiotemporal control of human locomotion. Blindfolded subjects walked along a walkway while tendon vibration, a powerful stimulus of Ia afferents, was applied to various muscles of the lower limb. The effects of tendon vibration were measured on joint kinematics and on intralimb and interlimb coordination. Tendon vibration of the tibialis anterior during locomotion led to a decreased plantar flexion at toe-off, whereas vibration of the triceps surae led to a decreased dorsiflexion during swing. Vibration of the quadriceps femoris at the knee led to a decreased knee flexion during swing. These local effects of vibration can be explained in the light of a lengthening illusion of the vibrated muscle in that phase of the gait cycle where the muscle is lengthened. Tendon vibration did not affect the qualitative features of intralimb coordination. With respect to interlimb coordination, only vibration of the biceps femoris showed a significant increase in phase lead of the vibrated limb. The present results suggest the involvement of Ia afferent input in the online control of joint rotations. Additionally it is hypothesized that the proprioceptive input of biceps femoris might be involved in the control of coordination between the limbs, whereas the coordination between the segments of one limb appears to be unaffected by disturbance of muscle spindle input of one muscle.

Adult↗

Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination.

Single neuronal activity was recorded from the supplementary motor area (SMA-proper and pre-SMA) and primary motor cortex (M1) in two Macaca fascicularis trained to perform a delayed conditional sequence of coordinated bimanual pull and grasp movements. The behavioural paradigm was designed to distinguish neuronal activity associated with bimanual coordination from that related to a comparable motor sequence but executed unimanually (left or right arm only). The bimanual and unimanual trials were instructed in a random order by a visual cue. Following the cue, there was a waiting period until presentation of a "go-signal", signalling the monkey to perform the instructed movement. A total of 143 task-related neurons were recorded from the SMA (SMA-proper, 62; pre-SMA, 81). Most SMA units (87%) were active in both unimanual contralateral and unimanual ipsilateral trials (bilateral neurons), whereas 9% of units were active only in unimanual contralateral trials and 3% were active only in unimanual ipsilateral trials. Forty-eight per cent of SMA task-related units were classified as bimanual, defined as neurons in which the activity observed in bimanual trials could not be predicted from that associated with unimanual trials when comparing the same events related to the same arm. For direct comparison, 527 neurons were recorded from M1 in the same monkeys performing the same tasks. The comparison showed that M1 contains significantly less bilateral neurons (75%) than the SMA, whereas the reverse was observed for contralateral neurons (22% in M1). The proportion of M1 bimanual cells (53%) was not statistically different from that observed in the SMA. The results suggest that both the SMA and M1 may contribute to the control of sequential bimanual coordinated movements. Interlimb coordination may then take place in a distributed network including at least the SMA and M1, but the contribution of other cortical and subcortical areas such as cingulate motor cortex and basal ganglia remains to be investigated.

Animals↗

The development of quadrupedal locomotion in the kitten.

The development of bipedal treadmill locomotion and overground locomotion has previously been studied in the kitten; the development of quadrupedal treadmill locomotion has not. We evaluated and compared all three forms of locomotion in the normal kitten and present quantitative data comparing the development of quadrupedal treadmill and overground locomotion. Overground locomotion was studied from the day of birth to 5 months of age and quadrupedal treadmill locomotion was studied in the same animals from 9 weeks to 5 months of age. Treadmill locomotion was initiated postweaning, since it could not be reliably elicited without a food reward. Three locomotor characteristics (weight support, balance, and coordination between the forelimbs and the hindlimbs) were evaluated quantitatively. Kittens first consistently demonstrated overground steps with the ventral surface of their bodies supported above the walking surface throughout the entire step cycle during the second and third postnatal weeks. By 4 weeks of age, overground locomotion consistently showed full weight support and midline positioning of the hindquarters. Coordination between the forelimbs and the hindlimbs developed differently in the two forms of quadrupedal locomotion evaluated. During overground locomotion, the kittens initially used a single pattern in which only one limb was in swing at any time. As the kittens' weight support and trunk control improved, additional swing phase coordination patterns emerged and these patterns were correlated with the animals' ability to change speeds during locomotion. The consistency with which a dominant interlimb swing phase pattern was used at a particular speed increased with age and, by 6 weeks, the frequency of each speed-related dominant pattern approached 100% during overground locomotion. At 6 weeks, interlimb coordination also was evident in the nearly consistent interlimb phase interval present between the forelimb's initiation of the first extension subphase and the ipsilateral hindlimb's initiation of the flexion phase. The consistent patterns appeared to be fostered by maturation of weight support and balance. In contrast, the interlimb phase interval was inconsistent during quadrupedal treadmill locomotion until 20 weeks of age. Moreover, the interlimb swing phase patterns used during quadrupedal treadmill locomotion differed from those used during overground locomotion. The differences in the developmental time course and patterns of interlimb coordination between overground and quadrupedal treadmill locomotion suggest that different mechanisms regulate the control of interlimb coordination during these two different forms of quadrupedal locomotion.

Age Factors↗