Task-dependent compensatory responses to perturbations applied during rhythmic movements in humans

Modulation of the responses to perturbation applied during different phases of three rhythmic movements in humans-running, cycling, and hopping-was studied. The perturbation was an electrical stimulus. The results showed gating and modulation of the responses in both ipsi- and contralateral limb muscles. The responses during running and cycling were only excitatory in nature, while during hopping an inhibitory response was observed. These responses were not correlated with the normal activity during the movement. The latency of the response in general was not altered for different stimulation phases. The alterations in the step cycle demonstrated overt behavioral changes due to the responses. There were differences between the responses observed during these movements and walking. In running, the major adaptation to perturbations appears to be in the contralateral side as seen in the changes in the step cycle. During cycling (except for one phase) and hopping, the same set of muscles was activated in response to perturbation. This represents a simplifying strategy in response organization. The dependency of the response on the task characteristics, postural stability requirement, and external constraints imposed on the subject is discussed. These studies provide insights into task-dependent strategies adopted by the nervous system to meet unexpected perturbation during rhythmic movements in humans.     

Phase-dependent compensatory responses to perturbation applied during walking in humans

The interaction between the peripheral and the central regulation of locomotion was studied by examining the dependency of the response to unexpected perturbation on the phase of the step cycle. The changes in the latency and magnitude of various muscle responses to electrical stimulation of the toe and applied unexpectedly at different phases of the locomotor cycle in humans are described. The results show that response to perturbation is gated and modulated in both ipsi- and contralateral limb muscles. These muscle responses, when present, were always excitatory in nature. They were not correlated with the normal locomotor activity, thus suggesting a more complex organization of the response. Except for one muscle in the contralateral limb, the latency of the other muscle responses did not vary across the step cycle. in response to the perturbation, the appropriate phase of the step cycle was shortened. The results from this study suggest that the perturbation applied elicits a phase-independent, normal ipsilateral flexor response in the tibialis anterior muscle, while the gating and modulation of other ipsi- and contralateral muscles provide appropriate phase-dependent adaptive response to maintain postural stability and continue with the ongoing task of locomotion.     

Phase-Dependent Compensatory Responses to Perturbation Applied During Walking in Humans

The interaction between the peripheral and the central regulation of locomotion was studied by examining the dependency of the response to unexpected perturbation on the phase of the step cycle. The changes in the latency and magnitude of various muscle responses to electrical stimulation of the toe applied unexpectedly at different phases of the locomotor cycle in humans are described. The results show that response to perturbation is gated and modulated in both ipsi-and contralateral limb muscles. These muscle responses, when present, were always excitatory in nature. They were not correlated with the normal locomotor activity, thus suggesting a more complex organization of the response. Except for one muscle in the contralateral limb, the latency of the other muscle responses did not vary across the step cycle. In response to the perturbation, the appropriate phase of the step cycle was shortened. The results from this study suggest that the perturbation applied elicits a phase-independent, normal ipsilateral flexor response in the tibialis anterior muscle, while the gating and modulation of other ipsi-and contralateral muscles provide appropriate phase-dependent adaptive response to maintain postural stability and continue with the ongoing task of locomotion.     

Stretch reflexes in the human masticatory muscles: a brief review and a new functional role

Stretch reflexes play a vital role in fine-tuning movements and in automatically maintaining posture. This article briefly reviews the operation of the stretch reflex in the human masticatory system. The conventional approach of stretching muscles in an open-loop manner has yielded much valuable information on the operation of this reflex. In particular, it has revealed that stretching the jaw-closing muscles evokes a reflex response with two major components. The short-latency reflex is favoured when stretches are brisk, but slower stretches evoke an additional long-latency component. In the hand muscles, the long-latency response is transcortical: in the masticatory muscles, it is not. In addition to its role in servo-control of muscle length during chewing, the stretch reflex in the jaw-closing muscles maintains the vertical position of the mandible during vigorous head movements such as those that occur during running, jumping, hopping and other vigorous whole-body movements in which the head moves briskly up and down. This is an interesting model system in which to investigate stretch reflexes with natural stimuli under unrestrained, physiological conditions.     

Rhythmic performance during a whole body movement: dynamic analysis of force-time curves

The purpose of this study was to investigate rhythmic performance during two-legged hopping in place. In particular, it was tested whether (a) timing control is independent of force control, (b) a dynamic timer model explains rhythmic performance, and (c) it is a force related parameter that carries the timing information. Eleven participants performed two-legged hopping at their preferred hopping frequency (PHF) and at two hopping frequencies set by an external rhythmic stimulus as lower (LHF) and higher (HHF) than their PHF, respectively. A force plate was used to record the ground reaction force (GRF) time curves during two-legged hopping. The primary temporal and force related parameters determined from the GRF-time curves were the durations of the cycle of movement (t(cycle)), of the contact phase (t(contact)), of the flight phase (t(flight)), the magnitude of peak force (Fz(peak)) and the rate of peak force development (RFD). Control of t(cycle) was independent of force control as shown by the non-significant correlations between t(cycle) and the force parameters of the GRF-time curve. Lag 1 autocorrelations of t(cycle) were not significant in any of the HF, thereby a dynamic timer model is considered to explain the timing of t(cycle) during two-legged hopping. RFD varied more than any other GRF-time curve parameter, exhibited consistent significant strong correlations with the GRF-time curve parameters and significant negative lag 1 autocorrelations in PHF, thus, it was highlighted as the potent timing control parameter. Finally, we provide a practical application for the optimization of rhythmic performance.     

Electromyographic activity,H-reflex modulation and corticospinal input to forearm motoneurones during active and passive rhythmic movements

Four subjects produced coordinated movements, consisting of flexion and extension of the wrist in ipsilateral (right wrist only), contralateral (left wrist only), inphase (both wrists in flexion or both in extension) and antiphase (one wrist in flexion, the other in extension) conditions. Electromyographic (EMG) activity was recorded from right wrist flexor and extensor muscles. In one session, transcranial magnetic stimuli (TMS) of the left motor cortex, around threshold intensity, evoked short-latency responses in the right wrist extensors and flexors. In another session, the median nerve at the cubital fossa was stimulated to elicit an H-reflex in the right flexor carpi radialis (rFCR). A movement cycle was divided into 8 segments. In total, 10 identical stimuli were delivered during each segment in each condition, at two movement frequencies. The magnitude of the EMG reponses to TMS was modulated markedly during movements made in the ipsilateral condition, and in both bimanual conditions. EMG activity was greater, and motor-evoked potentials (MEPs) were larger in the antiphase condition than in the inphase condition. When the amplitudes of the MEPs were normalised with respect to background EMG, no significant differences between the bimanual conditions were obtained. For H-reflexes, significant differences between the two bimanual conditions were observed, suggesting differences in levels of excitability of the Ia afferent pathway. These differences were attributed to segmental input associated with changes in muscle length arising from limb movement, and upon descending input to the spinal cord, possibly mediated by Renshaw cell inhibition. During rhythmic passive movement of the right limb, H-reflexes were inhibited and MEPs potentiated in a cyclic fashion. Passive movement of the contralateral left limb resulted in inhibition of both responses.PsycINFO classification: 2330; 2530; 2540     

An alternative view of the concept of utilisation of elastic energy in human movement

It is widely accepted that the series elastic component (SEC) of muscles and tendons plays an important role in dynamic human movements. Many experiments seem to show that during a pre-stretch movement energy can be stored in the SEC which is re-used during the subsequent concentric contraction. Mechanical calculations were performed to calculate the capacity for muscles and tendons to store elastic energy. The storage of elastic energy in muscle tissue appears to be negligible. In tendons some energy can be stored but the total elastic capacity of the tendons of the lower extremities appears far too small to explain reported advantages of a pre-stretch during jumping and running.Based on literature concerning chemical change and enthalpy production during experiments on isolated muscles, a model is proposed which can explain the advantages of a preliminary counter movement on force and work output during the subsequent concentric contraction. The main advantage of a pre-stretch, as seen in movements like jumping, throwing and running, seems to be to prevent a waste of cross bridges at the onset of a contraction in taking up the slack of the muscle. The model can explain why the mechanical efficiency in running can be much higher than in cycling. A muscle which is stretched prior to concentric contraction can do more work at the same metabolic cost when compared with a concentric contraction without pre-stretch.     

Human locomotor adjustments during perturbed walking

The locomotor adjustment induced by step perturbation of human subjects walking on a treadmill was described by a quantitative analysis of the EMG activities of selected trunk and leg muscles and by rotations of leg joints. The role of the proprioceptive input in the EMG reaction was also evaluated. The perturbation was obtained by a rapid and unexpected increase of belt speed. The motor response showed the stereotyped characteristics of a motor automatism and was accomplished without affecting the basic motor pattern of the gait. The EMG adjustment showed short-latency reflex responses (40–60 msec) of muscles acting at the joints more directly affected by the perturbing stimulus. This result supports the hypothesis of a spinal neuronal mechanism involved in the rapid adjustment of gait. The activity of primary spindle afferents seems to play an important role in the production of the faster EMG responses.     

Rapid motor adaptations to subliminal frequency shifts during syncopated rhythmic sensorimotor synchronization

The synchronization of rhythmic arm movements to a syncopated metronome cue was studied in a step-change design whereby small tempo shifts were inserted at fixed time points into the metronome frequency. The cueing sequence involved three stimulus types: (1) target contact in synchrony with the metronome beats, (2) syncopated target contact midway in time between audible beats, and (3) syncopated target contact following either a +2% or -2% change in stimulus frequency. Analysis of normalized and aggregated data revealed that (1) during the syncopation condition the response period showed a rapid adaptation to the frequency-incremented stimulus period, (2) response period was less variable during syncopated movement, (3) mean synchronization error and variability, calculated during syncopation relative to the mathematical midpoint of the stimulus cycle, were reduced during syncopated movements, and (4) synchronization error following the frequency increment showed trends to return linearly to pre-increment values which was fully achieved in the -2% change condition only. The results suggest that frequency entrainment to stimulus period was possible during syncopated movement with the response and stimulus onsets 180 degrees out of phase. Most remarkably, 70-80% of the adaptation of the response period to the new stimulus period was immediately attained during the second half cycle of the syncopated movement. Finally, a mathematical model, based on recursion, was introduced that accurately modeled actual data as a function of the previous stimulus and response intervals and a weighted response of period error and synchronization error, which showed dominance of frequency entrainment over phase entrainment during rhythmic synchronization.     

Evidence for generalized motor programs using gait pattern analysis

Human intra limb gait kinematics were analyzed via statistical and structural pattern recognition methods to determine the role of relative timing of limb segments within and between modes of gait. Five experienced runners were filmed while walking (3-6 km/hour) and running (8-12 km/hour) on a motor driven treadmill. Kinematic data consisted of relative timing of the four phases of the Philippson step cycle and intersegmental limb trajectories, determined from angle-angle diagrams. Despite marked decreases in absolute time durations within gaits remained constant over the speeds which were studied. Although a 2-fold increase in locomotor speed occurred in walking and a 1.5-fold speed increase occurred within running, the percentage of time spent in each of the Philippson phases was not significantly changed. However, significant differences in the time percentages and sequences of the step cycle phases were found between walking and running. Correlations between limb segment trajectories occurring in the different gaits showed strong coherence for overall step cycle patterns, but within step cycle phases and across speeds, selective phases displayed little correspondence.     

Activity of wrist muscles elicited during imposed or voluntary movements about the elbow joint

To examine the coordination of muscles during multijoint movement, we compared the response of wrist muscles to perturbations about the elbow joint with their activation during a volitional elbow movement. The purpose was to test the following two predictions: (a) Responses can occur in muscles not stretched by the perturbation, as has been reported for other multijoint systems; and (b) the motor pattern in response to a perturbation mimics an opposing volitional motor pattern across the two joints. We recorded the electromyographic (EMG) activity of elbow and wrist muscles as well as the flexion/extension motions at the elbow and wrist joints during individual trials that either involved a response to a torque perturbation that extended the elbow or required volitional elbow flexion. The results of this study confirmed that responses were elicited in the nonstretched wrist muscles when the elbow joint was perturbed. The same motor sequence of elbow and wrist flexors was present for both the volitional and perturbation task (with the forearm supinated), regardless of whether the wrist joint was immobilized or freely moving. The findings suggest that the nervous system relies on the purposeful coupling of elbow and wrist flexors to counter the inertial effects during the unrestricted voluntary movement, even though the coupling does not appear to be purposeful during the perturbation or with the wrist immobilized. The coupling of elbow and wrist flexors, however, was not rigidly fixed, as evidenced by muscle onsets that adapted over repeated perturbation trials and a reversal of the wrist muscle activated (wrist extensor) when the forearm was pronated. Hence, the coupling of muscle activities can be modified quantitatively when not beneficial and can be altered qualitatively with different initial configurations of the arm.     

Axial muscle activation provides stabilization against perturbations while running

Incidence of traumatic brain injury is an important hazard in sports and recreation. Unexpected (blind-sided) impacts with other players, obstacles, and the ground can be particularly dangerous. We believe this is partially due to the lack of muscular activation which would have otherwise provided protective bracing. In this study participants were asked to run on the treadmill while undergoing perturbations applied at the waist which pulled participants in the fore-aft and lateral directions. To determine the effect of unexpected impacts, participants were given a directional audio-visual warning 0.5 s prior to the perturbation in half of the trials and were unwarned in the other half of the trials. Perturbations were given during the start of the stance phase and during the start of the flight phase to examine two distinct points within the locomotor cycle. Muscle activity was monitored in axial muscles before, during, and after the perturbations were given. We hypothesized that the presence of a warning would allow for voluntary axial muscle activity prior to and during perturbations that would provide bracing of the body, and decreased displacement and acceleration of the head compared to unwarned perturbations. Our results indicate that when a warning is given prior to perturbation, the body was displaced significantly less, and the linear acceleration of the head was also significantly lessened in response to some perturbations. The perturbations given in this study caused significant increases in axial muscle activity compared to activity present during control running. We found evidence that cervical and abdominal muscles increased activity in response to the warning and that typically the warned trials displayed a lower reflexive muscle activity response. Additionally, we found a stronger effect of the warnings on muscle activity within the perturbations given during flight phase than those given at stance phase. Results from this study support the hypothesis that knowledge regarding an impending perturbation is used by the neuromuscular system to activate relevant core musculature and provide bracing to the athlete.     

Longitudinal Development of the Automatic Postural Response in Infants

In this longitudinal study, the development of automatic postural responses elicited during stance following perturbation of the support surface was investigated. Infants (N = 9) unable to stand without support were tested initially: follow-up tests were performed until the infants were able to stand and walk independently. Surface electromyographic recordings of leg and trunk muscle activity following a postural perturbation induced by a forward or backward translation of the support surface were made for each infant. Muscle onset latencies following the perturbation and the proportion of trials in which muscle activity was recorded were determined. First, infants activated appropriate muscles either in isolation or in pairs and then combined these muscles into functional synergies. Although activation of all three postural muscles was recorded in infants before they were able to stand and walk independently, the three-muscle response was not consistent in the youngest children. The proportion of trials eliciting muscle activity continued to increase (p <.O5) after infants began to walk independently, with postural muscle activity recorded in virtually every trial by late independent walking. Thus. the automatic postural response elicited during stance was shown to begin with activity in single or paired muscles, followed by activation of the postural muscles in functional synergies. These data illustrate the progressive development of an effective sensory-motor organization.     

Knee joint kinematics and neuromuscular responses in female athletes during and after multi-directional perturbations

The purpose of this study was to investigate weight-bearing knee joint kinematic and neuromuscular responses during lateral, posterior, rotational, and combination (simultaneous lateral, posterior, and rotational motions) perturbations and post-perturbations phases in 30° flexed-knee and straight-knee conditions. Thirteen healthy female athletes participated. Knee joint angles and muscle activity of vastus lateralis (VL), vastus medialis (VM), biceps femoris (BF), semitendinosus (ST), lateral gastrocnemius (LG), and medial gastrocnemius (MD) muscles were computed. Knee abducted during lateral perturbations, whereas it adducted during the other perturbations. It was internally rotated during flexed-knee and externally rotated during straight-knee perturbations and post-perturbations. VL and VM's mean and maximum activities during flexed-knee perturbations were greater than those of straight-knee condition. BF's mean activities were greater during flexed-knee perturbations compared with straight-knee condition, while its maximum activities observed during combination perturbations. ST's maximum activities during combination perturbations were greatest compared with the other perturbations. LG and MG's activities were greater during straight-knee conditions. Compared with the perturbation phase, the mean and maximum muscles' activities were significantly greater during post-perturbations. The time of onset of maximum muscle activity showed a distinctive pattern among the perturbations and phases. The perturbation direction is an important variable which induces individualized knee kinematic and neuromuscular response.     

The multimodality of infant's rhythmic movements as a modulator of the interaction with their caregivers

Children’s rhythmic movements during the first year of life possess a meaningful predictive validity for later communicative development. However, their role within adult-child interactions is still underexplored. In this study, we examined whether children’s rhythmic movements were significantly responded by adults and the role of multimodality and object use in this process. We observed 22 dyads of 9-month-olds and their parents in natural play interactions. Infants’ multimodal rhythmic movements increased the probability of adult responding. Adults offered different types of responses and significantly followed the child’s focus of attention. These dynamics could support communicative development by promoting joint attention frameworks.     

An Energetic Comparison of Symmetrical and Asymmetrical Human Gait

This article contrasts the mechanical energy profiles of asymmetrical galloping with those of symmetrical running in adult humans. Seven female subjects were filmed while performing overground running and galloping at their preferred velocities. A previous study (Whitall & Caldwell, 1992) showed that kinematic differences between these gait modes included higher preferred velocity for running than galloping, with distinct differences in interlimb coordination but surprisingly similar intralimb patterns. Energetically, in the present study the whole body center of mass during galloping was found to behave much as it does in walking; kinetic and potential energy profiles were out of phase, as compared with running, which exhibited in-phase fluctuations of kinetic and potential energies. The primary reason for these center of mass differences was found in the energetics of the back leg of galloping, which demonstrated alterations in timing of its energy fluctuations and less energy generation than the front leg. Analysis of the power sources underlying the segmental energies during swing phase showed that the back leg's energy changes were accomplished mainly through reduced use of the hip muscles and less interlimb energy transfer. The back leg's energetics during swing also displayed a shift toward greater reliance on nonmuscular energy sources. A pattern of energy inflow during early swing and energy outflow during late swing was common to both running and galloping, although the galloping legs both demonstrated more abrupt transitions between these phases. The possibility is raised that the 67/33 interlimb phasing ratio used in galloping is selected to reduce mechanical energy variations of the total body center of mass. These data suggest that models of asymmetric gait in humans must account for more than merely phase alteration.     

Review of first trial responses in balance control: influence of vestibular loss and Parkinson's disease

The reaction to an unexpected balance disturbance is unpractised, often startling and frequently associated with falls. This everyday situation can be reproduced in an experimental setting by exposing standing humans to sudden, unexpected and controlled movements of a support surface. In this review, we focus on the responses to the very first balance perturbation, the so-called first trial reactions (FTRs). Detailed analysis of FTRs may have important implications, both for clinical practice (providing new insights into the pathophysiological mechanisms underlying accidental falls in real life) and for understanding human physiology (what triggers and mediates these FTRs, and what is the relation to startle responses?). Several aspects of the FTRs have become clear. FTRs are characterized by an exaggerated postural reaction, with large EMG responses and co-contracting muscles in multiple body segments. This balance reaction is associated with marked postural instability (greater body sway to the perturbation). When the same perturbation is repeated, the size of the postural response habituates and the instability disappears. Other issues about FTRs remain largely unresolved, and these are addressed here. First, the functional role of FTRs is discussed. It appears that FTRs produce primarily increased trunk flexion during the multi-segmental response to postural perturbations, thus producing instability. Second, we consider which sensory signals trigger and modulate FTRs, placing specific emphasis on the role of vestibular signals. Surprisingly, vestibular signals appear to have no triggering role, but vestibular loss leads to excessive upper body FTRs due to loss of the normal modulatory influence. Third, we address the question whether startle-like responses are contributing to FTRs triggered by proprioceptive signals. We explain why this issue is still unresolved, mainly because of methodological difficulties involved in separating FTRs from ‘pure’ startle responses. Fourth, we review new work about the influence of perturbation direction on FTRs. Recent work from our group shows that the largest FTRs are obtained for toe-up support surface rotations which perturb the COM in the posterior direction. This direction corresponds to the directional preponderance for falls seen both in the balance laboratory and in daily life. Finally, we briefly touch upon clinical diagnostic issues, addressing whether FTRs (as opposed to habituated responses) could provide a more ecologically valid perspective of postural instability in patients compared to healthy subjects. We conclude that FTRs are an important source of information about human balance performance, both in health and disease. Future studies should no longer discard FTRs, but routinely include these in their analyses. Particular emphasis should be placed on the link between FTRs and everyday balance performance (including falls), and on the possible role played by startle reactions in triggering or modulating FTRs.     

Effects of walking on various inclines on EMG patterns of lower limb muscles in humans

Myoelectric signals from several muscles of the lower limb were studied during treadmill locomotion over various inclines. A pattern recognition technique was used to analyse these activity patterns. The analyses revealed the following rules. These are common features among the various muscle activity patterns. The results suggest that the limb is controlled as a unit. Both phasic and average components of the muscle activity patterns are modulated to meet demands imposed by the various inclines. The distal muscles in general are more tightly controlled than the proximal muscles. The changes in average EMG values are muscle-specific, and are not similar for the stance and swing phases of the step cycle. On average, the proximal muscles show greater increases than the distal muscles. These results are compared with those found previously in the different speed and stride-length condition. Studies such as these shed light on the adaptability of the basic locomotor synergy.     

Chaos in Human Rhythmic Movement

Rhythmic movements typical of locomotory actions are usually modeled as limit cycle dynamics, and their deviations from pure periodicity are attributed to stochastic physiological noise. In the present study, the dynamics of human rhythmic movements were found to contain more than the 2 dynamically active variables expected from limit cycle dynamics; the number depended upon the size of the limb oscillator. Observed positive Lyapunov exponents and fractal attractor dimensions indicated that the gross variability of human rhythmic movements may stem largely from low-dimensional chaotic motion on strange attractors.     

An analysis of air-stepping in normal infant vervet monkeys

Limb movements during air-stepping were analyzed in three neonatal vervet monkeys over a three-week period. The movements had similar temporal organization both across animals and across time. For example, the duration of both the hind and the forelimb cycle equaled about 500 ms, with hind limb return strokes lasting much longer than the hind limb power strokes. Furthermore, there were clear indications of both intra- and interlimb coordination. Specifically, all the joints of a limb tended to flex and extend simultaneously, and contralateral and ipsilateral limb pairs had an average phase relationship of approximately 50% of cycle duration. Despite a qualitative similarity between limb movements during air-stepping in the neonates and overground locomotion in older animals, there were notable differences both in temporal relationships and joint displacement patterns. Finally, there appeared to be important similarities between air-stepping in these monkeys and stepping in newborn humans. Most notably, both tended to disappear after a limited period. The implications of these similarities, as well as the overall results, are discussed in relation to the understanding of the development of locomotor behavior in human and nonhuman primates, using approaches based both upon the hard-wired and dynamic models.