Yuri P. Ivanenko

Five basic muscle activation patterns account for muscle activity during human locomotion

An electromyographic (EMG) activity pattern for individual muscles in the gait cycle exhibits a great deal of intersubject, intermuscle and context‐dependent variability. Here we examined the issue of common underlying patterns by applying factor analysis to the set of EMG records obtained at different walking speeds and gravitational loads. To this end healthy subjects were asked to walk on a treadmill at speeds of 1, 2, 3 and 5kmh−1 as well as when 35–95% of the body weight was supported using a harness. We recorded from 12–16 ipsilateral leg and trunk muscles using both surface and intramuscular recording and determined the average, normalized EMG of each record for 10–15 consecutive step cycles. We identified five basic underlying factors or component waveforms that can account for about 90% of the total waveform variance across different muscles during normal gait. Furthermore, while activation patterns of individual muscles could vary dramatically with speed and gravitational load, both the limb kinematics and the basic EMG components displayed only limited changes. Thus, we found a systematic phase shift of all five factors with speed in the same direction as the shift in the onset of the swing phase. This tendency for the factors to be timed according to the lift‐off event supports the idea that the origin of the gait cycle generation is the propulsion rather than heel strike event. The basic invariance of the factors with walking speed and with body weight unloading implies that a few oscillating circuits drive the active muscles to produce the locomotion kinematics. A flexible and dynamic distribution of these basic components to the muscles may result from various descending and proprioceptive signals that depend on the kinematic and kinetic demands of the movements.

Locomotor Primitives in Newborn Babies and Their Development

Mammalian locomotion patterns share common roots. How rudimentary movements evolve into sophisticated ones during development remains unclear. It is often assumed that the primitive patterns of neural control are suppressed during development, replaced by entirely new patterns. Here we identified the basic patterns of lumbosacral motoneuron activity from multimuscle recordings in stepping neonates, toddlers, preschoolers, and adults. Surprisingly, we found that the two basic patterns of stepping neonates are retained through development, augmented by two new patterns first revealed in toddlers. Markedly similar patterns were observed also in the rat, cat, macaque, and guineafowl, consistent with the hypothesis that, despite substantial phylogenetic distances and morphological differences, locomotion in several animal species is built starting from common primitives, perhaps related to a common ancestral neural network.

Coordination of Locomotion with Voluntary Movements in Humans

Muscle activity occurring during human locomotion can be accounted for by five basic temporal activation patterns in a variety of locomotion conditions. Here, we examined how these activation patterns interact with muscle activity required for a voluntary movement. Subjects produced a voluntary movement during locomotion, and we examined the resulting kinematics, kinetics, and EMG activity in 16-31 ipsilateral limb and trunk muscles during the tasks. There were four voluntary tasks added to overground walking (∼5 km/h) in which subjects kicked a ball, stepped over an obstacle, or reached down and grasped an object on the floor (weight support on either the right or the left foot). Statistical analyses of EMG waveforms showed that the five basic locomotion patterns were invariantly present in each task, although they could be differently weighted across muscles, suggesting a characteristic locomotion timing of muscle activations. We also observed a separate activation that was timed to the voluntary task. The coordination of locomotion with the voluntary task was accomplished by combining activation timings that were associated separately with the voluntary task and locomotion. Activation associated with the voluntary tasks was either synchronous with the timing for locomotion or had additional activations not represented in the basic locomotion timing. We propose that this superposition of an invariant locomotion timing pattern with a voluntary activation timing may be consistent with the proposal suggesting that compound movements are produced through a superposition of motor programs.

Motor Control Programs and Walking

The question of how the central nervous system coordinates muscle activity is central to an understanding of motor control. The authors argue that motor programs may be considered as a characteristic timing of muscle activations linked to specific kinematic events. In particular, muscle activity occurring during human locomotion can be accounted for by five basic temporal components in a variety of locomotion conditions. Spatiotemporal maps of spinal cord motoneuron activation also show discrete periods of activity. Furthermore, the coordination of locomotion with voluntary tasks is accomplished through a superposition of motor programs or activation timings that are separately associated with each task. As a consequence, the selection of muscle synergies appears to be downstream from the processes that generate activation timings.

Patterned control of human locomotion

Abstract  There is much experimental evidence for the existence of biomechanical constraints which simplify the problem of control of multi‐segment movements. In addition, it has been hypothesized that movements are controlled using a small set of basic temporal components or activation patterns, shared by several different muscles and reflecting global kinematic and kinetic goals. Here we review recent studies on human locomotion showing that muscle activity is accounted for by a combination of few basic patterns, each one timed at a different phase of the gait cycle. Similar patterns are involved in walking and running at different speeds, walking forwards or backwards, and walking under different loading conditions. The corresponding weights of distribution to different muscles may change as a function of the condition, allowing highly flexible control. Biomechanical correlates of each activation pattern have been described, leading to the hypothesis that the co‐ordination of limb and body segments arises from the coupling of neural oscillators between each other and with limb mechanical oscillators. Muscle activations need only intervene during limited time epochs to force intrinsic oscillations of the system when energy is lost.

Modular Control of Limb Movements during Human Locomotion

The idea that the CNS may control complex interactions by modular decomposition has received considerable attention. We explored this idea for human locomotion by examining limb kinematics. The coordination of limb segments during human locomotion has been shown to follow a planar law for walking at different speeds, directions, and levels of body unloading. We compared the coordination for different gaits. Eight subjects were asked to walk and run on a treadmill at different speeds or to walk, run, and hop over ground at a preferred speed. To explore various constraints on limb movements, we also recorded stepping over an obstacle, walking with the knees flexed, and air-stepping with body weight support. We found little difference among covariance planes that depended on speed, but there were differences that depended on gait. In each case, we could fit the planar trajectories with a weighted sum of the limb length and orientation trajectories. This suggested that limb length and orientation might provide independent predictors of limb coordination. We tested this further by having the subjects step, run, and hop in place, thereby varying only limb length and maintaining limb orientation fixed, and also by marching with knees locked to maintain limb length constant while varying orientation. The results were consistent with a modular control of limb kinematics where limb movements result from a superposition of separate length- and orientation-related angular covariance. The hypothesis finds support in the animal findings that limb proprioception may also be encoded in terms of these global limb parameters.

Impulses of activation but not motor modules are preserved in the locomotion of subacute stroke patients

It has been hypothesized that the coordinated activation of muscles is controlled by the central nervous system by means of a small alphabet of control signals (also referred to as activation signals) and motor modules (synergies). We analyzed the locomotion of 10 patients recently affected by stroke (maximum of 20 wk) and compared it with that of healthy controls. The aim was to assess whether the walking of subacute stroke patients is based on the same motor modules and/or activation signals as healthy subjects. The activity of muscles of the lower and upper limb and the trunk was measured and used for extracting motor modules. Four modules were sufficient to explain the majority of variance in muscle activation in both controls and patients. Modules from the affected side of stroke patients were different from those of healthy controls and from the unaffected side of stroke patients. However, the activation signals were similar between groups and between the affected and unaffected side of stroke patients, and were characterized by impulses at specific time instants within the gait cycle, underlying an impulsive controller of gait. In conclusion, motor modules observed in healthy subjects during locomotion are different from those used by subacute stroke patients, despite similar impulsive activation signals. We suggest that this pattern is consistent with a neuronal network in which the timing of activity generated by central pattern generators is directed to the motoneurons via a premotor network that distributes the activity in a task-dependent manner determined by sensory and descending control information.

Effect of gaze on postural responses to neck proprioceptive and vestibular stimulation in humans

1 We studied the effect of gaze orientation on postural responses evoked by vibration of neck dorsal muscles or by galvanic stimulation of the vestibular system during quiet standing in healthy humans. Various gaze orientations were obtained by different combinations of horizontal head‐on‐feet (−90, −45, 0, 45, 90 deg) and eye‐in‐orbit (−30, 0, 30 deg) positions. The instantaneous centre of foot pressure was recorded with a force platform. 2 With a symmetrical position of the vibrator relative to the spine, neck muscle vibration elicited a body sway in the direction of the head naso‐occipital axis when the eyes were aligned with it. The same result was obtained both during head rotations and when the head and trunk were rotated together. 3 For lateral eye deviations, the direction of the body sway was aligned with gaze orientation. The effect of gaze was present both with eyes open and eyes closed. After long‐lasting (1 min) lateral fixation of the target the effect of gaze decreased significantly. 4 Postural responses to galvanic vestibular stimulation tended to occur orthogonal to the head naso‐occipital axis (towards the anodal ear) but in eight of the 11 subjects the responses were also biased by the direction of gaze. 5 The prominent effect of gaze in reorienting automatic postural reactions indicates that both neck proprioceptive and vestibular stimuli are processed in the context of visual control of posture. The results point out the importance of a viewer‐centred frame of reference for processing multisensory information.

Kinematics in Newly Walking Toddlers Does Not Depend Upon Postural Stability

When a toddler starts to walk without support, gait kinematics and electromyographic (EMG) activity differ from those of older children and the body displays considerable oscillations due to poor equilibrium. Postural instability clearly affects motor patterns in adults, but does instability explain why toddlers walk with a different gait? Here we addressed this question by comparing kinematics and EMGs in toddlers performing their first independent steps with or without hand or trunk support. Hand support significantly improved postural stability and some general gait parameters, reducing percent of falls, step width, lateral hip deviations and trunk oscillations. However, the kinematic and EMG patterns were unaffected by increased postural stability. In particular, the co-variance of the angular motion of the lower limb segments, the pattern of bilateral coordination of the vertical movement of the two hip joints, high variability of the foot path, the elliptic or single peak trajectory of the foot in the swing phase, and characteristic EMG bursts at foot contact remained idiosyncratic of toddler locomotion. Instead the toddler pattern shared fundamental features with adult stepping in place, suggesting that toddlers implement a mixed locomotor strategy, combining forward progression with elements of stepping in place. Furthermore, gait kinematics remained basically unchanged until the occurrence of the first unsupported steps and rapidly matured thereafter. We conclude that idiosyncratic features in newly walking toddlers do not simply result from undeveloped balance control but may represent an innate kinematic template of stepping.

Motor Patterns During Walking on a Slippery Walkway

Friction and gravity represent two basic physical constraints of terrestrial locomotion that affect both motor patterns and the biomechanics of bipedal gait. To provide insights into the spatiotemporal organization of the motor output in connection with ground contact forces, we studied adaptation of human gait to steady low-friction conditions. Subjects walked along a slippery walkway (7 m long; friction coefficient approximately 0.06) or a normal, nonslippery floor at a natural speed. We recorded gait kinematics, ground reaction forces, and bilateral electromyographic (EMG) activity of 16 leg and trunk muscles and we mapped the recorded EMG patterns onto the spinal cord in approximate rostrocaudal locations of the motoneuron (MN) pools to characterize the spatiotemporal organization of the motor output. The results revealed several idiosyncratic features of walking on the slippery surface. The step length, cycle duration, and horizontal shear forces were significantly smaller, the head orientation tended to be stabilized in space, whereas arm movements, trunk rotations, and lateral trunk inclinations considerably increased and foot motion and gait kinematics resembled those of a nonplantigrade gait. Furthermore, walking on the slippery surface required stabilization of the hip and of the center-of-body mass in the frontal plane, which significantly improved with practice. Motor patterns were characterized by an enhanced (roughly twofold) level of MN activity, substantial decoupling of anatomical synergists, and the absence of systematic displacements of the center of MN activity in the lumbosacral enlargement. Overall, the results show that when subjects are confronted with unsteady surface conditions, like the slippery floor, they adopt a gait mode that tends to keep the COM centered over the supporting limbs and to increase limb stiffness. We suggest that this behavior may represent a distinct gait mode that is particularly suited to uncertain surface conditions in general.