Distinct locomotor precursors in newborn babies.

Mature locomotion involves modular spinal drives generating a set of fundamental patterns of motoneuron activation, each timed at a specific phase of locomotor cycles and associated with a stable muscle synergy. How locomotor modules develop and to what extent they depend on prior experience or intrinsic programs remains unclear. To address these issues, we herein leverage the presence at birth of two types of locomotor-like movements, spontaneous kicking and weight-bearing stepping. The former is expressed thousands of times in utero and postnatally, whereas the latter is elicited de novo by placing the newborn on the ground for the first time. We found that the neuromuscular modules of stepping and kicking differ substantially. Neonates kicked with an adult-like number of temporal activation patterns, which lacked a stable association with systematic muscle synergies across movements. However, on the ground neonates stepped with fewer temporal patterns but all structured in stable synergies. Since kicking and ground-stepping coexist at birth, switching between the two behaviors may depend on a dynamic reconfiguration of the underlying neural circuits as a function of sensory feedback from surface contact. We tracked the development of ground-stepping in 4- to 48-mo-old infants and found that, after the age of 6 mo, the number of temporal patterns increased progressively, reaching adult-like conformation only after independent walking was established. We surmise that mature locomotor modules may derive by combining the multiple patterns of repeated kicking, on the one hand, with synergies resulting from fractionation of those revealed by sporadic weight-bearing stepping, on the other hand.

Evaluation of Spatiotemporal Patterns of the Spinal Muscle Coordination Output during Walking in the Exoskeleton.

Recent advances in the performance and evaluation of walking in exoskeletons use various assessments based on kinematic/kinetic measurements. While such variables provide general characteristics of gait performance, only limited conclusions can be made about the neural control strategies. Moreover, some kinematic or kinetic parameters are a consequence of the control implemented on the exoskeleton. Therefore, standard indicators based on kinematic variables have limitations and need to be complemented by performance measures of muscle coordination and control strategy. Knowledge about what happens at the spinal cord output level might also be critical for rehabilitation since an abnormal spatiotemporal integration of activity in specific spinal segments may result in a risk for abnormalities in gait recovery. Here we present the PEPATO software, which is a benchmarking solution to assess changes in the spinal locomotor output during walking in the exoskeleton with respect to reference data on normal walking. In particular, functional and structural changes at the spinal cord level can be mapped into muscle synergies and spinal maps of motoneuron activity. A user-friendly software interface guides the user through several data processing steps leading to a set of performance indicators as output. We present an example of the usage of this software for evaluating walking in an unloading exoskeleton that allows a person to step in simulated reduced (the Moon's) gravity. By analyzing the EMG activity from lower limb muscles, the algorithms detected several performance indicators demonstrating differential adaptation (shifts in the center of activity, prolonged activation) of specific muscle activation modules and spinal motor pools and increased coactivation of lumbar and sacral segments. The software is integrated at EUROBENCH facilities to benchmark the performance of walking in the exoskeleton from the point of view of changes in the spinal locomotor output.

Backward walking highlights gait asymmetries in children with cerebral palsy.

To investigate how early injuries to developing motor regions of the brain affect different forms of gait, we compared the spatiotemporal locomotor patterns during forward (FW) and backward (BW) walking in children with cerebral palsy (CP). Bilateral gait kinematics and EMG activity of 11 pairs of leg muscles were recorded in 14 children with CP (9 diplegic, 5 hemiplegic; 3.0-11.1 yr) and 14 typically developing (TD) children (3.3-11.8 yr). During BW, children with CP showed a significant increase of gait asymmetry in foot trajectory characteristics and limb intersegmental coordination. Furthermore, gait asymmetries, which were not evident during FW in diplegic children, became evident during BW. Factorization of the EMG signals revealed a comparable structure of the motor output during FW and BW in all groups of children, but we found differences in the basic temporal activation patterns. Overall, the results are consistent with the idea that both forms of gait share pattern generation control circuits providing similar (though reversed) kinematic patterns. However, BW requires different muscle activation timings associated with muscle modules, highlighting subtle gait asymmetries in diplegic children, and thus provides a more comprehensive assessment of gait pathology in children with CP. The findings suggest that spatiotemporal asymmetry assessments during BW might reflect an impaired state and/or descending control of the spinal locomotor circuitry and can be used for diagnostic purposes and as complementary markers of gait recovery. NEW & NOTEWORTHY Early injuries to developing motor regions of the brain affect both forward progression and other forms of gait. In particular, backward walking highlights prominent gait asymmetries in children with hemiplegia and diplegia from cerebral palsy and can give a more comprehensive assessment of gait pathology. The observed spatiotemporal asymmetry assessments may reflect both impaired supraspinal control and impaired state of the spinal circuitry.

Changes in the spinal segmental motor output for stepping during development from infant to adult.

Human stepping movements emerge in utero and show several milestones during development to independent walking. Recently, imaging has become an essential tool for investigating the development and function of pattern generation networks in the spinal cord. Here we examine the development of the spinal segmental output by mapping the distribution of motoneuron activity in the lumbosacral spinal cord during stepping in newborns, toddlers, preschoolers, and adults. Newborn stepping is characterized by an alternating bilateral motor output with only two major components that are active at all lumbosacral levels of the spinal cord. This feature was similar across different cycle durations of neonate stepping. The alternating spinal motor output is consistent with a simpler organization of neuronal networks in neonates. Furthermore, a remarkable feature of newborn stepping is a higher overall activation of lumbar versus sacral segments, consistent with a rostrocaudal excitability gradient. In toddlers, the stance-related motor pool activity migrates to the sacral cord segments, while the lumbar motoneurons are separately activated at touchdown. In the adult, the lumbar and sacral patterns become more dissociated with shorter activation times. We conclude that the development of human locomotion from the neonate to the adult starts from a rostrocaudal excitability gradient and involves a gradual functional reorganization of the pattern generation circuitry.

Function dictates the phase dependence of vision during human locomotion.

In human and animal locomotion, sensory input is thought to be processed in a phase-dependent manner. Here we use full-field transient visual scene motion toward or away from subjects walking on a treadmill. Perturbations were presented at three phases of walking to test 1) whether phase dependence is observed for visual input and 2) whether the nature of phase dependence differs across body segments. Results demonstrated that trunk responses to approaching perturbations were only weakly phase dependent and instead depended primarily on the delay from the perturbation. Recording of kinematic and muscle responses from both right and left lower limb allowed the analysis of six distinct phases of perturbation effects. In contrast to the trunk, leg responses were strongly phase dependent. Leg responses during the same gait cycle as the perturbation exhibited gating, occurring only when perturbations were applied in midstance. In contrast, during the postperturbation gait cycle, leg responses occurred at similar response phases of the gait cycle over a range of perturbation phases. These distinct responses reflect modulation of trunk orientation for upright equilibrium and modulation of leg segments for both hazard accommodation/avoidance and positional maintenance on the treadmill. Overall, these results support the idea that the phase dependence of responses to visual scene motion is determined by different functional tasks during walking.

Development of running is not related to time since onset of independent walking, a longitudinal case study.

Introduction: Children start to run after they master walking. How running develops, however, is largely unknown. Methods: We assessed the maturity of running pattern in two very young, typically developing children in a longitudinal design spanning about three years. Leg and trunk 3D kinematics and electromyography collected in six recording sessions, with more than a hundred strides each, entered our analysis. We recorded walking during the first session (the session of the first independent steps of the two toddlers at the age of 11.9 and 10.6 months) and fast walking or running for the subsequent sessions. More than 100 kinematic and neuromuscular parameters were determined for each session and stride. The equivalent data of five young adults served to define mature running. After dimensionality reduction using principal component analysis, hierarchical cluster analysis based on the average pairwise correlation distance to the adult running cluster served as a measure for maturity of the running pattern. Results: Both children developed running. Yet, in one of them the running pattern did not reach maturity whereas in the other it did. As expected, mature running appeared in later sessions (>13 months after the onset of independent walking). Interestingly, mature running alternated with episodes of immature running within sessions. Our clustering approach separated them. Discussion: An additional analysis of the accompanying muscle synergies revealed that the participant who did not reach mature running had more differences in muscle contraction when compared to adults than the other. One may speculate that this difference in muscle activity may have caused the difference in running pattern.

Comparison of the forward and sideways locomotor patterns in children with Cerebral Palsy.

Switching locomotion direction is a common task in daily life, and it has been studied extensively in healthy people. Little is known, however, about the locomotor adjustments involved in changing locomotion direction from forward (FW) to sideways (SW) in children with cerebral palsy (CP). The importance of testing the ability of children with CP in this task lies in the assessment of flexible, adaptable adjustments of locomotion as a function of the environmental context. On the one hand, the ability of a child to cope with novel task requirements may provide prognostic cues as to the chances of modifying the gait adaptively. On the other hand, challenging the child with the novel task may represent a useful rehabilitation tool to improve the locomotor performance. SW is an asymmetrical locomotor task and requires a differential control of right and left limb muscles. Here, we report the results of a cross-sectional study comparing FW and SW in 27 children with CP (17 diplegic, 10 hemiplegic, 2-10 years) and 18 age-matched typically developing (TD) children. We analyzed gait kinematics, joint moments, EMG activity of 12 pairs of bilateral muscles, and muscle modules evaluated by factorization of EMG signals. Task performance in several children with CP differed drastically from that of TD children. Only 2/3 of children with CP met the primary outcome, i.e. they succeeded to step sideways, and they often demonstrated attempts to step forward. They tended to rotate their trunk FW, cross one leg over the other, flex the knee and hip. Moreover, in contrast to TD children, children with CP often exhibited similar motor modules for FW and SW. Overall, the results reflect developmental deficits in the control of gait, bilateral coordination and adjustment of basic motor modules in children with CP. We suggest that the sideways (along with the backward) style of locomotion represents a novel rehabilitation protocol that challenges the child to cope with novel contextual requirements.

Complexity of modular neuromuscular control increases and variability decreases during human locomotor development.

When does modular control of locomotion emerge during human development? One view is that modularity is not innate, being learnt over several months of experience. Alternatively, the basic motor modules are present at birth, but are subsequently reconfigured due to changing brain-body-environment interactions. One problem in identifying modular structures in stepping infants is the presence of noise. Here, using both simulated and experimental muscle activity data from stepping neonates, infants, preschoolers, and adults, we dissect the influence of noise, and identify modular structures in all individuals, including neonates. Complexity of modularity increases from the neonatal stage to adulthood at multiple levels of the motor infrastructure, from the intrinsic rhythmicity measured at the level of individual muscles activities, to the level of muscle synergies and of bilateral intermuscular network connectivity. Low complexity and high variability of neuromuscular signals attest neonatal immaturity, but they also involve potential benefits for learning locomotor tasks.

Smooth changes in the EMG patterns during gait transitions under body weight unloading.

During gradual speed changes, humans exhibit a sudden discontinuous switch from walking to running at a specific speed, and it has been suggested that different gaits may be associated with different functioning of neuronal networks. In this study we recorded the EMG activity of leg muscles at slow increments and decrements in treadmill belt speed and at different levels of body weight unloading. In contrast to normal walking at 1 g, at lower levels of simulated gravity (<0.4 g) the transition between walking and running was generally gradual, without systematic abrupt changes in either intensity or timing of EMG patterns. This phenomenon depended to a limited extent on the gravity simulation technique, although the exact level of the appearance of smooth transitions (0.4-0.6 g) tended to be lower for the vertical than for the tilted body weight support system. Furthermore, simulations performed with a half-center oscillator neuromechanical model showed that the abruptness of motor patterns at gait transitions at 1 g could be predicted from the distinct parameters anchored already in the normal range of walking and running speeds, whereas at low gravity levels the parameters of the model were similar for the two human gaits. A lack of discontinuous changes in the pattern of speed-dependent locomotor characteristics in a hypogravity environment is consistent with the idea of a continuous shift in the state of a given set of central pattern generators, rather than the activation of a separate set of central pattern generators for each distinct gait.

Age-related changes in the neuromuscular control of forward and backward locomotion.

Previous studies found significant modification in spatiotemporal parameters of backward walking in healthy older adults, but the age-related changes in the neuromuscular control have been considered to a lesser extent. The present study compared the intersegmental coordination, muscle activity and corresponding modifications of spinal montoneuronal output during both forward and backward walking in young and older adults. Ten older and ten young adults walked forward and backward on a treadmill at different speeds. Gait kinematics and EMG activity of 14 unilateral lower-limb muscles were recorded. As compared to young adults, the older ones used shorter steps, a more in-phase shank and foot motion, and the activity profiles of muscles innervated from the sacral segments were significantly wider in each walking condition. These findings highlight age-related changes in the neuromuscular control of both forward and backward walking. A striking feature of backward walking was the differential organization of the spinal output as compared to forward gait. In addition, the resulting spatiotemporal map patterns also characterized age-related changes of gait. Finally, modifications of the intersegmental coordination with aging were greater during backward walking. On the whole, the assessment of backward walk in addition to routine forward walk may help identifying or unmasking neuromuscular adjustments of gait to aging.

Neuromuscular Age-Related Adjustment of Gait When Moving Upwards and Downwards.

Locomotor movements are accommodated to various surface conditions by means of specific locomotor adjustments. This study examined underlying age-related differences in neuromuscular control during level walking and on a positive or negative slope, and during stepping upstairs and downstairs. Ten elderly and eight young adults walked on a treadmill at two different speeds and at three different inclinations (0°, +6°, and -6°). They were also asked to ascend and descend stairs at self-selected speeds. Full body kinematics and surface electromyography of 12 lower-limb muscles were recorded. We compared the intersegmental coordination, muscle activity, and corresponding modifications of spinal motoneuronal output in young and older adults. Despite great similarity between the neuromuscular control of young and older adults, our findings highlight subtle age-related differences in all conditions, potentially reflecting systematic age-related adjustments of the neuromuscular control of locomotion across various support surfaces. The main distinctive feature of walking in older adults is a significantly wider and earlier activation of muscles innervated by the sacral segments. These changes in neuromuscular control are reflected in a reduction or lack of propulsion observed at the end of stance in older adults at different slopes, with the result of a delay in the timing of redirection of the centre-of-mass velocity and of an unanticipated step-to-step transition strategy.

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.

Migration of motor pool activity in the spinal cord reflects body mechanics in human locomotion.

During the evolution of bipedal modes of locomotion, a sequential rostrocaudal activation of trunk muscles due to the undulatory body movements was replaced by more complex and discrete bursts of activity. Nevertheless, the capacity for segmental rhythmogenesis and the rostrocaudal propagation of spinal cord activity has been conserved. In humans, motoneurons of different muscles are arranged in columns, with a specific grouping of muscles at any given segmental level. The muscle patterns of locomotor activity and the biomechanics of the body center of mass have been studied extensively, but their interrelationship remains poorly understood. Here we mapped the electromyographic activity recorded from 30 bilateral leg muscles onto the spinal cord in approximate rostrocaudal locations of the motoneuron pools during walking and running in humans. We found that the rostrocaudal displacements of the center of bilateral motoneuron activity mirrored the changes in the energy due to the center-of-body mass motion. The results suggest that biomechanical mechanisms of locomotion, such as the inverted pendulum in walking and the pogo-stick bouncing in running, may be tightly correlated with specific modes of progression of motor pool activity rostrocaudally in the spinal cord.

Kinematic strategies in newly walking toddlers stepping over different support surfaces.

In adults, locomotor movements are accommodated to various support surface conditions by means of specific anticipatory locomotor adjustments and changes in the intersegmental coordination. Here we studied the kinematic strategies of toddlers at the onset of independent walking when negotiating various support surface conditions: stepping over an obstacle, walking on an inclined surface, and on a staircase. Generally, toddlers could perform these tasks only when supported by the arm. They exhibited strategies very different from those of the adults. Although adults maintained walking speed roughly constant, toddlers markedly accelerated when walking downhill or downstairs and decelerated when walking uphill or upstairs. Their coordination pattern of thigh-shank-foot elevation angles exhibited greater inter-trial variability than that in adults, but it did not undergo the systematic change as a function of task that was present in adults. Thus the intersegmental covariance plane rotated across tasks in adults, whereas its orientation remained roughly constant in toddlers. In contrast with the adults, the toddlers often tended to place the foot onto the obstacle or across the edges of the stairs. We interpret such foot placements as part of a haptic exploratory repertoire and we argue that the maintenance of a roughly constant planar covariance--irrespective of the surface inclination and height--may be functional to the exploratory behavior. The latter notion is consistent with the hypothesis proposed decades ago by Bernstein that, when humans start to learn a skill, they may restrict the number of degrees of freedom to reduce the size of the search space and simplify the coordination.

The many roles of vision during walking.

Vision can improve bipedal upright stability during standing and locomotion. However, during locomotion, vision supports additional behaviors such as gait cycle modulation, navigation, and obstacle avoidance. Here, we investigate how the multiple roles of vision are reflected in the dynamics of trunk control as the neural control problem changes from a fixed to a moving base of support. Subjects were presented with either low- or high-amplitude broadband visual stimuli during standing posture or while walking on a treadmill at 1 km/h and 5 km/h. Frequency response functions between visual scene motion (input) and trunk kinematics (output) revealed little or no change in the gain of trunk orientation in the standing posture and walking conditions. However, a dramatic increase in gain was observed in trunk (hip and shoulder) horizontal displacement from posture to locomotion. Such increases in gain may be interpreted as an increased coupling to visual scene motion. However, we believe that the increased gain reflects a decrease in stability due to a change of the control problem from standing to locomotion. Indeed, keeping the body upright with the use of vision during walking is complicated by the additional locomotor processes at work. Unlike during standing, vision plays many roles during locomotion, providing information for upright stability as well as body position relative to the external environment.

Emergence of Different Gaits in Infancy: Relationship Between Developing Neural Circuitries and Changing Biomechanics.

How does gait-specific pattern generation evolve in early infancy? The idea that neural and biomechanical mechanisms underlying mature walking and running differ to some extent and involve distinct spinal and supraspinal neural circuits is supported by various studies. Here we consider the issue of human gaits from the developmental point of view, from neonate stepping to adult mature gaits. While differentiating features of the walk and run are clearly distinct in adults, the gradual and progressive developmental bifurcation between the different gaits suggests considerable sharing of circuitry. Gaits development and their biomechanical determinants also depend on maturation of the musculoskeletal system. This review outlines the possible overlap in the neural and biomechanical control of walking and running in infancy, supporting the idea that gaits may be built starting from common, likely phylogenetically conserved elements. Bridging connections between movement mechanics and neural control of locomotion could have profound clinical implications for technological solutions to understand better locomotor development and to diagnose early motor deficits. We also consider the neuromuscular maturation time frame of gaits resulting from active practice of locomotion, underlying plasticity of development.

Maturation of the Locomotor Circuitry in Children With Cerebral Palsy.

The first years of life represent an important phase of maturation of the central nervous system, processing of sensory information, posture control and acquisition of the locomotor function. Cerebral palsy (CP) is the most common group of motor disorders in childhood attributed to disturbances in the fetal or infant brain, frequently resulting in impaired gait. Here we will consider various findings about functional maturation of the locomotor output in early infancy, and how much the dysfunction of gait in children with CP can be related to spinal neuronal networks vs. supraspinal dysfunction. A better knowledge about pattern generation circuitries in infancy may improve our understanding of developmental motor disorders, highlighting the necessity for regulating the functional properties of abnormally developed neuronal locomotor networks as a target for early sensorimotor rehabilitation. Various clinical approaches and advances in biotechnology are also considered that might promote acquisition of the locomotor function in infants at risk for locomotor delays.

Clinical Relevance of State-of-the-Art Analysis of Surface Electromyography in Cerebral Palsy.

Surface electromyography (sEMG) can be used to assess the integrity of the neuromuscular system and its impairment in neurological disorders. Here we will consider several issues related to the current clinical applications, difficulties and limited usage of sEMG for the assessment and rehabilitation of children with cerebral palsy. The uniqueness of this methodology is that it can determine hyperactivity or inactivity of selected muscles, which cannot be assessed by other methods. In addition, it can assist for intervention or muscle/tendon surgery acts, and it can evaluate integrated functioning of the nervous system based on multi-muscle sEMG recordings and assess motor pool activation. The latter aspect is especially important for understanding impairments of the mechanisms of neural controllers rather than malfunction of individual muscles. Although sEMG study is an important tool in both clinical research and neurorehabilitation, the results of a survey on the clinical relevance of sEMG in a typical department of pediatric rehabilitation highlighted its limited clinical usage. We believe that this is due to limited knowledge of the sEMG and its neuromuscular underpinnings by many physiotherapists, as a result of lack of emphasis on this important methodology in the courses taught in physical therapy schools. The lack of reference databases or benchmarking software for sEMG analysis may also contribute to the limited clinical usage. Despite the existence of educational and technical barriers to a widespread use of, sEMG does provide important tools for planning and assessment of rehabilitation treatments for children with cerebral palsy.

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.

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 (approximately 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.