Effect of age and speed on the step-to-step transition strategies in children.

The development and acquisition of mature walking in children is multifactorial, depending among others on foot interaction with the ground, body dynamics and the knowledge of the 'rules' stemming from the gravity field. Indeed, each step the velocity of the centre of mass must be redirected upwards. This redirection may be initiated by the trailing leg, propulsing forward and upward the body before foot contact, or later by the loading limb after the contact with the ground. While it has been suggested that mature walking develops slowly from first independent steps to about 7 years of age, it is still unknown how children acquire the appropriate loading and propulsion forces during the step-to-step transition. To answer that question, twenty-four children (from 3 to 12 years old) and twelve young adults (from 20 to 27 years old) walked on force platforms at different walking speed. The ground reaction forces under each foot were recorded and the vertical velocity of the centre of mass of the body was computed. With decreasing age and increasing velocity (or Froude number), the occurrence of unanticipated transition is higher, related to a different ratio between the vertical support of the front and back leg. The different transition strategy observed in children indicates that body weight transfer from one limb to the other is not fully mature at 12 years old.

Muscle Activity during Passive and Active Movements in Preterm and Full-Term Infants.

Manifestation of muscle reactions at an early developmental stage may reflect the processes underlying the generation of appropriate muscle tone, which is also an integral part of all movements. In preterm infants, some aspects of muscular development may occur differently than in infants born at term. Here we evaluated early manifestations of muscle tone by measuring muscle responses to passive stretching (StR) and shortening (ShR) in both upper and lower limbs in preterm infants (at the corrected age from 0 weeks to 12 months), and compared them to those reported in our previous study on full-term infants. In a subgroup of participants, we also assessed spontaneous muscle activity during episodes of relatively large limb movements. The results showed very frequent StR and ShR, and also responses in muscles not being primarily stretched/shortened, in both preterm and full-term infants. A reduction of sensorimotor responses to muscle lengthening and shortening with age suggests a reduction in excitability and/or the acquisition of functionally appropriate muscle tone during the first year of life. The alterations of responses during passive and active movements in preterm infants were primarily seen in the early months, perhaps reflecting temporal changes in the excitability of the sensorimotor networks.

Exoskeleton gait training with spinal cord neuromodulation.

Neuromodulating the locomotor network through spinal cord electrical stimulation (SCES) is effective for restoring function in individuals with gait deficits. However, SCES alone has limited effectiveness without concurrent locomotor function training that enhances activity-dependent plasticity of spinal neuronal networks by sensory feedback. This mini review discusses recent developments in using combined interventions, such as SCES added to exoskeleton gait training (EGT). To develop personalized therapies, it is crucial to assess the state of spinal circuitry through a physiologically relevant approach that identifies individual characteristics of spinal cord function to develop person-specific SCES and EGT. The existing literature suggests that combining SCES and EGT to activate the locomotor network can have a synergistic rehabilitative effect on restoring walking abilities, somatic sensation, and cardiovascular and bladder function in paralyzed individuals.

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.

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.

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.

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.

Muscle synergy analysis yields an efficient and physiologically relevant method of assessing stroke.

The Fugl-Meyer Assessment is widely used to test motor function in stroke survivors. In the Fugl-Meyer Assessment, stroke survivors perform several movement tasks and clinicians subjectively rate the performance of each task item. The individual task items in the Fugl-Meyer Assessment are selected on the basis of clinical experience, and their physiological relevance has not yet been evaluated. In the present study, we aimed to objectively rate the performance of task items by measuring the muscle activity of 41 muscles from the upper body while stroke survivors and healthy participants performed 37 Fugl-Meyer Assessment upper extremity task items. We used muscle synergy analysis to compare muscle activity between subjects and found that 13 muscle synergies in the healthy participants (which we defined as standard synergies) were able to reconstruct all of the muscle activity in the Fugl-Meyer Assessment. Among the standard synergies, synergies involving the upper arms, forearms and fingers were activated to varying degrees during different task items. In contrast, synergies involving posterior trunk muscles were activated during all tasks, which suggests the importance of posterior trunk muscle synergies throughout all sequences. Furthermore, we noted the inactivation of posterior trunk muscle synergies in stroke survivors with severe but not mild impairments, suggesting that lower trunk stability and the underlying activity of posterior trunk muscle synergies may have a strong influence on stroke severity and recovery. By comparing the synergies of stroke survivors with standard synergies, we also revealed that some synergies in stroke survivors corresponded to merged standard synergies; the merging rate increased with the impairment of stroke survivors. Moreover, the degrees of severity-dependent changes in the merging rate (the merging rate-severity relationship) were different among different task items. This relationship was significant for 26 task items only and not for the other 11 task items. Because muscle synergy analysis evaluates coordinated muscle activities, this different dependency suggests that these 26 task items are appropriate for evaluating muscle coordination and the extent of its impairment in stroke survivors. Overall, we conclude that the Fugl-Meyer Assessment reflects physiological function and muscle coordination impairment and suggest that it could be performed using a subset of the 37 task items.

Higher Responsiveness of Pattern Generation Circuitry to Sensory Stimulation in Healthy Humans Is Associated with a Larger Hoffmann Reflex.

The state and excitability of pattern generators are attracting the increasing interest of neurophysiologists and clinicians for understanding the mechanisms of the rhythmogenesis and neuromodulation of the human spinal cord. It has been previously shown that tonic sensory stimulation can elicit non-voluntary stepping-like movements in non-injured subjects when their limbs were placed in a gravity-neutral unloading apparatus. However, large individual differences in responsiveness to such stimuli were observed, so that the effects of sensory neuromodulation manifest only in some of the subjects. Given that spinal reflexes are an integral part of the neuronal circuitry, here we investigated the extent to which spinal pattern generation excitability in response to the vibrostimulation of muscle proprioceptors can be related to the H-reflex magnitude, in both the lower and upper limbs. For the H-reflex measurements, three conditions were used: stationary limbs, voluntary limb movement and passive limb movement. The results showed that the H-reflex was considerably higher in the group of participants who demonstrated non-voluntary rhythmic responses than it was in the participants who did not demonstrate them. Our findings are consistent with the idea that spinal reflex measurements play important roles in assessing the rhythmogenesis of the spinal cord.

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.

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.

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.

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.

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.

Exoskeleton Walk Training in Paralyzed Individuals Benefits From Transcutaneous Lumbar Cord Tonic Electrical Stimulation.

In recent years, advanced technologies featuring wearable powered exoskeletons and neuromodulation of lumbosacral spinal networks have been developed to facilitate stepping and promote motor recovery in humans with paralysis. Here we studied a combined effect of spinal cord electrical stimulation (SCES) and exoskeleton walk training (EWT) during an intensive 2-week rehabilitative protocol in spinal cord injury individuals (n = 19, American Spinal Injury Association Impairment Scale (AIS) A-11, B-5, C-3). The purpose of this study was to evaluate the compatibility of methods and to explore the main effects of combined SCES and EWT. All participants had a chronic state of paralysis (1-11 years after trauma). In addition, in the control group (n = 16, AIS A-7, B-5, C-4), we performed EWT without SCES. For EWT, we used a powered exoskeleton (ExoAtlet), while stability was assisted by crutches, with automatic arrest of stepping if excessive torques were detected. SCES was applied to the level of the mid-lumbar cord over the Th12 vertebra at 1 or 3 pulses/s (4 individuals with severe spasticity were also stimulated in an anti-spastic mode 67 pulses/s). The vertical component of the ground reaction force was recorded using the F-Scan system at the onset and after training with SCES. EWT with SCES significantly increased the foot loading forces, could decrease their asymmetry and 8 out of 19 subjects improved their Hauser Ambulation Index. The anti-spastic mode of stimulation also allowed individuals with severe spasticity to walk with the aid of the exoskeleton. Participants reported facilitation when walking with SCES, paresthesia in leg muscles and new non-differential sensation of passive motion in leg joints. Neurological examination showed an increase of tactile (7) and/or pain (7) sensation and an increase of the AIS motor scale in 9 individuals, including both incomplete and complete paralysis. Improvements in the neurological scores were, however, limited in the control group (EWT without SCES). The results suggest that SCES may facilitate training and walking in the exoskeleton by activating the locomotor networks and augmenting compensative sensitivity.

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.

Development of Locomotor-Related Movements in Early Infancy.

This mini-review focuses on the emergence of locomotor-related movements in early infancy. In particular, we consider multiples precursor behaviors of locomotion as a manifestation of the development of the neuronal networks and their link in the establishment of precocious locomotor skills. Despite the large variability of motor behavior observed in human babies, as in animals, afferent information is already processed to shape the behavior to specific situations and environments. Specifically, we argue that the closed-loop interaction between the neural output and the physical dynamics of the mechanical system should be considered to explore the complexity and flexibility of pattern generation in human and animal neonates.