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Summary: Human gait is a complex behavior requiring dynamic control of upper and lower extremities that is accompanied by cortical activity in multiple brain areas. We investigated the contribution of beta (15–30 Hz) and gamma (30–50 Hz) band electroencephalography (EEG) activity during specific phases of the gait cycle, comparing treadmill walking with and without arm swing. Modulations of spectral power in the beta band during early double support and swing phases source-localized to the sensorimotor cortex ipsilateral, but not contralateral, to the leading leg. The lateralization disappeared in the condition with constrained arms, together with an increase of activity in bilateral supplementary motor areas. By contrast, gamma band modulations that localized to the presumed leg area of sensorimotor cortex around the heel-strike events were unaffected by arm movement. Our findings demonstrate that arm swing is accompanied by considerable cortical activation that should not be neglected in gait-related neuroimaging studies.

IntroductionChildren start to run after they master walking. How running develops, however, is largely unknown.MethodsWe 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.ResultsBoth 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.DiscussionAn 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.

Accelerometers are low-cost measurement devices that can readily be used outside the lab. However, determining isolated gait events from accelerometer signals, especially foot-off events during running, is an open problem. We outline a two-step approach where machine learning serves to predict vertical ground reaction forces from accelerometer signals, followed by force-based event detection. We collected shank accelerometer signals and ground reaction forces from 21 adults during comfortable walking and running on an instrumented treadmill. We trained one common reservoir computer using segmented data using both walking and running data. Despite being trained on just a small number of strides, this reservoir computer predicted vertical ground reaction forces in continuous gait with high quality. The subsequent foot contact and foot off event detection proved highly accurate when compared to the gold standard based on co-registered ground reaction forces. Our proof-of-concept illustrates the capacity of combining accelerometry with machine learning for detecting isolated gait events irrespective of mode of locomotion.

Summary: The neural locomotor system strongly relies on spinal circuitries. Yet, the control of bipedal gait is accompanied by activity in motor cortex. In human gait control, the functional interaction between these cortical contributions and their spinal counterparts are largely elusive. We focused on four spinal activation patterns during walking and explored their cortical signatures in toddlers and adults. In both groups, cortico-spinal coherence analysis revealed activity in primary motor cortex to be closely related to two of the four spinal patterns. Their corresponding muscle synergies are known to develop around the onset of independent walking. By hypothesis, the cortex hence contributes to the emergence of these synergies. In contrast, the other two spinal patterns investigated here resembled those present during newborn stepping. As expected, they did not show any cortical involvement. Together, our findings suggest a crucial role of motor cortex for independent walking in humans.

The first years of life might be critical for encouraging independent walking in children with cerebral palsy (CP). We sought to identify mechanisms that may underlie the impaired development of walking in three young children with early brain lesions, at high risk of CP, via comprehensive instrumented longitudinal assessments of locomotor patterns and muscle activation during walking. We followed three children (P1–P3) with early brain lesions, at high risk of CP, during five consecutive gait analysis sessions covering a period of 1 to 2 years, starting before the onset of independent walking, and including the session during the first independent steps. In the course of the study, P1 did not develop CP, P2 was diagnosed with unilateral and P3 with bilateral CP. We monitored the early development of locomotor patterns over time via spatiotemporal gait parameters, intersegmental coordination (estimated via principal component analysis), electromyography activity, and muscle synergies (determined from 11 bilateral muscles via nonnegative matrix factorization). P1 and P2 started to walk independently at the corrected age of 14 and 22 months, respectively. In both of them, spatiotemporal gait parameters, intersegmental coordination, muscle activation patterns, and muscle synergy structure changed from supported to independent walking, although to a lesser extent when unilateral CP was diagnosed (P2), especially for the most affected leg. The child with bilateral CP (P3) did not develop independent walking, and all the parameters did not change over time. Our exploratory longitudinal study revealed differences in maturation of locomotor patterns between children with divergent developmental trajectories. We succeeded in identifying mechanisms that may underlie impaired walking development in very young children at high risk of CP. When verified in larger sample sizes, our approach may be considered a means to improve prognosis and to pinpoint possible targets for early intervention.

Muscle synergies reflect the presence of a common neural input to multiple muscles. Steering small sets of synergies is commonly believed to simplify the control of complex motor tasks like walking and running. When these locomotor patterns emerge, it is likely that synergies emerge as well. We hence hypothesized that in children learning to run the number of accompanying synergies increases and that some of the synergies’ activities display a temporal shift related to a reduced stance phase as observed in adults. We investigated the development of locomotion in 23 children aged 2–9 years of age and compared them with seven young adults. Muscle activity of 15 bilateral leg, trunk, and arm muscles, ground reaction forces, and kinematics were recorded during comfortable treadmill walking and running, followed by a muscle synergy analysis. We found that toddlers (2–3.5 years) and preschoolers (3.5–6.5 years) utilize a “walk-run strategy” when learning to run: they managed the fastest speeds on the treadmill by combining double support (DS) and flight phases (FPs). In particular the activity duration of the medial gastrocnemius muscle was weakly correlated with age. The number of synergies across groups and conditions needed to cover sufficient data variation ranged between four and eight. The number of synergies tended to be smaller in toddlers than it did in preschoolers and school-age children but the adults had the lowest number for both conditions. Against our expectations, the age groups did not differ significantly in the timing or duration of synergies. We believe that the increase in the number of muscle synergies in older children relates to motor learning and exploration. The ability to run with a FP is clearly associated with an increase in the number of muscle synergies.

When walking speed is increased, the frequency ratio between the arm and leg swing switches spontaneously from 2:1 to 1:1. We examined whether these switches are accompanied by changes in functional connectivity between multiple muscles. Subjects walked on a treadmill with their arms swinging along their body while kinematics and surface electromyography (EMG) of 26 bilateral muscles across the body were recorded. Walking speed was varied from very slow to normal. We decomposed EMG envelopes and intermuscular coherence spectra using non-negative matrix factorization (NMF), and the resulting modes were combined into multiplex networks and analyzed for their community structure. We found five relevant muscle synergies that significantly differed in activation patterns between 1:1 and 2:1 arm-leg coordination and the transition period between them. The corresponding multiplex network contained a single module indicating pronounced muscle co-activation patterns across the whole body during a gait cycle. NMF of the coherence spectra distinguished three EMG frequency bands: 4–8, 8–22, and 22–60 Hz. The community structure of the multiplex network revealed four modules, which clustered functional and anatomical linked muscles across modes of coordination. Intermuscular coherence at 4–22 Hz between upper and lower body and within the legs was particularly pronounced for 1:1 arm-leg coordination and was diminished when switching between modes of coordination. These findings suggest that the stability of arm-leg coordination is associated with modulations in long-distant neuromuscular connectivity.

Background: Walking problems in children with cerebral palsy (CP) can in part be explained by limited selective motor control. Muscle synergy analysis is increasingly used to quantify altered neuromuscular control during walking. The early brain injury in children with CP may lead to a different development of muscle synergies compared to typically developing (TD) children, which might characterize the abnormal walking patterns.Objective: The overarching aim of this review is to give an overview of the existing studies investigating muscle synergies during walking in children with CP compared to TD children. The main focus is on how muscle synergies differ between children with CP and TD children, and we examine the potential of muscle synergies as a measure to quantify and predict treatment outcomes.Methods: Bibliographic databases were searched by two independent reviewers up to 22 April 2019. Studies were included if the focus was on muscle synergies of the lower limbs during walking, obtained by a matrix factorization algorithm, in children with CP.Results: The majority (n = 12) of the 16 included studies found that children with CP recruited fewer muscle synergies during walking compared to TD children, and several studies (n = 8) showed that either the spatial or temporal structure of the muscle synergies differed between children with CP and TD children. Variability within and between subjects was larger in children with CP than in TD children, especially in more involved children. Muscle synergy characteristics before treatments to improve walking function could predict treatment outcomes (n = 3). Only minimal changes in synergies were found after treatment.Conclusions: The findings in this systematic review support the idea that children with CP use a simpler motor control strategy compared to TD children. The use of muscle synergy analysis as a clinical tool to quantify altered neuromuscular control and predict clinical outcomes seems promising. Further investigation on this topic is necessary, and the use of muscle synergies as a target for development of novel therapies in children with CP could be explored.

The ability to walk without support usually develops in the first year of a typically developing toddler’s life and matures further in the following years. Mature walking is characterized by the correct timing of the different gait phases that make up a full gait cycle formed by stance, swing, and double support phases. The harmony of mature walking is given by a specific self-similar structure of the ratios between the durations of these phases (stride/stance, stance/swing, swing/double support), that in adults all converge to the golden ratio (phi, about 1.618). The aim of this longitudinal, prospective, experimental study was to investigate the evolution of this gait harmonic structure in the transition from supported to independent walking. In total, 27 children were recruited and recorded at various stages of locomotor development, ranging from neonatal stepping up to an independent walking experience of about six months. Differently from walking speed that progressively increased with age, the gait phase ratios started to converge to golden value only after the first independent steps, suggesting a relation to the maturation of the walking experience. The independent walking experience seems to represent a trigger for the evolution of a locomotor harmonic pattern in toddlers learning to walk.

BackgroundChildren with cerebral palsy (CP) often show impaired selective motor control (SMC) that induces limitations in motor function. Children with CP can improve aspects of pathological gait in an immediate response to visual biofeedback. It is not known, however, how these gait adaptations are achieved at the neural level, nor do we know the extent of SMC plasticity in CP.AimInvestigate the underlying SMC and changes that may occur when gait is adapted with biofeedback.MethodsTwenty-three ambulatory children with CP and related (hereditary) forms of spastic paresis (Aged: 10.4 ± 3.1, 6–16 years, M: 16/F: 9) were challenged with real-time biofeedback to improve step length, knee extension, and ankle power while walking on an instrumented treadmill in a virtual reality environment. The electromyograms of eight superficial muscles of the leg were analyzed and synergies were further decomposed using non-negative matrix factorization (NNMF) using 1 to 5 synergies, to quantify SMC. Total variance accounted for (tVAF) was used as a measure of synergy complexity. An imposed four synergy solution was investigated further to compare similarity in weightings and timing patterns of matched paired synergies between baseline and biofeedback trials.ResultsDespite changes in walking pattern, changes in synergies were limited. The number of synergies required to explain at least 90% of muscle activation increased significantly, however, the change in measures of tVAF1 from baseline (0.75 ± 0.08) were less than ±2% between trials. In addition, within-subject similarity of synergies to baseline walking was high (>0.8) across all biofeedback trials.ConclusionThese results suggest that while gait may be adapted in an immediate response, SMC as quantified by synergy analysis is perhaps more rigidly impaired in CP. Subtle changes in synergies were identified; however, it is questionable if these are clinically meaningful at the level of an individual. Adaptations may be limited in the short term, and further investigation is essential to establish if long term training using biofeedback leads to adapted SMC.

Early brain lesions which produce cerebral palsy (CP) may affect the development of walking. It is unclear whether or how neuromuscular control, as evaluated by muscle synergy analysis, differs in young children with CP compared to typically developing (TD) children with the same walking ability, before and after the onset of independent walking. Here we grouped twenty children with (high risk of) CP and twenty TD children (age 6.5–52.4 months) based on their walking ability, supported or independent walking. Muscle synergies were extracted from electromyography data of bilateral leg muscles using non-negative matrix factorization. Number, synergies’ structure and variability accounted for when extracting one (VAF1) or two (VAF2) synergies were compared between CP and TD. Children in the CP group recruited fewer synergies with higher VAF1 and VAF2 compared to TD children in the supported and independent walking group. The most affected side in children with asymmetric CP walking independently recruited fewer synergies with higher VAF1 compared to the least affected side. Our findings suggest that early brain lesions result in early alterations of neuromuscular control, specific for the most affected side in asymmetric CP.

The aim of this study was to explore the underlying age-related differences in dynamic motor control during different step ascent conditions using muscle synergy analysis. Eleven older women (67.0 y ± 2.5) and ten young women (22.5 y ± 1.6) performed stepping in forward and lateral directions at step heights of 10, 20 and 30 cm. Surface electromyography was obtained from 10 lower limb and torso muscles. Non-negative matrix factorization was used to identify sets of (n) synergies across age groups and stepping conditions. In addition, variance accounted for (VAF) by the detected number of synergies was compared to assess complexity of motor control. Finally, correlation coefficients of muscle weightings and between-subject variability of the temporal activation patterns were calculated and compared between age groups and stepping conditions. Four synergies accounted for >85% VAF across age groups and stepping conditions. Age and step height showed a significant negative correlation with VAF during forward stepping but not lateral stepping, with lower VAF indicating higher synergy complexity. Muscle weightings showed higher similarity across step heights in older compared to young women. Neuromuscular control of young and community-dwelling older women could not be differentiated based on the number of synergies extracted. Additional analyses of synergy structure and complexity revealed subtle age- and step-height-related differences, indicating that older women rely on more complex neuromuscular control strategies.

BackgroundOn Earth only a few legged species, such as water strider insects, some aquatic birds and lizards, can run on water. For most other species, including humans, this is precluded by body size and proportions, lack of appropriate appendages, and limited muscle power. However, if gravity is reduced to less than Earth's gravity, running on water should require less muscle power. Here we use a hydrodynamic model to predict the gravity levels at which humans should be able to run on water. We test these predictions in the laboratory using a reduced gravity simulator.Methodology/principal findingsWe adapted a model equation, previously used by Glasheen and McMahon to explain the dynamics of Basilisk lizard, to predict the body mass, stride frequency and gravity necessary for a person to run on water. Progressive body-weight unloading of a person running in place on a wading pool confirmed the theoretical predictions that a person could run on water, at lunar (or lower) gravity levels using relatively small rigid fins. Three-dimensional motion capture of reflective markers on major joint centers showed that humans, similarly to the Basilisk Lizard and to the Western Grebe, keep the head-trunk segment at a nearly constant height, despite the high stride frequency and the intensive locomotor effort. Trunk stabilization at a nearly constant height differentiates running on water from other, more usual human gaits.Conclusions/significanceThe results showed that a hydrodynamic model of lizards running on water can also be applied to humans, despite the enormous difference in body size and morphology.

Little is known on the role that knowledge about body dimensions plays within this process. Here we directly addressed this question by evaluating whether changes in body proportions interfere with computation of traveled distance for targets located outside the reaching space. We studied locomotion and distance estimation in an achondroplastic child (ACH, 11 yr) before and after surgical elongation of the shank segments of both lower limbs and in healthy adults walking on stilts, designed to mimic shank-segment elongation. Kinematic analysis of gait revealed that dynamic coupling of the thigh, shank, and foot segments changed substantially as a result of elongation. Step length remained unvaried, in spite of the significant increase in total limb length (∼1.5-fold). These relatively shorter strides resulted from smaller oscillations of the shank segment, as would be predicted by proportional increments in limb size and not by asymmetrical segmental increment as in the present case (length of thighs was not modified). Distance estimation was measured by walking with eyes closed toward a memorized target. Before surgery, the behavior of ACH was comparable to that of typically developing participants. In contrast, following shank elongation, the ACH walked significantly shorter distances when aiming at the same targets. Comparable changes in limb kinematics, stride length, and estimation of traveled distance were found in adults wearing on stilts, suggesting that path integration errors in both cases were related to alterations in the intersegmental coordination of the walking limbs. The results are consistent with a dynamic locomotor body schema used for controlling step length and path estimation, based on inherent relationships between gait parameters and body proportions. [ABSTRACT FROM AUTHOR]

On earth, body weight is an inherent constraint, and accordingly, load-regulating mechanisms play an important role in terrestrial locomotion. How do toddlers deal with the effects of their full body weight when faced with the task of independent upright locomotion for the first time? Here we studied the effect of load variation on walking in 12 toddlers during their first unsupported steps, 15 older children (1.3–5 yr), and 10 adults. To simulate various levels of body weight, an experimenter held the trunk of the subject with both hands and supplied an approximately constant vertical force during stepping on a force platform. During unsupported stepping, the shape of the foot path in toddlers (typically single-peak toe trajectory) was different from that of adults and older children (double-peak trajectory). In contrast to adults and older children, who showed only limited changes in kinematic coordination, the "reduced-gravity" condition considerably affected the shape of the foot path in toddlers: they tended to make a high lift and forward foot overshoot at the end of swing. In addition, stepping at high levels of body unloading was characterized by a significant change in the initial direction of foot motion during early swing. Intermediate walkers (1.5–5 mo after walking onset) showed only partial improvement in foot trajectory characteristics. The results suggest that, at the onset of walking, changes in vertical body loads are not compensated accurately by the kinematic controllers; compensation necessitates a few months of independent walking experience. [ABSTRACT FROM AUTHOR]