Exploring harmonic walking development in children with unilateral cerebral palsy and typically developing toddlers: Insights from walking experience.

This longitudinal study investigated the impact of the first independent steps on harmonic gait development in unilateral cerebral palsy (CP) and typically developing (TD) children. We analysed the gait ratio values (GR) by comparing the duration of stride/stance, stance/swing and swing/double support phases. Our investigation focused on identifying a potential trend towards the golden ratio value of 1.618, which has been observed in the locomotion of healthy adults as a characteristic of harmonic walking. Locomotor ability was assessed in both groups at different developmental stages: before and after the emergence of independent walking. Results revealed that an exponential fit was observed only after the first unsupported steps were taken. TD children achieved harmonic walking within a relatively short period (approximately one month) compared to children with CP, who took about seven months to develop harmonic walking. Converging values for stride/stance and stance/swing gait ratios, averaged on the two legs, closely approached the golden ratio in TD children (R2 = 0.9) with no difference in the analysis of the left vs right leg separately. In contrast, children with CP exhibited a trend for stride/stance and stance/swing (R2 = 0.7), with distinct trends observed for the most affected leg which did not reach the golden ratio value for the stride/stance ratio (GR = 1.5), while the least affected leg exceeded it (GR = 1.7). On the contrary, the opposite trend was observed for the stance/swing ratio. These findings indicate an overall harmonic walking in children with CP despite the presence of asymmetry between the two legs. These results underscore the crucial role of the first independent steps in the progressive development of harmonic gait over time.

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.

Predicting vertical ground reaction forces from 3D accelerometry using reservoir computers leads to accurate gait event detection.

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.

Cortical contributions to locomotor primitives in toddlers and adults.

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 Role of Walking Experience in the Emergence of Gait Harmony in Typically Developing Toddlers.

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.

Body Weight Control Is a Key Element of Motor Control for Toddlers' Walking.

New-borns can step when supported for about 70-80% of their own body weight. Gravity-related sensorimotor information might be an important factor in developing the ability to walk independently. We explored how body weight support alters motor control in toddlers during the first independent steps and in toddlers with about half a year of walking experience. Sixteen different typically developing children were assessed during (un)supported walking on a running treadmill. Electromyography of 18-24 bilateral leg and back muscles and vertical ground reaction forces were recorded. Strides were grouped into four levels of body weight support ranging from no (<10%), low (10-35%), medium (35-55%), and high (55-95%) support. We constructed muscle synergies and muscle networks and assessed differences between levels of support and between groups. In both groups, muscle activities could be described by four synergies. As expected, the mean activity decreased with body weight support around foot strikes. The younger first-steps group showed changes in the temporal pattern of the synergies when supported for more than 35% of their body weight. In this group, the muscle network was dense with several interlimb connections. Apparently, the ability to process gravity-related information is not fully developed at the onset of independent walking causing motor control to be fairly disperse. Synergy-specific sensitivity for unloading implies distinct neural mechanisms underlying (the emergence of) these synergies.

Muscle synergy structure and gait patterns in children with spastic cerebral palsy.

AIM: To determine if muscle synergy structure (activations and weights) differs between gait patterns in children with spastic cerebral palsy (CP). METHOD: In this cross-sectional study, we classified 188 children with unilateral (n=82) or bilateral (n=106) spastic CP (mean age: 9y 5mo, SD: 4y 3mo, range: 3y 9mo-17y 7mo; 75 females; Gross Motor Function Classification System [GMFCS] level I: 106, GMFCS level II: 55, GMFCS level III: 27) into a minor deviations (n=34), drop foot (n=16), genu recurvatum (n=26), apparent equinus (n=53), crouch (n=39), and jump gait pattern (n=20). Surface electromyography recordings from eight lower limb muscles of the most affected side were used to calculate synergies with weighted non-negative matrix factorization. We compared synergy activations and weights between the patterns. RESULTS: Synergy structure was similar between gait patterns, although weights differed in the more impaired children (crouch and jump gait) when compared to the other patterns. Variability in synergy structure between participants was high. INTERPRETATION: The similarity in synergy structure between gait patterns suggests a generic motor control strategy to compensate for the brain lesion. However, the differences in weights and high variability between participants indicate that this generic motor control strategy might be individualized and dependent on impairment level.

How wide should you view to fight? Establishing the size of the visual field necessary for grip fighting in judo.

Peripheral vision is often considered vital in (combat) sports, yet most experimental paradigms (e.g., eye tracking) ignore peripheral information or struggle to make inferences about the role of peripheral vision in an in-situ performance environment. This study aimed to determine where visual information is located in the peripheral field during an in-situ combat sports task. Eight advanced judokas competed in grip-fighting exchanges while wearing a mobile eye-tracker to locate gaze direction. Three-dimensional position data of the head and hands were tracked using a VICON motion capture system. Gaze analysis through automatic feature detection showed that participants predominantly fixated on their opponent's chest. Kinematic data were used to calculate the angles between the opponent's hands and the gaze-anchor point on the chest of the opponent. Results revealed a nonlinear relationship between visual field (VF) size and visibility of the hands, with athletes needing a VF of at least 30-40 degrees radius to simultaneously monitor both hands of the opponent most of the time. These findings hold implications for the regulation of Paralympic judo for athletes with vision impairment, suggesting that a less severe degree of impairment should be required to qualify than the current criterion of 20 degrees radius.

Early Development of Locomotor Patterns and Motor Control in Very Young Children at High Risk of Cerebral Palsy, a Longitudinal Case Series.

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 in Children Walking and Running on a Treadmill.

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.

Neuromuscular Control before and after Independent Walking Onset in Children with Cerebral Palsy.

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 development of mature gait patterns in children during walking and running.

PURPOSE: We sought to identify the developing maturity of walking and running in young children. We assessed gait patterns for the presence of flight and double support phases complemented by mechanical energetics. The corresponding classification outcomes were contrasted via a shotgun approach involving several potentially informative gait characteristics. A subsequent clustering turned out very effective to classify the degree of gait maturity. METHODS: Participants (22 typically developing children aged 2-9 years and 7 young, healthy adults) walked/ran on a treadmill at comfortable speeds. We determined double support and flight phases and the relationship between potential and kinetic energy oscillations of the center-of-mass. Based on the literature, we further incorporated a total of 93 gait characteristics (including the above-mentioned ones) and employed multivariate statistics comprising principal component analysis for data compression and hierarchical clustering for classification. RESULTS: While the ability to run including a flight phase increased with age, the flight phase did not reach 20% of the gait cycle. It seems that children use a walk-run-strategy when learning to run. Yet, the correlation strength between potential and kinetic energies saturated and so did the amount of recovered mechanical energy. Clustering the set of gait characteristics allowed for classifying gait in more detail. This defines a metric for maturity in terms of deviations from adult gait, which disagrees with chronological age. CONCLUSIONS: The degree of gait maturity estimated statistically using various gait characteristics does not always relate directly to the chronological age of the child.

Motion tracking in developmental research: Methods, considerations, and applications.

In this chapter, we explore the use of motion tracking methodology in developmental research. With motion tracking, also called motion capture, human movements can be precisely recorded and analyzed. Motion tracking provides developmental researchers with objective measurements of motor and (socio-)cognitive development. It can further be used to create carefully-controlled stimuli videos and can offer means of measuring development outside of the lab. We discuss three types of motion tracking that lend themselves to developmental applications. First, marker-based systems track optical or electromagnetic markers or sensors placed on the body and offer high accuracy measurements. Second, markerless methods entail image processing of videos to track the movement of bodies without participants being hindered by physical markers. Third, inertial motion tracking measures three-dimensional movements and can be used in a variety of settings. The chapter concludes by examining three example topics from developmental literature in which motion tracking applications have contributed to our understanding of human development.

Muscle Synergies and Coherence Networks Reflect Different Modes of Coordination During Walking.

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.

Muscle Synergies During Walking in Children With Cerebral Palsy: A Systematic Review.

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.

Muscle Synergies in Response to Biofeedback-Driven Gait Adaptations in Children With Cerebral Palsy.

BACKGROUND: Children 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. AIM: Investigate the underlying SMC and changes that may occur when gait is adapted with biofeedback. METHODS: Twenty-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. RESULTS: Despite 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. CONCLUSION: These 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.

The human sensorimotor cortex fosters muscle synergies through cortico-synergy coherence.

In neuromotor control, the dimensionality of complex muscular activation patterns is effectively reduced through the emergence of muscle synergies. Muscle synergies are tailored to task-specific biomechanical needs. Traditionally, they are considered as low-dimensional neural output of the spinal cord and as such their coherent cortico-muscular pathways have remained underexplored in humans. We investigated whether muscle synergies have a higher-order origin, especially, whether they are manifest in the cortical motor network. We focused on cortical muscle synergy representations involved in balance control and examined changes in cortico-synergy coherence accompanying short-term balance training. We acquired electromyography and electro-encephalography and reconstructed cortical source activity using adaptive spatial filters. The latter were based on three muscle synergies decomposed from the activity of nine unilateral leg muscles using non-negative matrix factorization. The corresponding cortico-synergy coherence displayed phase-locked activity at the Piper rhythm, i.e., cortico-spinal synchronization around 40 Hz. Our study revealed the presence of muscle synergies in the motor cortex, in particular, in the paracentral lobule, known for the representation of lower extremities. We conclude that neural oscillations synchronize between the motor cortex and spinal motor neuron pools signifying muscle synergies. The corresponding cortico-synergy coherence around the Piper rhythm decreases with training-induced balance improvement.

Engagement of the Rat Hindlimb Motor Cortex across Natural Locomotor Behaviors.

Contrary to cats and primates, cortical contribution to hindlimb locomotor movements is not critical in rats. However, the importance of the motor cortex to regain locomotion after neurological disorders in rats suggests that cortical engagement in hindlimb motor control may depend on the behavioral context. To investigate this possibility, we recorded whole-body kinematics, muscle synergies, and hindlimb motor cortex modulation in freely moving rats performing a range of natural locomotor procedures. We found that the activation of hindlimb motor cortex preceded gait initiation. During overground locomotion, the motor cortex exhibited consistent neuronal population responses that were synchronized with the spatiotemporal activation of hindlimb motoneurons. Behaviors requiring enhanced muscle activity or skilled paw placement correlated with substantial adjustment in neuronal population responses. In contrast, all rats exhibited a reduction of cortical activity during more automated behavior, such as stepping on a treadmill. Despite the facultative role of the motor cortex in the production of locomotion in rats, these results show that the encoding of hindlimb features in motor cortex dynamics is comparable in rats and cats. However, the extent of motor cortex modulations appears linked to the degree of volitional engagement and complexity of the task, reemphasizing the importance of goal-directed behaviors for motor control studies, rehabilitation, and neuroprosthetics. SIGNIFICANCE STATEMENT: We mapped the neuronal population responses in the hindlimb motor cortex to hindlimb kinematics and hindlimb muscle synergies across a spectrum of natural locomotion behaviors. Robust task-specific neuronal population responses revealed that the rat motor cortex displays similar modulation as other mammals during locomotion. However, the reduced motor cortex activity during more automated behaviors suggests a relationship between the degree of engagement and task complexity. This relationship emphasizes the importance of the behavioral procedure to engage the motor cortex during motor control studies, gait rehabilitation, and locomotor neuroprosthetic developments in rats.

Spatiotemporal neuromodulation therapies engaging muscle synergies improve motor control after spinal cord injury.

Electrical neuromodulation of lumbar segments improves motor control after spinal cord injury in animal models and humans. However, the physiological principles underlying the effect of this intervention remain poorly understood, which has limited the therapeutic approach to continuous stimulation applied to restricted spinal cord locations. Here we developed stimulation protocols that reproduce the natural dynamics of motoneuron activation during locomotion. For this, we computed the spatiotemporal activation pattern of muscle synergies during locomotion in healthy rats. Computer simulations identified optimal electrode locations to target each synergy through the recruitment of proprioceptive feedback circuits. This framework steered the design of spatially selective spinal implants and real-time control software that modulate extensor and flexor synergies with precise temporal resolution. Spatiotemporal neuromodulation therapies improved gait quality, weight-bearing capacity, endurance and skilled locomotion in several rodent models of spinal cord injury. These new concepts are directly translatable to strategies to improve motor control in humans.