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.

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.

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 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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.