Understanding movement control in infants through the analysis of limb intersegmental dynamics

One important component in the understanding of the control of limb movements is the way in which the central nervous system accounts for joint forces and torques that may be generated not only by muscle actions but by gravity and by passive reactions related to the movements of limb segments. In this study, we asked how the neuromotor system of young infants controls a range of active and passive forces to produce a stereotypic, nonintentional movement. We specifically analyzed limb intersegmental dynamics in spontaneous, cyclic leg movements (kicking) of varying intensity in supine 3-month-old human infants. Using inverse dynamics, we calculated the contributions of active (muscular) and passive (motion-dependent and gravitational) torque components at the hip, knee, and ankle joints from three-dimensional limb kinematics. To calculate joint torques, accurate estimates were needed of the limb's anthropometric parameters, which we determined using a model of the human body. Our analysis of limb intersegmental dynamics explicitly quantified the complex interplay of active and passive forces producing the simple, involuntary kicking movements commonly seen in 3-month-old infants. our results revealed that in nonvigorous kicks, hip joint reversal was the result of an extensor torque due to gravity, opposed by the combined flexor effect of the muscle torque and the total motion-dependent torque. The total motion-dependent torque increased as a hip flexor torque in more vigorous kicks; an extensor muscle torque was necessary to counteract the flexor influences of the total motion-dependent torque and, in the case of large ranges of motion, a flexor gravity torque as well. Thus, with changing passive torque influences due to motions of the linked segments, the muscle torques were adjusted to produce a net torque to reverse the kicking motion. As a consequence, despite considerable heterogeneity in the intensity, range of motion, coordination, and movement context of each kick, smooth trajectories resulted from the muscle torque, counteracting and complementing not only gravity but also the motion-dependent torques generated by movement of the linked segments.     

Development of infant leg coordination: Exploiting passive torques

Leg joint coordination systematically changes over the first months of life, yet there is minimal data on the underlying change in muscle torques that might account for this change in coordination. The purpose of this study is to investigate the contribution of torque changes to early changes in leg joint coordination. Kicking actions were analyzed of 10 full-term infants between 6 and 15-weeks of age using three-dimensional kinematics and kinetics. We found 11 of 15 joint angle pairs demonstrated a change from more in-phase intralimb coordination at 6-weeks to less in-phase coordination at 15-weeks. Although the magnitude of joint torques normalized to the mass of the leg remained relatively consistent, we noted more complex patterns of torque component contribution across ages. By focusing on the change in torques associated with hip–knee joint coordination, we found that less in-phase hip–knee joint coordination at 15-weeks was associated with decreased influence of knee muscle torque and increased influence of knee gravitational and motion-dependent torques, supporting that infants coordinate hip muscle torque with passive knee gravitational and motion-dependent torques to generate kicks with reduced active knee muscle torque. We propose that between 6 and 15-weeks of age less in-phase hip–knee coordination emerges as infants exploit passive dynamics in the coordination of hip and knee motions.     

Adaptive Dynamics of the Leg Movement Patterns of Human Infants: I. The Effects of Posture on Spontaneous Kicking

This is the first of two articles in which we describe how infants adapt their spontaneous leg movements to changes in posture or to elicitation of behaviors by a mechanical treadmill. In this article, we compare the kinematics of kicks produced by 3-month-old infants in three postures, supine, angled (45°), and vertical, and examine the changes in muscular and nonmuscular force contributions to limb trajectory. By manipulating posture we were able to assess the sensitivity of the nascent motor system to changes in the gravitational context. The postural manipulation elicited a distinct behavioral and dynamic effect. In the more upright postures, gravitational resistance to motion at the hip was 4 to 10 times greater than resistance met in the supine posture, necessitating larger muscle torques to drive hip flexion. Kicks produced in the vertical posture showed a reduction in hip joint range of motion and an increase in synchronous joint flexion and extension at the hip and knee. At the same time, hip and knee muscle torques were also more highly correlated in kicks performed in the vertical than in the supine or angled posture. This increased correlation between muscle torques at the hip and knee implicates anatomical and energetic constraints—the intrinsic limb dynamics—in creating coordinated limb behavior out of nonspecific muscle activations.     

Adaptive Dynamics of the Leg Movement Patterns of Human Infants: I. The Effects of Posture on Spontaneous Kicking

This is the first of two articles in which we describe how infants adapt their spontaneous leg movements to changes in posture or to elicitation of behaviors by a mechanical treadmill. In this article, we compare the kinematics of kicks produced by 3-month-old infants in three postures, supine, angled (45 degrees ), and vertical, and examine the changes in muscular and nonmuscular force contributions to limb trajectory. By manipulating posture we were able to assess the sensitivity of the nascent motor system to changes in the gravitational context. The postural manipulation elicited a distinct behavioral and dynamic effect. In the more upright postures, gravitational resistance to motion at the hip was 4 to 10 times greater than resistance met in the supine posture, necessitating larger muscle torques to drive hip flexion. Kicks produced in the vertical posture showed a reduction in hip joint range of motion and an increase in synchronous joint flexion and extension at the hip and knee. At the same time, hip and knee muscle torques were also more highly correlated in kicks performed in the vertical than in the supine or angled posture. This increased correlation between muscle torques at the hip and knee implicates anatomical and energetic constraints-the intrinsic limb dynamics-in creating coordinated limb behavior out of nonspecific muscle activations.     

Effector dynamics of rhythmic wrist activity and its implications for (modeling) bimanual coordination

To examine the role of the effector dynamics of the wrist in the production of rhythmic motor activity, we estimated the phase shifts between the EMG and the task-related output for a rhythmic isometric torque production task and an oscillatory movement, and found a substantial difference (45-52 degrees) between the two. For both tasks, the relation between EMG and task-related output (torque or displacement) was adequately reproduced with a physiologically motivated musculoskeletal model. The model simulations demonstrated the importance of the contribution of passive structures to the overall dynamics and provided an account for the observed phase shifts in the dynamic task. Additional simulations of the musculoskeletal model with added load suggested that particular changes in the phase relation between EMG and movement may follow largely from the intrinsic muscle dynamics, rather than being the result of adaptations in the neural control of joint stiffness. The implications of these results are discussed in relation to (models of) interlimb coordination in rhythmic tasks.     

The influence of visual perception of self-motion on locomotor adaptation to unilateral limb loading

Self-perception of motion through visual stimulation may be important for adapting to locomotor conditions. Unilateral limb loading is a locomotor condition that can improve stability and reduce abnormal limb movement. In the present study, the authors investigated the effect of self-perception of motion through virtual reality (VR) on adaptation to unilateral limb loading. Healthy young adults, assigned to either a VR or a non-VR group, walked on a treadmill in the following 3 locomotor task periods--no load, loaded, and load removed. Subjects in the VR group viewed a virtual corridor during treadmill walking. Exposure to VR reduced cadence and muscle activity. During the loaded period, the swing time of the unloaded limb showed a larger increase in the VR group. When the load was removed, the swing time of the previously loaded limb and the stance time of the previously unloaded limb showed larger decrease and the swing time of the previously unloaded limb showed a smaller increase in the VR group. Lack of visual cues may cause the adoption of cautious strategies (higher muscle activity, shorter and more frequent steps, changes in the swing and stance times) when faced with situations that require adaptations. VR technology, providing such perceptual cues, has an important role in enhancing locomotor adaptation.     

Multi-body dynamic coupling mechanism for generating throwing arm velocity during baseball pitching

The purpose of this study was to identify the detailed mechanism how the maximum throwing arm endpoint velocity is determined by the muscular torques and non-muscular interactive torques from the perspective of the dynamic coupling among the trunk, thorax and throwing and non-throwing arm segments. The pitching movements of ten male collegiate baseball pitchers were measured by a three-dimensional motion capture system. Using the induced-segmental velocity analysis (IVA) developed in this study, the maximum fingertip velocity of the throwing arm (MFV) was decomposed into each contribution of the muscular torques, passive motion-dependent torques due to gyroscopic moment, Coriolis force and centrifugal force, and other interactive torque components. The results showed that MFV (31.6 ± 1.7 m/s) was mainly attributed to two different mechanisms. The first is the passive motion-dependent effect on increasing the angular velocities of three joints (thorax rotation, elbow extension and wrist flexion). The second is the muscular torque effect of the shoulder internal rotation (IR) torque on generating IR angular velocity. In particular, the centrifugal force-induced elbow extension motion, which was the greatest contributor among individual joint contributions, was caused primarily by the angular velocity-dependent forces associated with the humerus, thorax, and trunk rotations. Our study also found that a compensatory mechanism was achieved by the negative and positive contributions of the muscular torque components. The current IVA is helpful to understand how the rapid throwing arm movement is determined by the dynamic coupling mechanism.     

A comparison of the mechanical effect of arm swing and countermovement on the lower extremities in vertical jumping

The purposes of this study were to quantify and compare how arm swing and countermovement affect lower extremity torque and work during vertical jumping and to gain insight into the mechanisms that enable the arm swing and countermovement to increase jump height. Five participants maximally performed two types of vertical squat jumps with (SJA) and without (SJ) an arm swing and two types of countermovement vertical jumps with (CJA) and without (CJ) an arm swing. The participants jumped from a force platform and all performances were videotaped with a high-speed video camera (200Hz). Jump heights, joint torques and work were calculated by combining kinematic and kinetic data. It was found that of the four jumping conditions, the participants jumped highest when they used an arm swing with countermovement (i.e., CJA). The increase of the countermovement jump height with an arm swing is the result of the increase of the lower extremity work. In the hip joint, the increase in torque caused by the countermovement predominantly occurred at the beginning of the propulsion phase, while the increase in torque caused by the arm swing occurred in the rest of the propulsion phase. A key finding of our study is that arm swing and countermovement have independent effects on lower extremity work, and their effects are additive in CJA to produce greater jump height.     

Changes in lower limb co-contraction and stiffness by toddlers with Down syndrome and toddlers with typical development during the acquisition of independent gait

During gait acquisition, children learn to use their changing resources to meet the requirements of the task. Compared to typically developing toddlers (TD), toddlers with Down syndrome (DS) have functionally different musculoskeletal characteristics, such as hypotonia, and joint and ligament laxity, that could produce a reduced passive stiffness. The interplay between this inherently lower passive stiffness and the demands of walking may result in different strategies during gait acquisition. This study compared normalized global stiffness and lower limb's co-contraction indices (CCI) used by toddlers with TD (n=12) and with DS (n=12), during the early stages of gait acquisition. Stiffness and CCI were normalized by gravitational torque (mLg) in both phases of gait (stance, swing). Five longitudinal evaluations were conducted from the onset of locomotion until three months post-acquisition. All children were video taped and had electromyographic (EMG) recordings from muscle pairs of one leg, which were used to calculate CCI of hip, knee, ankle, and total leg CCI. Body and lower limb stiffness were calculated according to a hybrid pendulum resonance equation. Results from ANOVAs revealed no group differences on stiffness or on CCI's during stance but children with DS showed greater CCI during swing. Despite the structural musculoskeletal differences between toddlers with TD and with DS, the similarities observed in their processes of gait development suggest functional equivalences.     

Shoulder Muscle Activity Dampens Arm Swing Motion When Altering Upper Limb Mass Characteristics During Locomotion

Weighting the arms during locomotion results in decreased swing motion and increased shoulder muscle activity. To determine the functional relevance of this activity, participants walked on a treadmill with the arms unweighted, or weighted unilaterally or bilaterally. Similar to past work, the weighted arms decreased in swing amplitude and increased their shoulder muscle activity. A close examination of shoulder muscle activities in specific regions of the arm swing cycle suggested these muscles primarily acted eccentrically for all weighting conditions. These findings suggest that the increased shoulder muscle activities when weighting the arms act to dampen the arms when the inertial characteristics of the arms are altered, as opposed to assisting in driving swing of the heavier arms.     

Asymmetrical loading affects intersegmental dynamics during the swing phase of walking

Much of the work related to lower extremity inertia manipulations has focused on temporal, kinematic and traditional inverse dynamics assessments during locomotion. Intersegmental dynamics is an analytical technique that provides further insights into mechanisms underlying linked-segment motion. The purpose of this study was to determine how intersegmental dynamics during the swing phase of walking are altered during asymmetrical lower extremity loading. Participants walked overground at a speed of 1.57 m s^?1 with 0, 0.5, 1.0, and 2.0 kg attached to one foot. Net, interaction, gravitational, and muscle moments were computed. Moment magnitudes at joints of the loaded leg increased systematically with increasing load, whereas unloaded leg moments were unaffected by loading. With increasing load, relative contributions of interaction moments about the knee and hip and gravitational moment about the ankle increased (i.e., 21%, 8%, and 44% increases, respectively), whereas the relative contributions of muscle moments about all three joints declined (i.e., ?4%, ?13%, and ?8% decreases for the ankle, knee, and hip, respectively for unloaded vs. 2.0 kg). These results suggest that altered inertia properties of the limb not only affected the amount of muscular effort required to swing the leg, but also changed the nature of the interaction between segments.     

Age and gender moderate the effects of localized muscle fatigue on lower extremity joint torques used during quiet stance

This study examined the effects of localized muscle fatigue, age, and gender on lower extremity joint torques used during quiet stance. Thirty-two participants performed exercises designed to fatigue the ankle plantarflexors, knee extensors, torso extensors, or shoulder flexors. Body kinematics and ground reaction forces were obtained both before and after the exercises, and joint torques were derived via inverse dynamics. Single joint fatigue affected torque variability at all lower extremity joints, with similar changes for both age groups. Males and females exhibited increased ankle torque variability after different tasks, with males showing more variability after ankle fatigue and females after shoulder and lumbar fatigue. Correlations between peak torques and torque variability differed between males and females and between age groups in certain cases. The results of this study suggested that both age and gender moderate the effects of fatigue on postural control and should be considered when developing strategies to prevent occupational falls.     

State-dependent corrective reactions for backward balance losses during human walking

We investigated corrective reactions for backward balance losses during walking. Several biomechanical studies have suggested that backward falling can be predicted from the horizontal position and velocity of the body center of mass (COM) related to the stance foot. Our hypothesis was that corrective reactions for backward balance losses depend on whether the body moves forward or backward after a perturbation. Using a split-belt treadmill, backward balance losses during walking were induced by rapid decreases of belt speed from 3.5 km/h to 2.5, 2.0, 1.5 and 1.0 km/h. We measured kinematic data and surface electromyography (EMG) during corrective reactions while walking on the treadmill. Phase portrait analysis of COM trajectories revealed that backward balance stability was decreased by the perturbations. When the perturbed belt speed was 1.0 km/h, the COM states at toe-off were significantly lower than the stability limit; a rapid touch-down of the swing foot posterior to the stance foot then occurred, and the gait rhythm was modulated so that the phase advanced. EMG recordings during perturbed steps revealed a bilateral response, including modulation of the swing leg during the recovery. For weaker perturbations, the swing foot placements were anterior to the stance foot and there was a phase delay. In contrast to the bilateral responses for stronger perturbations, unilateral EMG responses were observed for weaker perturbations. The differences in joint kinematics and EMG patterns in the unperturbed swing leg depended on the COM states at toe-off, suggesting the existence of different responses consisting of ongoing swing movements and rapid touch-down. Thus, we conclude that corrective reactions for backward balance losses are not only phase-dependent but also state-dependent. In addition, the control system for backward balance losses predicts the feasibility of forward progression and modulates swing movement and walking rhythm according to backward balance stability.     

Changes in muscle and joint coordination in learning to direct forces

While it has been suggested that bi-articular muscles have a specialized role in directing external reaction forces, it is unclear how humans learn to coordinate mono- and bi-articular muscles to perform force-directing tasks. Participants were asked to direct pedal forces in a specified target direction during one-legged cycling. We expected that with practice, performance improvement would be associated with specific changes in joint torque patterns and mono- and bi-articular muscular coordination. Nine male participants practiced pedaling an ergometer with only their left leg, and were instructed to always direct their applied pedal force perpendicular to the crank arm (target direction) and to maintain a constant pedaling speed. After a single practice session, the mean error between the applied and target pedal force directions decreased significantly. This improved performance was accompanied by a significant decrease in the amount of ankle angular motion and a smaller increase in knee and hip angular motion. This coincided with a re-organization of lower extremity joint torques, with a decrease in ankle plantarflexor torque and an increase in knee and hip flexor torques. Changes were seen in both mono- and bi-articular muscle activity patterns. The mono-articular muscles exhibited greater alterations, and appeared to contribute to both mechanical work and force-directing. With practice, a loosening of the coupling between bi-articular thigh muscle activation and joint torque co-regulation was observed. The results demonstrated that participants were able to learn a complex and dynamic force-directing task by changing the direction of their applied pedal forces through re-organization of joint torque patterns and mono- and bi-articular muscle coordination.     

Effects of walking on various inclines on EMG patterns of lower limb muscles in humans

Myoelectric signals from several muscles of the lower limb were studied during treadmill locomotion over various inclines. A pattern recognition technique was used to analyse these activity patterns. The analyses revealed the following rules. These are common features among the various muscle activity patterns. The results suggest that the limb is controlled as a unit. Both phasic and average components of the muscle activity patterns are modulated to meet demands imposed by the various inclines. The distal muscles in general are more tightly controlled than the proximal muscles. The changes in average EMG values are muscle-specific, and are not similar for the stance and swing phases of the step cycle. On average, the proximal muscles show greater increases than the distal muscles. These results are compared with those found previously in the different speed and stride-length condition. Studies such as these shed light on the adaptability of the basic locomotor synergy.     

Movement pattern and upper extremity muscle activation during fast and slow continuous steering movement

Continuous steering movement (CSM) is an essential component of the upper extremity (UE) task during vehicle driving, and could be a suitable candidate for multi-joint rehabilitation programs for patients with UE disabilities. This study aims to evaluate the UE muscle activation during CSM and how the rotating speed and direction affect CSM's kinematic and kinetic performance. Surface electromyography (EMG), hand contact information, and steering torque were measured under fast (180°/s) and slow (60°/s) constant-velocity CSM to reveal the activation of shoulder and elbow muscles, temporal characteristics, and force exertion during the stance and swing phases of a CSM cycle. Data from 24 normal young adults showed that shorter contact duration but higher force exertion occurred in the hand moving in an outward steering direction during only fast CSM in either the clockwise (CW) or counterclockwise (CCW) direction. During a steering cycle (either fast or slow speed), the triceps brachii, sternal part of the pectoralis major (PS), and posterior deltoid play major roles in generating steering torque in the CW direction of the CSM. In contrast, the PS, clavicular part of the pectoralis major (PC), and anterior deltoid (AD) largely contribute to torque generation during the CCW CSM. During the swing phase of CSM, AD, PC, and PS are the major muscles that move the hand for the next grasping of the steering wheel in all four conditions. Using the mean activation profiles of the major contributing muscles, the functional roles of these elbow and shoulder muscles were analyzed and are discussed herein. These findings help us to further understand the activation patterns of UE muscles and the kinematic and kinetic changes during two rotating directions and two speeds of CSM, and suggest important implications for future practice in clinical training.     

Influence of swing leg movement on running stability

The aim of this study was to investigate the role of the swing leg movement on running stability. A simple model was used describing a forward hopping motion. The model consisted of two sub-models, namely a spring-mass system for the stance phase and a functional control model for the swing phase (represented by a passive or actively driven pendulum). To verify the main simulation results, an experimental study on treadmill running was performed. The results of the model indicated that for certain running speeds and pendulum lengths, the behavior of the mechanical system was stable. The following characteristic dependencies between the model parameters were observed. (1) Pendulum length and hip muscle activity determined running height and therefore swing duration. (2) Horizontal velocity was inversely related to leg angle of attack. Increased speed corresponded to flatter leg angles at touch-down, which is in agreement with experimental studies and previous predictions of spring-mass running. It was shown that a biologically motivated control approach with oscillating leg movements is well capable of generating stable hopping movements. Due to its simplicity, however, the monopedal model failed to explain more detailed mechanisms like the swing-leg to stance-leg interaction or the functional role of the leg segmentation. This simple model is therefore considered as a functional mechanical template for legged locomotion, which could help to build more elaborate models in the future.     

A linked muscular activation model for movement generation and control

A new model for movement control is presented which incorporates characteristics of impulse-variability and mass-spring models. Movements in the model were controlled with phasic torque impulses in agonist and antagonist muscles and a tonic agonist torque. Characteristics of the phasic agonist and antagonist torque profiles were based on observed properties of movement-related EMGs and muscle isometric torques. Variability of the phasic impulses depended on impulse magnitude as in impulse-variability models. The model therefore predicted a speed-accuracy tradeoff for limb movement. The time of onset and magnitude of the antagonist torque depended on the magnitude of the preceding agonist torque as indicated in studies of movement-related EMGs. This led to the new concept of linkage between the agonist and antagonist muscle forces which was shown to be important for reducing variability of fast movements. Progressive development of linkage during practice could explain the previous findings of decreased movement variability with practice coupled with increased variability of movement-related EMGs. It was concluded that an inherently variable motor system deals with the variability associated with generation of large muscle forces by linking the forces produced by opposing muscles. In this way, variability in net joint torques and in movements can be decreased without the need for the nervous system to closely regulate the individual torques.     

Absolute pitch in infancy and adulthood: the role of tonal structure

Despite many similarities in infant and adult auditory processing, the literature suggests that two aspects of music perception, pitch processing and knowledge of tonal structure, change over development. The current experiments assess the use of absolute and relative pitch cues in a tone sequence statistical learning task containing tonal structure. The results suggest that infants preferentially process absolute pitch patterns in continuous tone sequences, supporting the hypothesis that absolute pitch is present in infancy, whereas adults tracked both absolute and relative pitch patterns. Infants and adults detected the tonal structure in the input, suggesting that humans are attuned to basic aspects of tonality early in life.     

A Linked Muscular Activation Model for Movement Generation and Control

A new model for movement control is presented which incorporates characteristics of impulse-variability and mass-spring models. Movements in the model were controlled with phasic torque impulses in agonist and antagonist muscles and a tonic agonist torque.

Characteristics of the phasic agonist and antagonist torque profiles were based on observed properties of movement-related EMGs and muscle isometric torques. Variability of the phasic impulses depended on impulse magnitude as in impulse-variability models. The model therefore predicted a speed-accuracy tradeoff for limb movement. The time of onset and magnitude of the antagonist torque depended on the magnitude of the preceding agonist torque as indicated in studies of movement-related EMGs. This led to the new concept of linkage between the agonist and antagonist muscle forces which was shown to be important for reducing variability of fast movements. Progressive development of linkage during practice could explain the previous findings of decreased movement variability with practice coupled with increased variability of movement-related EMGs.

It was concluded that an inherently variable motor system deals with the variability associated with generation of large muscle forces by linking the forces produced by opposing muscles. In this way, variability in net joint torques and in movements can be decreased without the need for the nervous system to closely regulate the individual torques.