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.

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.

Modular control of limb movements during human locomotion.

The idea that the CNS may control complex interactions by modular decomposition has received considerable attention. We explored this idea for human locomotion by examining limb kinematics. The coordination of limb segments during human locomotion has been shown to follow a planar law for walking at different speeds, directions, and levels of body unloading. We compared the coordination for different gaits. Eight subjects were asked to walk and run on a treadmill at different speeds or to walk, run, and hop over ground at a preferred speed. To explore various constraints on limb movements, we also recorded stepping over an obstacle, walking with the knees flexed, and air-stepping with body weight support. We found little difference among covariance planes that depended on speed, but there were differences that depended on gait. In each case, we could fit the planar trajectories with a weighted sum of the limb length and orientation trajectories. This suggested that limb length and orientation might provide independent predictors of limb coordination. We tested this further by having the subjects step, run, and hop in place, thereby varying only limb length and maintaining limb orientation fixed, and also by marching with knees locked to maintain limb length constant while varying orientation. The results were consistent with a modular control of limb kinematics where limb movements result from a superposition of separate length- and orientation-related angular covariance. The hypothesis finds support in the animal findings that limb proprioception may also be encoded in terms of these global limb parameters.

Coordination of locomotion with voluntary movements in humans.

Muscle activity occurring during human locomotion can be accounted for by five basic temporal activation patterns in a variety of locomotion conditions. Here, we examined how these activation patterns interact with muscle activity required for a voluntary movement. Subjects produced a voluntary movement during locomotion, and we examined the resulting kinematics, kinetics, and EMG activity in 16-31 ipsilateral limb and trunk muscles during the tasks. There were four voluntary tasks added to overground walking (approximately 5 km/h) in which subjects kicked a ball, stepped over an obstacle, or reached down and grasped an object on the floor (weight support on either the right or the left foot). Statistical analyses of EMG waveforms showed that the five basic locomotion patterns were invariantly present in each task, although they could be differently weighted across muscles, suggesting a characteristic locomotion timing of muscle activations. We also observed a separate activation that was timed to the voluntary task. The coordination of locomotion with the voluntary task was accomplished by combining activation timings that were associated separately with the voluntary task and locomotion. Activation associated with the voluntary tasks was either synchronous with the timing for locomotion or had additional activations not represented in the basic locomotion timing. We propose that this superposition of an invariant locomotion timing pattern with a voluntary activation timing may be consistent with the proposal suggesting that compound movements are produced through a superposition of motor programs.

Motor control programs and walking.

The question of how the central nervous system coordinates muscle activity is central to an understanding of motor control. The authors argue that motor programs may be considered as a characteristic timing of muscle activations linked to specific kinematic events. In particular, muscle activity occurring during human locomotion can be accounted for by five basic temporal components in a variety of locomotion conditions. Spatiotemporal maps of spinal cord motoneuron activation also show discrete periods of activity. Furthermore, the coordination of locomotion with voluntary tasks is accomplished through a superposition of motor programs or activation timings that are separately associated with each task. As a consequence, the selection of muscle synergies appears to be downstream from the processes that generate activation timings.

Sophisticated spinal contributions to motor control.

The neural circuitry of the spinal cord is capable of solving some of the most complex problems in motor control. Therefore, spinal mechanisms are much more sophisticated than many neuroscientists give them credit for. A key issue in motor control is how sensory inputs direct and inform motor output,--that is, the sensorimotor process. Other major issues involve the actual control of the motor apparatus. In general, there are at least three basic requirements for motor control: the transformations that map information from sensory to motor coordinates, the specification of individual muscle activations to achieve a kinematic goal, and the control of multiple degrees of freedom. Here, we make the case that the vertebrate spinal cord has the capacity to solve each of these problems to a degree that is relevant for normal behavior.

Locomotor-like leg movements evoked by rhythmic arm movements in humans.

Motion of the upper limbs is often coupled to that of the lower limbs in human bipedal locomotion. It is unclear, however, whether the functional coupling between upper and lower limbs is bi-directional, i.e. whether arm movements can affect the lumbosacral locomotor circuitry. Here we tested the effects of voluntary rhythmic arm movements on the lower limbs. Participants lay horizontally on their side with each leg suspended in an unloading exoskeleton. They moved their arms on an overhead treadmill as if they walked on their hands. Hand-walking in the antero-posterior direction resulted in significant locomotor-like movements of the legs in 58% of the participants. We further investigated quantitatively the responses in a subset of the responsive subjects. We found that the electromyographic (EMG) activity of proximal leg muscles was modulated over each cycle with a timing similar to that of normal locomotion. The frequency of kinematic and EMG oscillations in the legs typically differed from that of arm oscillations. The effect of hand-walking was direction specific since medio-lateral arm movements did not evoke appreciably leg air-stepping. Using externally imposed trunk movements and biomechanical modelling, we ruled out that the leg movements associated with hand-walking were mainly due to the mechanical transmission of trunk oscillations. EMG activity in hamstring muscles associated with hand-walking often continued when the leg movements were transiently blocked by the experimenter or following the termination of arm movements. The present results reinforce the idea that there exists a functional neural coupling between arm and legs.

Locomotor primitives in newborn babies and their development.

How rudimentary movements evolve into sophisticated ones during development remains unclear. It is often assumed that the primitive patterns of neural control are suppressed during development, replaced by entirely new patterns. Here we identified the basic patterns of lumbosacral motoneuron activity from multimuscle recordings in stepping neonates, toddlers, preschoolers, and adults. Surprisingly, we found that the two basic patterns of stepping neonates are retained through development, augmented by two new patterns first revealed in toddlers. Markedly similar patterns were observed also in the rat, cat, macaque, and guineafowl, consistent with the hypothesis that, despite substantial phylogenetic distances and morphological differences, locomotion in several animal species is built starting from common primitives, perhaps related to a common ancestral neural network.