Richard E. Poppele

Five basic muscle activation patterns account for muscle activity during human locomotion

An electromyographic (EMG) activity pattern for individual muscles in the gait cycle exhibits a great deal of intersubject, intermuscle and context‐dependent variability. Here we examined the issue of common underlying patterns by applying factor analysis to the set of EMG records obtained at different walking speeds and gravitational loads. To this end healthy subjects were asked to walk on a treadmill at speeds of 1, 2, 3 and 5kmh−1 as well as when 35–95% of the body weight was supported using a harness. We recorded from 12–16 ipsilateral leg and trunk muscles using both surface and intramuscular recording and determined the average, normalized EMG of each record for 10–15 consecutive step cycles. We identified five basic underlying factors or component waveforms that can account for about 90% of the total waveform variance across different muscles during normal gait. Furthermore, while activation patterns of individual muscles could vary dramatically with speed and gravitational load, both the limb kinematics and the basic EMG components displayed only limited changes. Thus, we found a systematic phase shift of all five factors with speed in the same direction as the shift in the onset of the swing phase. This tendency for the factors to be timed according to the lift‐off event supports the idea that the origin of the gait cycle generation is the propulsion rather than heel strike event. The basic invariance of the factors with walking speed and with body weight unloading implies that a few oscillating circuits drive the active muscles to produce the locomotion kinematics. A flexible and dynamic distribution of these basic components to the muscles may result from various descending and proprioceptive signals that depend on the kinematic and kinetic demands of the movements.

Locomotor Primitives in Newborn Babies and Their Development

Mammalian locomotion patterns share common roots. 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.

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 (∼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.

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.

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.

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.

On the Origin of Planar Covariation of Elevation Angles During Human Locomotion

Leg segment rotations in human walking covary, so that the three-dimensional trajectory of temporal changes in the elevation angles lies close to a plane. Recently the role of central versus biomechanical constraints on the kinematics control of human locomotion has been questioned. Here we show, based on both modeling and experimental data, that the planar law of intersegmental coordination is not a simple consequence of biomechanics. First, the full limb behavior in various locomotion modes (walking on inclined surface, staircase stepping, air-stepping, crouched walking, hopping) can be expressed as 2 degrees of freedom planar motion even though the orientation of the plane and pairwise segment angle correlations may differ substantially. Second, planar covariation is not an inevitable outcome of any locomotor movement. It can be systematically violated in some conditions (e.g., when stooping and grasping an object on the floor during walking or in toddlers at the onset of independent walking) or transferred into a simple linear relationship in others (e.g., during stepping in place). Finally, all three major limb segments contribute importantly to planar covariation and its characteristics resulting in a certain endpoint trajectory defined by the limb axis length and orientation. Recent advances in the neural control of movement support the hypothesis about central representation of kinematics components.

Myotatic Reflex: Its Input-Output Relation

The dynamic properties of the myotatic reflex and of its components were determined by a systems-analysis approach. The gain and phase relations between an applied stretch, whiclh initiates the reflex, and the output of the primary mulscle spindles, which impinge upon α-motoneurons, are not further changed by the properties of the motoneurons. The dynamic relation between motoneuron activity and the resultant muscle tension balances these changes in gain and phase; the result is a flat gain and nearly zero phase difference between stretch and tension produced by the myotatic reflex. Moreover, the distribution of activity in multiple channels extends the range in which the overall reflex is linear.

Spatiotemporal organization of α‐motoneuron activity in the human spinal cord during different gaits and gait transitions

Here we studied the spatiotemporal organization of motoneuron (MN) activity during different human gaits. We recorded the electromyographic (EMG) activity patterns in 32 ipsilateral limb and trunk muscles from normal subjects while running and walking on a treadmill (3–12 km/h). In addition, we recorded backward walking and skipping, a distinct human gait that comprises the features of both walking and running. We mapped the recorded EMG activity patterns onto the spinal cord in approximate rostrocaudal locations of the MN pools. The activation of MNs tends to occur in bursts and be segregated by spinal segment in a gait‐specific manner. In particular, sacral and cervical activation timings were clearly gait‐dependent. Swing‐related activity constituted an appreciable fraction (> 30%) of the total MN activity of leg muscles. Locomoting at non‐preferred speeds (running and walking at 5 and 9 km/h, respectively) showed clear differences relative to preferred speeds. Running at low speeds was characterized by wider sacral activation. Walking at high non‐preferred speeds was accompanied by an ‘atypical’ locus of activation in the upper lumbar spinal cord during late stance and by a drastically increased activation of lumbosacral segments. The latter findings suggest that the optimal speed of gait transitions may be related to an optimal intensity of the total MN activity, in addition to other factors previously described. The results overall support the idea of flexibility and adaptability of spatiotemporal activity in the spinal circuitry with constraints on the temporal functional connectivity of hypothetical pulsatile burst generators.