Neuromuscular adjustments of gait associated with unstable conditions.

A compact description of coordinated muscle activity is provided by the factorization of electromyographic (EMG) signals. With the use of this approach, it has consistently been shown that multimuscle activity during human locomotion can be accounted for by four to five modules, each one comprised of a basic pattern timed at a different phase of gait cycle and the weighting coefficients of synergistic muscle activations. These modules are flexible, in so far as the timing of patterns and the amplitude of weightings can change as a function of gait speed and mode. Here we consider the adjustments of the locomotor modules related to unstable walking conditions. We compared three different conditions, i.e., locomotion of healthy subjects on slippery ground (SL) and on narrow beam (NB) and of cerebellar ataxic (CA) patients on normal ground. Motor modules were computed from the EMG signals of 12 muscles of the right lower limb using non-negative matrix factorization. The unstable gait of SL, NB, and CA showed significant changes compared with controls in the stride length, stride width, range of angular motion, and trunk oscillations. In most subjects of all three unstable conditions, >70% of the overall variation of EMG waveforms was accounted for by four modules that were characterized by a widening of muscle activity patterns. This suggests that the nervous system adopts the strategy of prolonging the duration of basic muscle activity patterns to cope with unstable conditions resulting from either slippery ground, reduced support surface, or pathology.

Locomotor patterns in cerebellar ataxia.

Several studies have demonstrated how cerebellar ataxia (CA) affects gait, resulting in deficits in multijoint coordination and stability. Nevertheless, how lesions of cerebellum influence the locomotor muscle pattern generation is still unclear. To better understand the effects of CA on locomotor output, here we investigated the idiosyncratic features of the spatiotemporal structure of leg muscle activity and impairments in the biomechanics of CA gait. To this end, we recorded the electromyographic (EMG) activity of 12 unilateral lower limb muscles and analyzed kinematic and kinetic parameters of 19 ataxic patients and 20 age-matched healthy subjects during overground walking. Neuromuscular control of gait in CA was characterized by a considerable widening of EMG bursts and significant temporal shifts in the center of activity due to overall enhanced muscle activation between late swing and mid-stance. Patients also demonstrated significant changes in the intersegmental coordination, an abnormal transient in the vertical ground reaction force and instability of limb loading at heel strike. The observed abnormalities in EMG patterns and foot loading correlated with the severity of pathology [International Cooperative Ataxia Rating Scale (ICARS), a clinical ataxia scale] and the changes in the biomechanical output. The findings provide new insights into the physiological role of cerebellum in optimizing the duration of muscle activity bursts and the control of appropriate foot loading during locomotion.

Spatiotemporal characteristics of muscle patterns for ball catching.

What sources of information and what control strategies the central nervous system (CNS) uses to perform movements that require accurate sensorimotor coordination, such as catching a flying ball, is still debated. Here we analyzed the EMG waveforms recorded from 16 shoulder and elbow muscles in six subjects during catching of balls projected frontally from a distance of 6 m and arriving at two different heights and with three different flight times (550, 650, 750 ms). We found that a large fraction of the variation in the muscle patterns was captured by two time-varying muscle synergies, coordinated recruitment of groups of muscles with specific activation waveforms, modulated in amplitude and shifted in time according to the ball's arrival height and flight duration. One synergy was recruited with a short and fixed delay from launch time. Remarkably, a second synergy was recruited at a fixed time before impact, suggesting that it is timed according to an accurate time-to-contact estimation. These results suggest that the control of interceptive movements relies on a combination of reactive and predictive processes through the intermittent recruitment of time-varying muscle synergies. Knowledge of the dynamic effect of gravity and drag on the ball may be then implicitly incorporated in a direct mapping of visual information into a small number of synergy recruitment parameters.

A new ball launching system with controlled flight parameters for catching experiments.

Systematic investigations of sensorimotor control of interceptive actions in naturalistic conditions, such as catching or hitting a ball moving in three-dimensional space, requires precise control of the projectile flight parameters and of the associated visual stimuli. Such control is challenging when air drag cannot be neglected because the mapping of launch parameters into flight parameters cannot be computed analytically. We designed, calibrated, and experimentally validated an actuated launching apparatus that can control the average spatial position and flight duration of a ball at a given distance from a fixed launch location. The apparatus was constructed by mounting a ball launching machine with adjustable delivery speed on an actuated structure capable of changing the spatial orientation of the launch axis while projecting balls through a hole in a screen hiding the apparatus. The calibration procedure relied on tracking the balls with a motion capture system and on approximating the mapping of launch parameters into flight parameters by means of polynomials functions. Polynomials were also used to estimate the variability of the flight parameters. The coefficients of these polynomials were obtained using the launch and flight parameters of 660 launches with 65 different initial conditions. The relative accuracy and precision of the apparatus were larger than 98% for flight times and larger than 96% for ball heights at a distance of 6m from the screen. Such novel apparatus, by reliably and automatically controlling desired ball flight characteristics without neglecting air drag, allows for a systematic investigation of naturalistic interceptive tasks.

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.

Combining modules for movement.

We review experiments supporting the hypothesis that the vertebrate motor system produces movements by combining a small number of units of motor output. Using a variety of approaches such as microstimulation of the spinal cord, NMDA iontophoresis, and an examination of natural behaviors in intact and deafferented animals we have provided evidence for a modular organization of the spinal cord. A module is a functional unit in the spinal cord that generates a specific motor output by imposing a specific pattern of muscle activation. Such an organization might help to simplify the production of movements by reducing the degrees of freedom that need to be specified.

Modular organization of spinal motor systems.

The vertebrate nervous system produces a wide range of movement flexibly and efficiently, even though the simplest of these movements is potentially highly complex. The strategies by which the nervous system overcomes these complexities have therefore been of interest to motor physiologists for decades. In this review, the authors present a number of recent experiments that propose one strategy by which the nervous system might simplify the production of movement. These experiments suggest that spinal motor systems are organized in terms of a small number of distinct motor responses, or "modules." These distinct modules can be combined together simply to produce a wide range of different movements. Such a modular organization of spinal motor systems can potentially allow the nervous system to produce a wide range of natural behaviors in a simple and flexible manner.

Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog.

This paper relates to the problem of the existence of muscle synergies, that is whether the CNS command to muscles is simplified by controlling their activity in subgroups or synergies, rather than individually. We approach this problem with two methods that have been recently introduced: intraspinal N-methyl-D-aspartate (NMDA) microstimulation and a synergy-extracting algorithm. To search for a common set of synergies encoded for by the spinal cord whose combinations would account for a large range of electromyographic (EMG) patterns, we chose, rather than examining a large range of natural behaviors, to chemically microstimulate a large number of spinal cord interneuronal sites in different frogs. A possible advantage of this complementary method is that it is task-independent. Visual inspection suggested that the NMDA-elicited EMG patterns recorded from 12 leg muscles might indeed be constructed from smaller subgroups of muscles whose activity co-varied, suggestive of synergies. We used a modification of our extracting computational algorithm whereby a nonnegative least-squares method was employed to iteratively update both the synergies and their coefficients of activation in reconstructing the EMG patterns. Using this algorithm, a limited set of seven synergies was found whose linear combinations accounted for more than 91% of the variance in the pooled EMG data from 10 frogs, and more than 96% in individual frogs. The extracted synergies were similar among frogs. Further, preferred combinations of these synergies were clearly identified. This was found by extracting smaller sets of four, five, or six synergies and fitting each synergy from those sets as a combination from the set of seven synergies extracted from the same frog; the synergy combinations from each frog were then pooled together to examine their frequency of occurrence. Concordance with this method of identifying synergy combinations was found by examining how the synergies from the set of seven correlated pair-wise as they reconstructed the EMG data. These results support the existence of muscle synergies encoded within the spinal cord, which through preferred combinations, account for a large repertoire of spinal cord motor output. These findings are contrasted with previous approaches to the problem of synergies.

New perspectives on spinal motor systems.

The production and control of complex motor functions are usually attributed to central brain structures such as cortex, basal ganglia and cerebellum. In traditional schemes the spinal cord is assigned a subservient function during the production of movement, playing a predominantly passive role by relaying the commands dictated to it by supraspinal systems. This review challenges this idea by presenting evidence that the spinal motor system is an active participant in several aspects of the production of movement, contributing to functions normally ascribed to 'higher' brain regions.

Low dimensionality of supraspinally induced force fields.

Recent experiments using electrical and N-methyl-D-aspartate microstimulation of the spinal cord gray matter and cutaneous stimulation of the hindlimb of spinalized frogs have provided evidence for a modular organization of the frog's spinal cord circuitry. A "module" is a functional unit in the spinal cord circuitry that generates a specific motor output by imposing a specific pattern of muscle activation. The output of a module can be characterized as a force field: the collection of the isometric forces generated at the ankle over different locations in the leg's workspace. Different modules can be combined independently so that their force fields linearly sum. The goal of this study was to ascertain whether the force fields generated by the activation of supraspinal structures could result from combinations of a small number of modules. We recorded a set of force fields generated by the electrical stimulation of the vestibular nerve in seven frogs, and we performed a principal component analysis to study the dimensionality of this set. We found that 94% of the total variation of the data is explained by the first five principal components, a result that indicates that the dimensionality of the set of fields evoked by vestibular stimulation is low. This result is compatible with the hypothesis that vestibular fields are generated by combinations of a small number of spinal modules.