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

Optimization of Muscle Activity for Task-Level Goals Predicts Complex Changes in Limb Forces across Biomechanical Contexts

Optimality principles have been proposed as a general framework for understanding motor control in animals and humans largely based on their ability to predict general features movement in idealized motor tasks. However, generalizing these concepts past proof-of-principle to understand the neuromechanical transformation from task-level control to detailed execution-level muscle activity and forces during behaviorally-relevant motor tasks has proved difficult. In an unrestrained balance task in cats, we demonstrate that achieving task-level constraints center of mass forces and moments while minimizing control effort predicts detailed patterns of muscle activity and ground reaction forces in an anatomically-realistic musculoskeletal model. Whereas optimization is typically used to resolve redundancy at a single level of the motor hierarchy, we simultaneously resolved redundancy across both muscles and limbs and directly compared predictions to experimental measures across multiple perturbation directions that elicit different intra- and interlimb coordination patterns. Further, although some candidate task-level variables and cost functions generated indistinguishable predictions in a single biomechanical context, we identified a common optimization framework that could predict up to 48 experimental conditions per animal (n = 3) across both perturbation directions and different biomechanical contexts created by altering animals' postural configuration. Predictions were further improved by imposing experimentally-derived muscle synergy constraints, suggesting additional task variables or costs that may be relevant to the neural control of balance. These results suggested that reduced-dimension neural control mechanisms such as muscle synergies can achieve similar kinetics to the optimal solution, but with increased control effort (≈2×) compared to individual muscle control. Our results are consistent with the idea that hierarchical, task-level neural control mechanisms previously associated with voluntary tasks may also be used in automatic brainstem-mediated pathways for balance

Broad directional tuning in spinal projections to the cerebellum

1. Spinocerebellar neurons that project in the dorsal spinocerebellar tract (DSCT) receive mono- and polysynaptic inputs from specific sensory receptors in the hindlimb, and they project mossy fiber terminals to the cerebellar vermis. We examined the functional organization of these neurons and found that it relates to whole-limb parameters like limb posture and direction of limb movement. 2. We recorded the activity of 444 DSCT units during passive perturbations of the hind foot in anesthetized cats. The movements were either confined a single joint (the ankle; 234 cells) or involved the entire hindlimb (210 cells). The cells exhibited opposite responses for opposite directions of whole-limb movement, but a variety of response patterns for opposite directions of movement at one joint. We interpret the result to imply that the population encodes information about the whole limb rather than single joints. 3. Most of the 78 neurons recorded during passive limb placements (63%) responded to changes in limb length and also changes in limb orientation. In fact, the activity of most of the cells was broadly tuned with respect to the direction of passive limb movements generated by moving the hind foot in the sagittal plane. Changes in unit activity could be described by a cosine tuning function with respect to foot positions (72% of responses) and directions of foot movement (50%). 4. The similarity of this behavior to that of neurons in the motor cortex and cerebellar nuclei recorded during voluntary movements is consistent with a common neural code to represent the sensorimotor parameters of limb movement

Temporal features of directional tuning by spinocerebellar neurons: relation to limb geometry

1. We showed previously that neurons in the dorsal spinocerebellar tract (DSCT) may encode whole-limb parameters of movement and posture rather than localized proprioceptive information. Neurons were found to respond to hindlimb movements in the sagittal plane with maximum activity for foot placements in one direction and minimum activity for placements in the opposite direction. In contrast, movement direction is not specifically encoded by response activity when movement are restricted to a single joint. 2. We now describe the spatiotemporal characteristics of DSCT directional sensitivity for the responses of 267 neurons to small amplitude (0.5 cm) perturbations of the cat hindlimb. A small platform attached to the left hind foot was perturbed along four or eight directions in the sagittal plane, eliciting significant responses in 261 (98%) of the cells. The responses typically consisted of a sequence of peaks and troughs in poststimulus spike density lasting 150 ms or more following limb perturbation. 3. Peaks of activity in particular poststimulus intervals were broadly tuned for the direction of the perturbation, as determined by fitting the firing rates recorded in response to each perturbation direction to a cosine model. The parameters of the cosine model, namely the amplitude of modulation, the direction of maximum response, and the goodness of fit to the model, were computed for each 4 ms poststimulus interval. The parameters all showed the same tendency to wax and wane with respect to poststimulus time. For each period during which the cell activity was highly correlated with tuning model, the tuning indicated a different best direction. Thus each cell's directional tuning could be characterized by a set of tuning maxima associated with specific poststimulus times, when the amplitude of the tuning reached a local maximum and the fit to the cosine model was highly significant (R2 > 0.85). 4. Directions of the tuning maxima for the total population of cells were not uniformly distributed within particular poststimulus intervals. There was a statistically significant directional bias for upward directed perturbations in the poststimulus interval between 20 and 40 ms, followed by a period of downward bias from 45 to 55 ms. Between 60 and 85 ms, the distribution of tuning maxima was significantly skewed backward, whereas a very strong bias for the forward direction was present at about 100 ms. 5. Because the tuning was determined from responses to a very small perturbations of the limb in a given posture, it was not clear whether the responses were related to specific joint angles or muscle lengths, or whether they somehow represented the kinematics of the whole limb. To address this point, we examined the responses of 95 cells in two animals that were each tested in two different limb positions. One position was an approximation of the normal standing position. The other position consisted of a shortening of the limb axis (with major changes in all joint angles) in one animal, or a rotation of the limb axis backward (with little change in joint angles) in the other. 6. We compared each cell's responses to the same perturbations applied in the two limb positions and found they could be identical, scaled in time or magnitude, or completely different in the two positions. A greater percentage of cells with different responses was found in the experiment with the limb axis rotated. In the other experiment, in which there were major differences in joint angles in the two positions, the responses were mostly the same or scaled in time in the two positions. We also determined the population directional biases for the two positions in each experiment, and found that phase differences between the vectors representing population biases for the two positions were minimized when they were measured relative to the orientation of the limb axis (limb coordinates) rather than to the extrinsic vertical (lab coordinates). 7

Low sensitivity of dorsal spinocerebellar neurons to limb movement speed

This paper reports the effect of limb movement speed on dorsal spinocerebellar tract (DSCT) activity recorded while the cat hindlimb was passively moved through two types of foot trajectories (figure eight and step cycle) at different speeds. While nearly all the DSCT neurons sampled (151/159; 94.5%) were significantly modulated by the direction of foot movement in these trajectories, they were only modestly influenced by movement speed. We quantified the speed effect and also accounted for intrinsic cell variability by computing a variability index (VI) between pairs of responses to trajectories made either at the same or at different speeds. The distribution of same-speed VIs across cells indicated a mean variability of about 10% over a trajectory cycle, whereas the two-speed distributions indicated a mean change of about 25% for a two- to fourfold change in movement speed. We also examined the relative contribution of movement speed to the activity of each DSCT cell by means of a multivariate regression model that also included as predictors the position, movement direction, and interactions between movement and position. We found that 28 of 103 (27.2%) neurons were not sensitive to movement speed. The rest were modulated in varying degrees by changes in speed, and the speed modulation depended on limb position for most of them (54/75). Overall, DSCT speed sensitivity resembles the 0.3-power relationship used to describe the velocity sensitivity of muscle spindles for large muscle stretches. We examined this by recording muscle spindle activity during these passive foot trajectories and found that their speed sensitivity was within the range observed for the DSCT and explained by the 0.3-power law. In total, movement speed accounted for about 15% of the variance in DSCT activity across cells, while the directional component of movement accounted for about 45%. The results suggest a separate processing of sensory information about the two components of movement velocity: namely, its direction and magnitude

Modulation of dorsal spinocerebellar responses to limb movement. II. Effect of sensory input

Dorsal spinocerebellar tract (DSCT) neurons receive converging sensory inputs from muscle, skin, and joint receptors and their cerebellar projection is a product of the spinal sensory processing of movement-related information. We concluded earlier that DSCT activity relates to global rather than to local parameters of hindlimb postures and movement, specifically to a kinematic representation of the limb endpoint. The waveforms of principal components (PCs) derived from an ensemble of DSCT movement responses were found to correlate with either the waveform of the limb axis length or orientation trajectories. It was not clear, however, whether these global representations resulted from neural processing or from biomechanical factors. In this study, we perturbed the limb biomechanical factors by decoupling limb geometry from endpoint position during passively applied limb trajectories patterned after a step cycle. We used two types of perturbations: mechanical constraints that limited joint rotations and electrical stimulation of hindlimb muscles. We found that about half of the 89 cells studied showed statistically different response patterns during the perturbations. We compared the PCs of the altered responses with the PCs of the control responses, and found two basic results. With the joint constraints, >85% of the total variance in both control and changed responses was accounted for by the same five PCs that were also observed in the earlier study. The differences between altered and control responses could be fully accounted for by changes in the PC weighting, suggesting a modulation of global response components rather than an explicit representation of local parameters. With the muscle stimulation, only the first and third PCs were the same for the control and altered responses. The second PC was modified, and additional PCs were also required to account for the altered responses. This suggests that the stimulus parameters were specifically represented in the responses. The changes induced by both types of perturbation affected primarily the weighting or waveform of the second PC, which relates to the limb axis length trajectory. The results are consistent with the suggestion that information about limb orientation and length may be separately modulated

Representation of multiple kinematic parameters of the cat hindlimb in spinocerebellar activity

Dorsal spinocerebellar tract (DSCT) neurons have been shown to transmit signals related to hindlimb position and movement direction in the anesthetized cat. Because both parameters may be encoded by single neurons, we examined the extent to which their representations might occur sequentially or simultaneously by recording unit activity while the hindlimb was moved passively in the sagittal plane by a robot arm. A center-out/out-center paradigm moved the foot 2 cm from a given position radially to eight positions located 45 degrees apart, holding each position for 8 s. Another paradigm moved the foot along various paths to 20 positions distributed throughout most of the limb's workspace. With each paradigm, we could assess the activity related to foot position and the direction of movement to each position. Modulation of unit activity evoked by center-out/out-center movements was determined for each 1-s postmovement interval by use of a cosine tuning model that specified modulation amplitude and preferred direction. Of 125 units tested, 82.4% were significantly modulated (P < 0.05) according to this model. We assessed the relative contributions of position and movement by taking advantage of the fact that directional modulation following out-center movements to a common position could only be related to the movement, whereas that following the center-out movements related to both position and movement. The results suggested a simultaneous modulation by these two parameters. Each cell could be characterized by a similar preferred direction for position or movement modulation and the distribution of preferred directions across cells clustered significantly along an axis close to the limb axis. When the limb axis was rotated, the unit preferred directions rotated similarly, on average. Unexpectedly, we found the activity of more than half the cells to be modulated for > or = 8 s after out-center movements, implying a persistent movement-related activity well after a movement is completed. These findings were confirmed and extended with the second paradigm by using a multivariate regression model that included terms for position, movement, and their multiplicative interaction. The activity of 81.3% of the 97 neurons tested fit the model (R2 > 0.4, P < .0001); 31.6% were modulated exclusively by foot position, and 58.2% simultaneously by both position and movement, with significant interaction. We conclude from our results that DSCT neurons may be modulated simultaneously by limb position and movement, and their preferred directions tend to align with the limb axis. The modulation is interactive such that movement modulation amplitude depends on limb position, and many cells also retain a memory trace of recent movements. The results are discussed in terms of a possible role for the DSCT in encoding limb compliance

Encoding of hindlimb kinematics by spinocerebellar circuitry

Earlier work from our laboratory showed that principal component waveforms (PCs) from an ensemble of DSCT movement responses correlated with either the waveform of the limb axis length or orientation trajectories, suggesting that DSCT circuitry might elaborate an explicit representation of limb endpoint kinematics independent from limb geometry. In this study, we tested this idea by decoupling limb geometry from endpoint position with mechanical constraints that blocked the motion of the knee joint during step-like movements applied passively to the hindlimb of anesthetized cats. Only about half of the 50 cells studied showed statistically different response patterns when the limb was constrained compared to the unconstrained condition (control). However, the PC waveforms extracted from responses that showed significant changes with the knee constrained were found to be identical to those extracted from control responses. Instead, the differences between constrained and control responses could be accounted for by changes in the weighting of PCs suggesting a modulation of global response components rather than an explicit representation of local parameters

Reference frames for spinal proprioception: kinematics based or kinetics based?

This second paper of the series deals with another issue regarding sensorimotor representations in the CNS that has received much attention, namely the relative weighting of kinematic and kinetic representations. The question we address here is the contribution of muscle tension afferent information in dorsal spinocerebellar tract (DSCT) sensory representations of foot position. In five anesthetized cats, we activated major hindlimb muscle groups using electrical stimulation of ventral root filaments while passively positioning of the left hind foot throughout its workspace. In general, as the parameters of the joint angle covariance planes indicated, muscle stimulation did not significantly change hindlimb geometry. We analyzed the effects of the muscle stimulation on DSCT neuronal activity within the framework of a kinematic-based representation of foot position. We used a multivariate regression model described in the companion paper, wherein indicators of the experimental condition were added as firing rate predictors along with the limb axis length and orientation to account for possible effects of muscle stimulation. The results indicated that the response gain of 35/59 neurons studied (59%) was not changed by the muscle activations, although most neurons showed some change in their overall firing level with stimulation of one or more muscles. Most of the neurons responded to pseudorandom stimulation of the same muscle groups with complex temporal patterns of activity. For a subpopulation of 42 neurons, we investigated the extent to which their representation of foot position was affected by a rigid constraint of the knee joint and at least one type of muscle stimulation. Although they could be divided into four subgroups based on significance level cutoffs for the constraint or stimulation effect, these effects were in fact quite distributed. However, when we examined the preferred directions of spatial tuning relative to the limb axis position, we found it was unchanged by muscle stimulation for most cells. Even in those cases in which response gain was altered by muscle stimulation, the cell's preferred direction generally was unaltered. The invariance of preferred direction with muscle stimulation lead us to the conclusion that the reference frame for DSCT coding may be based primarily on limb kinematics