A simple neuromechanical model has been developed that describes a spinal central pattern generator (CPG) controlling the locomotor movement of a single-joint limb via activation of two antagonist (flexor and extensor) muscles. The limb performs rhythmic movements under control of the muscular, gravitational and ground reaction forces. Muscle afferents provide length-dependent (types Ia and II) and force-dependent (type Ib from the extensor) feedback to the CPG. We show that afferent feedback adjusts CPG operation to the kinematics and dynamics of the limb providing stable “locomotion.” Increasing the supraspinal drive to the CPG increases locomotion speed by reducing the duration of stance phase. We show that such asymmetric, extensor-dominated control of locomotor speed (with relatively constant swing duration) is provided by afferent feedback independent of the asymmetric rhythmic pattern generated by the CPG alone (in “fictive locomotion” conditions). Finally, we demonstrate the possibility of reestablishing stable locomotion after removal of the supraspinal drive (associated with spinal cord injury) by increasing the weights of afferent inputs to the CPG, which is thought to occur following locomotor training.

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Cutaneous sensory feedback from the paw pads plays an important role in regulating body balance, especially in challenging environments like ladder or slope walking. Here, we investigated the contribution of cutaneous sensory feedback from the paw pads to balance control in cats stepping on a split-belt treadmill. Fore- and hindpaws were anesthetized unilaterally using lidocaine injections. We evaluated body balance in intact and compromised cutaneous feedback conditions during split-belt locomotion with belt speed ratios of 0.5, 1.0, 1.5 and 2.0. Measures of body balance included step width, relative duration of limb support phases, lateral bias of center of mass (CoM) and margins of static and dynamic stability. In the intact condition, static and dynamic balance declined with increasing belt-speed ratio due to a lateral shift of the CoM toward the borders of support on the slower moving belt. Anesthesia of the ipsilateral paws improved locomotor balance with increasing belt speed ratios by reversing the CoM shift, decreasing the relative duration of the two-limb support phase, increasing the duration of four- or three-limb support phases, increasing the hindlimb step width and static stability. We observed no changes in most balance measures in anesthetized conditions during tied-belt locomotion at 0.4 m s−1. CoM lateral displacements closely resembled those of the inverted pendulum and of human walking. We propose that unilaterally compromised cutaneous feedback from the paw pads is compensated by improving lateral balance and by shifting the body toward the anesthetized paws to increase tactile sensation during the stance phase.

Animal locomotion requires changing direction, from forward to backward. Here, we tested the hypothesis that sensorimotor circuits within the spinal cord generate backward locomotion and adjust it to task demands. We collected kinematic and electromyography (EMG) data during forward and backward locomotion at different treadmill speeds before and after complete spinal transection in six adult cats (three males and three females). After spinal transection, five/six cats performed backward locomotion, which required tonic somatosensory input in the form of perineal stimulation. One spinal cat performed forward locomotion but not backward locomotion while two others stepped backward but not forward. Spatiotemporal adjustments to increasing speed were similar in intact and spinal cats during backward locomotion and strategies were similar to forward locomotion, with shorter cycle and stance durations and longer stride lengths. Patterns of muscle activations, including muscle synergies, were similar for forward and backward locomotion in spinal cats. Indeed, we identified five muscle synergies that were similar during forward and backward locomotion. Lastly, spinal cats also stepped backward on a split-belt treadmill, with the left and right hindlimbs stepping at different speeds. Therefore, our results show that spinal sensorimotor circuits generate backward locomotion but require additional excitability compared with forward locomotion. Similar strategies for speed modulation and similar patterns of muscle activations and muscle synergies during forward and backward locomotion are consistent with a shared spinal locomotor network, with sensory feedback from the limbs controlling the direction.

We investigated which of cat limb kinematic variables during swing of regular walking and accurate stepping along a horizontal ladder are stabilized by coordinated changes of limb segment angles. Three hypotheses were tested: 1) animals stabilize the entire swing trajectory of specific kinematic variables (performance variables); and 2) the level of trajectory stabilization is similar between regular and ladder walking and 3) is higher for forelimbs compared with hindlimbs. We used the framework of the uncontrolled manifold (UCM) hypothesis to quantify the structure of variance of limb kinematics in the limb segment orientation space across steps. Two components of variance were quantified for each potential performance variable, one of which affected it ("bad variance," variance orthogonal to the UCM, VORT) while the other one did not ("good variance," variance within the UCM, VUCM). The analysis of five candidate performance variables revealed that cats during both locomotor behaviors stabilize 1) paw vertical position during the entire swing (VUCM > VORT, except in mid-hindpaw swing of ladder walking) and 2) horizontal paw position in initial and terminal swing (except for the entire forepaw swing of regular walking). We also found that the limb length was typically stabilized in midswing, whereas limb orientation was not (VUCM ≤ VORT) for both limbs and behaviors during entire swing. We conclude that stabilization of paw position in early and terminal swing enables accurate and stable locomotion, while stabilization of vertical paw position in midswing helps paw clearance. This study is the first to demonstrate the applicability of the UCM-based analysis to nonhuman movement.

Our previous study of cat locomotion demonstrated that lateral displacements of the centre of mass (COM) were strikingly similar to those of human walking and resembled the behaviour of an inverted pendulum (Park et al. 2019 J. Exp. Biol. 222 , 14. (doi:10.1242/jeb.198648)). Here, we tested the hypothesis that frontal plane dynamics of quadrupedal locomotion are consistent with an inverted pendulum model. We developed a simple mathematical model of balance control in the frontal plane based on an inverted pendulum and compared model behaviour with that of four cats locomoting on a split-belt treadmill. The model accurately reproduced the lateral oscillations of cats' COM vertical projection. We inferred the effects of experimental perturbations on the limits of dynamic stability using data from different split-belt speed ratios with and without ipsilateral paw anaesthesia. We found that the effect of paw anaesthesia could be explained by the induced bias in the perceived position of the COM, and the magnitude of this bias depends on the belt speed difference. Altogether, our findings suggest that the balance control system is actively involved in cat locomotion to provide dynamic stability in the frontal plane, and that paw cutaneous receptors contribute to the representation of the COM position in the nervous system.

Although it is well established that the motor control system is modular, the organization of muscle synergies during locomotion and their change with ground slope are not completely understood. For example, typical reciprocal flexor-extensor muscle synergies of level walking in cats break down in downslope: one-joint hip extensors are silent throughout the stride cycle, whereas hindlimb flexors demonstrate an additional stance phase-related EMG burst (Smith et al. 1998a). Here we investigated muscle synergies during Level, Upslope (27o) and Downslope (-27o) walking in adult cats to examine common and distinct features of modular organization of locomotor EMG activity. Cluster analysis of EMG burst onset-offset times of 12 hindlimb muscles revealed 5 flexor and extensor burst groups that were generally shared across slopes. Stance-related bursts of flexor muscles in downslope were placed in a burst group from Level and Upslope walking formed by the rectus femoris. Walking Upslope changed swing/stance phase durations of Level walking but not the cycle duration. Five muscle synergies computed using non-negative matrix factorization accounted for at least 95% of variance in EMG patterns in each slope. Five synergies were shared between Level and Upslope walking, whereas only 3 of those were shared with Downslope synergies; these synergies were active during the swing phase and phase transitions. Two stance-related synergies of downslope walking were distinct; they comprised a mixture of flexors and extensors. We suggest that the modular organization of muscle activity during Level and Slope walking results from interactions between motion-related sensory feedback, CPG, and supraspinal inputs.