Yann Thibaudier

Split-Belt Walking Alters the Relationship between Locomotor Phases and Cycle Duration across Speeds in Intact and Chronic Spinalized Adult Cats

During overground or treadmill walking, the stance phase and cycle durations are reduced as speed increases, whereas swing phase duration remains relatively invariant. When the speed of the left and right sides is unequal, as is the case during split-belt locomotion or when walking along a circular path, adjustments in stance and swing phases are observed, which could alter the phase/cycle duration relationships. Here, we tested this hypothesis in the left and right hindlimbs of four intact and two chronic spinal-transected adult cats during tied-belt (i.e., equal left and right speeds) and split-belt (i.e., unequal left and right speeds) walking. During split-belt walking, one side (i.e., constant limb) walked at a constant speed while the other side (varying limb) varied its speed from 0.3 to 1.0 m/s. We show that the phase/cycle duration relationships differed in both hindlimbs concurrently during split-belt walking. Specifically, the slope of the phase/cycle duration relationships for the stance/extension phase increased in the varying limb from tied-belt to split-belt walking, whereas that of the swing/flexion phase decreased. In contrast, in the constant limb, the slope of the phase/cycle duration relationships for the stance/extension phase decreased, whereas that of the swing/flexion phase increased. The results were qualitatively similar in intact and spinal-transected cats, indicating that the modulation was mediated within the spinal cord. In conclusion, we propose that neuronal networks within the spinal cord that control left and right hindlimb locomotion can differentially and simultaneously modulate phase variations when the two sides walk at different speeds.

Coordination between the fore- and hindlimbs is bidirectional, asymmetrically organized, and flexible during quadrupedal locomotion in the intact adult cat

Despite the obvious importance of inter-girdle coordination for quadrupedal locomotion in terrestrial mammals, its organization remains poorly understood. Here, we evaluated cycle and phase durations, as well as footfall patterns of four intact adult cats trained to walk on a transverse split-belt treadmill that could independently control fore- and hindlimb speed. When the hindlimbs walked at faster speeds than the forelimbs, an equal rhythm was always maintained between the fore- and hindlimbs, even at the highest fore-hindlimb speed ratio of 1:3 (0.4:1.2 m/s). The locomotor pattern adjusted through changes in both hindlimb stance and swing phase durations, whereas only the forelimb stance phase was affected. In such conditions, when fore- and hindlimb values were compared to those obtained at matched speeds during tied-belt walking (i.e. predicted values based on treadmill speed), hindlimb cycle, stance and swing durations were consistently longer than predicted. On the other hand, forelimb cycle and stance durations were shorter than predicted but only at the highest split-belt speed ratios. Forelimb swing durations were as predicted based on front-belt speed. The sequence of footfall pattern when hindlimb speed was faster was identical to tied-belt walking. In stark contrast, when the forelimbs walked at slightly faster speeds than the hindlimbs, the rhythm between the fore- and hindlimbs broke down. In such conditions, the locomotor pattern was adjusted through changes in stance and swing phase durations in both the fore- and hindlimbs. When the rhythm between the fore- and hindlimbs broke down, hindlimb cycle and phase durations were similar to predicted values, whereas forelimb values were shorter than predicted. Moreover, several additional sequences of footfall patterns were observed. Therefore, the results clearly demonstrate the existence of a bidirectional, asymmetric, and flexible control of inter-girdle coordination during quadrupedal locomotion in the intact adult cat.

Speed-dependent modulation of phase variations on a step-by-step basis and its impact on the consistency of interlimb coordination during quadrupedal locomotion in intact adult cats.

It is well established that stance duration changes more than swing duration for a given change in cycle duration. Small variations in cycle duration are also observed at any given speed on a step-by-step basis. To evaluate the step-by-step effect of speed on phase variations, we measured the slopes of the linear regressions between the phases (i.e., stance, swing) and cycle duration during individual episodes at different treadmill speeds in five adult cats. We also determined the pattern of dominance, defined as the phase that varies most with cycle duration. We found a significant effect of speed on hindlimb phase variations, with significant differences observed between the slowest speed of 0.3 m/s compared with faster speeds. Moreover, although patterns of phase dominance were primarily stance/extensor dominated at the slowest speeds, as speed increased the patterns were increasingly categorized as covarying, whereby both stance/extensor and swing/flexor phases changed in approximately equal proportion with cycle duration. Speed significantly affected the relative duration of support periods as well as interlimb phasing between homolateral and diagonal pairs of limbs but not between homologous pairs of limbs. Speed also significantly affected the consistency of interlimb coordination on a step-by-step basis, being less consistent at the slowest speed of 0.3 m/s compared with faster speeds. We found a strong linear relationship between hindlimb phase variations and the consistency of interlimb coordination. Therefore, results show that phase variations on a step-by-step basis are modulated by speed, which appears to influence the consistency of interlimb coordination.

Spatiotemporal control of interlimb coordination during transverse split-belt locomotion with 1:1 or 2:1 coupling patterns in intact adult cats

Interlimb coordination must be flexible to adjust to an ever-changing environment. Here adjustments in interlimb coordination were quantified during tied-belt (equal speed of the fore- and hindlimbs) and transverse split-belt (unequal speed of the fore- and hindlimbs) locomotion in five intact adult cats. Cats performed tied-belt locomotion at 0.4 m/s and 0.8 m/s. For transverse split-belt locomotion, the forelimbs stepped at 0.4 m/s and 0.8 m/s while the hindlimbs stepped at 0.8 m/s (4F8H condition) and 0.4 m/s (8F4H condition), respectively. In the 8F4H condition, the forelimbs could take two steps within one hindlimb cycle, or a 2:1 forelimb-hindlimb relationship. The sequence of limbs contacting the ground and the duration of support periods were differentially modified if the forelimbs stepped faster or slower than the hindlimbs. During transverse split-belt locomotion, the hindlimbs performed longer strides when the forelimbs took shorter strides. In the 8F4H condition with a 2:1 forelimb-hindlimb relationship, phase and gap intervals for the first and second steps were found around certain values and were not randomly distributed, indicating that a new coupling pattern was established. However, temporal and spatial coordination indexes revealed that bilateral coordination between hindlimbs was less accurate and more variable with a 2:1 coupling pattern. Importantly, the animals did not stumble, indicating that spatial and temporal adjustments in interlimb coordination allowed the animals to maintain dynamic stability. The results provide a better understanding of the spatiotemporal adjustments that take place among the four limbs during locomotion when interlimb coordination is challenged.

Modulation of phase durations, phase variations, and temporal coordination of the four limbs during quadrupedal split-belt locomotion in intact adult cats

Stepping along curvilinear paths produces speed differences between the inner and outer limb(s). This can be reproduced experimentally by independently controlling left and right speeds with split-belt locomotion. Here we provide additional details on the pattern of the four limbs during quadrupedal split-belt locomotion in intact cats. Six cats performed tied-belt locomotion (same speed bilaterally) and split-belt locomotion where one side (constant side) stepped at constant treadmill speed while the other side (varying side) stepped at several speeds. Cycle, stance, and swing durations changed in parallel in homolateral limbs with shorter and longer stance and swing durations on the fast side, respectively, compared with the slow side. Phase variations were quantified in all four limbs by measuring the slopes of the regressions between stance and cycle durations (rSTA) and between swing and cycle durations (rSW). For a given limb, rSTA and rSW were not significantly different from one another on the constant side whereas on the varying side rSTA increased relative to tied-belt locomotion while rSW became more negative. Phase variations were similar for homolateral limbs. Increasing left-right speed differences produced a large increase in homolateral double support on the slow side, while triple-support periods decreased. Increasing left-right speed differences altered homologous coupling, homolateral coupling on the fast side, and coupling between the fast hindlimb and slow forelimb. Results indicate that homolateral limbs share similar control strategies, only certain features of the interlimb pattern adjust, and spinal locomotor networks of the left and right sides are organized symmetrically.

Modulation of forelimb and hindlimb muscle activity during quadrupedal tied-belt and split-belt locomotion in intact cats

The modulation of the neural output to forelimb and hindlimb muscles when the left and right sides step at different speeds from one another in quadrupeds was assessed by obtaining electromyography (EMG) in seven intact adult cats during split-belt locomotion. To determine if changes in EMG during split-belt locomotion were modulated according to the speed of the belt the limb was stepping on, values were compared to those obtained during tied-belt locomotion (equal left-right speeds) at matched speeds. Cats were chronically implanted for EMG, which was obtained from six muscles: biceps brachii, triceps brachii, flexor carpi ulnaris, sartorius, vastus lateralis and medial gastrocnemius. During tied-belt locomotion, cats stepped from 0.4 to 1.0m/s in 0.1m/s increments whereas during split-belt locomotion, cats stepped with left-right speed differences of 0.1 to 0.4m/s in 0.1m/s increments. During tied-belt locomotion, EMG burst durations and mean EMG amplitudes of all muscles respectively decreased and increased with increasing speed. During split-belt locomotion, there was a clear differential modulation of the EMG patterns between flexors and extensors and between the slow and fast sides. Changes in the EMG pattern of some muscles could be explained by the speed of the belt the limb was stepping on, while in other muscles there were clear dissociations from tied-belt values at matched speeds. Therefore, results show that EMG patterns during split-belt locomotion are modulated to meet task requirements partly via signals related to the stepping speed of the homonymous limb and from the other limbs.

Sensory regulation of quadrupedal locomotion: a top-down or bottom-up control system?

Propriospinal pathways are thought to be critical for quadrupedal coordination by coupling cervical and lumbar central pattern generators (CPGs). However, the mechanisms involved in relaying information between girdles remain largely unexplored. Using an in vitro spinal cord preparation in neonatal rats, Juvin and colleagues (Juvin et al. 2012) have recently shown sensory inputs from the hindlimbs have greater influence on forelimb CPGs than forelimb sensory inputs on hindlimb CPGs, in other words, a bottom-up control system. However, results from decerebrate cats suggest a top-down control system. It may be that both bottom-up and top-down control systems exist and that the dominance of one over the other is task or context dependent. As such, the role of sensory inputs in controlling quadrupedal coordination before and after injury requires further investigation.

Effect of stimulating the lumbar skin caudal to a complete spinal cord injury on hindlimb locomotion

Sensory feedback is a potent modulator of the locomotor pattern generated by spinal networks. The purpose of this study was to assess the effect of cutaneous inputs from the back on the spinal-generated locomotor pattern. The spinal cord of six adult cats was transected at low thoracic levels. Cats were then trained to recover hindlimb locomotion. During experiments, the skin overlying lumbar vertebrae L2 to L7 was mechanically stimulated by a small calibrated clip or by manual pinching. Trials without and with cutaneous stimulation were performed at a treadmill speed of 0.4 m/s. Although manually pinching the skin completely stopped hindlimb locomotion and abolished weight support, cutaneous stimulation with the calibrated clip produced smaller effects. Specifically, more focalized cutaneous stimulation with the clip reduced flexor and extensor muscle activity and led to a more caudal positioning of the paw at contact and liftoff. Moreover, cutaneous stimulation with the clip led to a greater number of steps with improper nonplantigrade paw placements at contact and paw drag at the stance-to-swing transition. The most consistent effects on the hindlimb locomotor pattern were observed with cutaneous stimulation at midlumbar levels, from L3 to L5. The results indicate that cutaneous stimulation of the skin modulates the excitability of spinal circuits involved in generating locomotion and weight support, particularly at spinal segments thought to be critical for rhythm generation.

Cutaneous inputs from the back abolish locomotor-like activity and reduce spastic-like activity in the adult cat following complete spinal cord injury

Spasticity is a condition that can include increased muscle tone, clonus, spasms, and hyperreflexia. In this study, we report the effect of manually stimulating the dorsal lumbosacral skin on spontaneous locomotor-like activity and on a variety of reflex responses in 5 decerebrate chronic spinal cats treated with clonidine. Cats were spinalized 1 month before the terminal experiment. Stretch reflexes were evoked by stretching the left triceps surae muscles. Crossed reflexes were elicited by electrically stimulating the right tibial or superficial peroneal nerves. Wind-up of reflex responses was evoked by electrically stimulating the left tibial or superficial peroneal nerves. We found that pinching the skin of the back abolished spontaneous locomotor-like activity. We also found that back pinch abolished the rhythmic activity observed during reflex testing without eliminating the reflex responses. Some of the rhythmic episodes of activity observed during reflex testing were consistent with clonus with an oscillation frequency greater than 3 Hz. Pinching the skin of the back effectively abolished rhythmic activity occurring spontaneously or evoked during reflex testing, irrespective of oscillation frequency. The results are consistent with the hypothesis that locomotion and clonus are produced by common central pattern-generators. Stimulating the skin of the back could prove helpful in managing undesired rhythmic activity in spinal cord-injured humans.

The spinal control of locomotion and step-to-step variability in left-right symmetry from slow to moderate speeds

When speed changes during locomotion, both temporal and spatial parameters of the pattern must adjust. Moreover, at slow speeds the step-to-step pattern becomes increasingly variable. The objectives of the present study were to assess if the spinal locomotor network adjusts both temporal and spatial parameters from slow to moderate stepping speeds and to determine if it contributes to step-to-step variability in left-right symmetry observed at slow speeds. To determine the role of the spinal locomotor network, the spinal cord of 6 adult cats was transected (spinalized) at low thoracic levels and the cats were trained to recover hindlimb locomotion. Cats were implanted with electrodes to chronically record electromyography (EMG) in several hindlimb muscles. Experiments began once a stable hindlimb locomotor pattern emerged. During experiments, EMG and bilateral video recordings were made during treadmill locomotion from 0.1 to 0.4 m/s in 0.05 m/s increments. Cycle and stance durations significantly decreased with increasing speed, whereas swing duration remained unaffected. Extensor burst duration significantly decreased with increasing speed, whereas sartorius burst duration remained unchanged. Stride length, step length, and the relative distance of the paw at stance offset significantly increased with increasing speed, whereas the relative distance at stance onset and both the temporal and spatial phasing between hindlimbs were unaffected. Both temporal and spatial step-to-step left-right asymmetry decreased with increasing speed. Therefore, the spinal cord is capable of adjusting both temporal and spatial parameters during treadmill locomotion, and it is responsible, at least in part, for the step-to-step variability in left-right symmetry observed at slow speeds.