Key pointsr Coordination between the left and right sides is essential for dynamic stability during locomotion.r The immature or neonatal mammalian spinal cord can adjust to differences in speed between the left and right sides during split-belt locomotion by taking more steps on the fast side.r We show that the adult mammalian spinal cord can also adjust its output so that the fast side can take more steps.r During split-belt locomotion, only certain parts of the cycle are modified to adjust left-right coordination, primarily those associated with swing onset.r When the fast limb takes more steps than the slow limb, strong left-right interactions persist. r Therefore, the adult mammalian spinal cord has a remarkable adaptive capacity for left-right coordination, from simple to extreme conditions. Abstract Although left-right coordination is essential for locomotion, its control is poorly understood, particularly in adult mammals. To investigate the spinal control of left-right coordination, a spinal transection was performed in six adult cats that were then trained to recover hindlimb locomotion. Spinal cats performed tied-belt locomotion from 0.1 to 1.0 m s −1 and split-belt locomotion with low to high (1:1.25-10) slow/fast speed ratios. With the left hindlimb stepping at 0.1 m s −1 and the right hindlimb stepping from 0.2 to 1.0 m s −1 , 1:1, 1:2, 1:3, 1:4 and 1:5 left-right step relationships could appear. The appearance of 1:2+ relationships was not linearly dependent on the difference in speed between the slow and fast belts. The last step taken by the fast hindlimb displayed longer cycle, stance and swing durations and increased extensor activity, as the slow limb transitioned to swing. During split-belt locomotion with 1:1, 1:2 and 1:3 relationships, the timing of stance onset of the fast limb relative to the slow limb and placement of both limbs at contact were invariant with increasing slow/fast speed ratios. In contrast, the timing of stance onset of the slow limb relative to the fast limb and the placement of both limbs at swing onset were modulated with slow/fast speed ratios. Thus, left-right coordination is adjusted by modifying specific parts of the cycle. Results highlight the remarkable adaptive capacity of the adult mammalian spinal cord, providing insight into spinal mechanisms and sensory signals regulating left-right coordination.

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.

When the foot contacts an obstacle during locomotion, cutaneous inputs activate spinal circuits to ensure dynamic balance and forward progression. In quadrupeds, this requires coordinated reflex responses between the four limbs. Here, we investigated the patterns and phasic modulation of cutaneous reflexes in forelimb and hindlimb muscles evoked by inputs from all four limbs. Five female cats were implanted to record muscle activity and to stimulate the superficial peroneal and superficial radial nerves during locomotion. Stimulating these nerves evoked short-, mid-, and longer-latency excitatory and/or inhibitory responses in all four limbs that were phase-dependent. The largest responses were generally observed during the peak activity of the muscle. Cutaneous reflexes during mid-swing were consistent with flexion of the homonymous limb and accompanied by modification of the stance phases of the other three limbs, by coactivating flexors and extensors and/or by delaying push-off. Cutaneous reflexes during mid-stance were consistent with stabilizing the homonymous limb by delaying and then facilitating its push-off and modifying the support phases of the homolateral and diagonal limbs, characterized by coactivating flexors and extensors, reinforcing extensor activity and/or delaying push-off. The shortest latencies of homolateral and diagonal responses were consistent with fast-conducting disynaptic or trisynaptic pathways. Descending homolateral and diagonal pathways from the forelimbs to the hindlimbs had a higher probability of eliciting responses compared with ascending pathways from the hindlimbs to the forelimbs. Thus, in quadrupeds, intralimb and interlimb reflexes activated by cutaneous inputs ensure dynamic coordination of the four limbs, producing a whole-body response. The skin contains receptors that, when activated, send inputs to spinal circuits, signaling a perturbation. Rapid responses, or reflexes, in muscles of the contacted limb and opposite homologous limb help maintain balance and forward progression. Here, we investigated reflexes during quadrupedal locomotion in the cat by electrically stimulating cutaneous nerves in each of the four limbs. Functionally, responses appear to modify the trajectory or stabilize the movement of the stimulated limb while modifying the support phase of the other limbs. Reflexes between limbs are mediated by fast-conducting pathways that involve excitatory and inhibitory circuits controlling each limb. The comparatively stronger descending pathways from cervical to lumbar circuits controlling the forelimbs and hindlimbs, respectively, could serve a protective function.

Cutaneous reflexes are important for responding rapidly to perturbations, correcting limb trajectory, and strengthening support. During locomotion, they are modulated by phase to generate functionally appropriate responses. The goal of the present study was to determine whether cutaneous reflexes and their phase-dependent modulation are altered with increasing speed and if this is accomplished at the spinal level. Four adult cats that recovered stable hindlimb locomotion after spinal transection were implanted with electrodes to record hindlimb muscle activity chronically and to stimulate the superficial peroneal nerve electrically to evoke cutaneous reflexes. The speed-dependent modulation of cutaneous reflexes was assessed by evoking and characterizing ipsilateral and contralateral responses in semitendinosus, vastus lateralis, and lateral gastrocnemius muscles at four treadmill speeds: 0.2, 0.4, 0.6, and 0.8 m/s. The amplitudes of ipsilateral and contralateral responses were largest at intermediate speeds of 0.4 and 0.6 m/s, followed by the slowest and fastest speeds of 0.2 and 0.8 m/s, respectively. The phase-dependent modulation of reflexes was maintained across speeds, with ipsilateral and contralateral responses peaking during the stance-to-swing transition and swing phase of the ipsilateral limb or midstance of the contralateral limb. Reflex modulation across speeds also correlated with the spatial symmetry of the locomotor pattern, but not with temporal symmetry. That the cutaneous reflex amplitude in all muscles was similarly modulated with increasing speed independently of the background level of muscle activity is consistent with a generalized premotoneuronal spinal control mechanism that could help to stabilize the locomotor pattern when changing speed. When walking, receptors located in the skin respond to mechanical pressure and send signals to the CNS to correct the trajectory of the limb and to reinforce weight support. These signals produce different responses, or reflexes, if they occur when the foot is contacting the ground or in the air. This is known as phase-dependent modulation of reflexes. However, when walking at faster speeds, we do not know if and how these reflexes are changed. In the present study, we show that reflexes from the skin are modulated with speed and that this is controlled at the level of the spinal cord. This modulation could be important in preventing sensory signals from destabilizing the walking pattern.

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