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IntroductionDuring locomotion, cutaneous reflexes play an essential role in rapidly responding to an external perturbation, for example, to prevent a fall when the foot contacts an obstacle. In cats and humans, cutaneous reflexes involve all four limbs and are task- and phase modulated to generate functionally appropriate whole-body responses.MethodsTo assess task-dependent modulation of cutaneous interlimb reflexes, we electrically stimulated the superficial radial or superficial peroneal nerves in adult cats and recorded muscle activity in the four limbs during tied-belt (equal left-right speeds) and split-belt (different left-right speeds) locomotion.ResultsWe show that the pattern of intra- and interlimb cutaneous reflexes in fore- and hindlimbs muscles and their phase-dependent modulation were conserved during tied-belt and split-belt locomotion. Short-latency cutaneous reflex responses to muscles of the stimulated limb were more likely to be evoked and phase-modulated when compared to muscles in the other limbs. In some muscles, the degree of reflex modulation was significantly reduced during split-belt locomotion compared to tied-belt conditions. Split-belt locomotion increased the step-by-step variability of left-right symmetry, particularly spatially.DiscussionThese results suggest that sensory signals related to left-right symmetry reduce cutaneous reflex modulation, potentially to avoid destabilizing an unstable pattern.

Spinal sensorimotor circuits interact with supraspinal and peripheral inputs to generate quadrupedal locomotion. Ascending and descending spinal pathways ensure coordination between the fore- and hindlimbs. Spinal cord injury disrupts these pathways. To investigate control of interlimb coordination and hindlimb locomotor recovery, we performed two lateral thoracic hemisections on opposite sides of the cord (right T5-T6 and left T10-T11) at an interval of approximately two months in eight adult cats. In three cats, the spinal cord was transected at T12-T13. We collected electromyography and kinematic data during quadrupedal and hindlimb-only locomotion before and after spinal lesions. We show that 1) cats spontaneously recover quadrupedal locomotion following staggered hemisections but require balance assistance after the second one, 2) coordination between the fore- and hindlimbs displays 2:1 patterns (two cycles of one forelimb within one hindlimb cycle) and becomes weaker and more variable after both hemisections, 3) left-right asymmetries in hindlimb stance and swing durations appear after the first hemisection and reverse after the second, and 4) support periods reorganize after staggered hemisections to favor support involving both forelimbs and diagonal limbs. Cats expressed hindlimb locomotion the day following spinal transection, indicating that lumbar sensorimotor circuits play a prominent role in hindlimb locomotor recovery after staggered hemisections. These results reflect a series of changes in spinal sensorimotor circuits that allow cats to maintain and recover some level of quadrupedal locomotor functionality with diminished motor commands from the brain and cervical cord, although the control of posture and interlimb coordination remains impaired.Significance StatementCoordinating the limbs during locomotion depends on pathways in the spinal cord. We used a spinal cord injury model that disrupts communication between the brain and spinal cord by sectioning half of the spinal cord on one side and then about two months later, half the spinal cord on the other side at different levels of the thoracic cord in cats. We show that despite a strong contribution from neural circuits located below the second spinal cord injury in the recovery of hindlimb locomotion, the coordination between the forelimbs and hindlimbs weakens and postural control is impaired. We can use our model to test approaches to restore the control of interlimb coordination and posture during locomotion after spinal cord injury.

Locomotion after complete spinal cord injury (spinal transection) in animal models is usually evaluated in a hindlimb-only condition with the forelimbs suspended or placed on a stationary platform and compared with quadrupedal locomotion in the intact state. However, because of the quadrupedal nature of movement in these animals, the forelimbs play an important role in modulating the hindlimb pattern. This raises the question: whether changes in the hindlimb pattern after spinal transection are due to the state of the system (intact versus spinal) or because the locomotion is hindlimb-only. We collected kinematic and electromyographic data during locomotion at seven treadmill speeds before and after spinal transection in nine adult cats during quadrupedal and hindlimb-only locomotion in the intact state and hindlimb-only locomotion in the spinal state. We attribute some changes in the hindlimb pattern to the spinal state, such as convergence in stance and swing durations at high speed, improper coordination of ankle and hip joints, a switch in the timing of knee flexor and hip flexor bursts, modulation of burst durations with speed, and incidence of bi-phasic bursts in some muscles. Alternatively, some changes relate to the hindlimb-only nature of the locomotion, such as paw placement relative to the hip at contact, magnitude of knee and ankle yield, burst durations of some muscles and their timing. Overall, we show greater similarity in spatiotemporal and EMG variables between the two hindlimb-only conditions, suggesting that the more appropriate pre-spinal control is hindlimb-only rather than quadrupedal locomotion.