Within the cervical and lumbar spinal enlargements, central pattern generating (CPG) circuitry produces the rhythmic output necessary for limb coordination during locomotion. Long propriospinal neurons that inter-connect these CPGs are thought to secure hindlimb-forelimb coordination, ensuring that diagonal limb pairs move synchronously while the ipsilateral limb pairs move out-of-phase during stepping. Here, we show that silencing long ascending propriospinal neurons (LAPNs) that interconnect the lumbar and cervical CPGs disrupts left-right limb coupling of each limb pair in the adult rat during overground locomotion on a high-friction surface. These perturbations occurred independent of the locomotor rhythm, intralimb coordination, and speed-dependent (or any other) principal features of locomotion. Strikingly, the functional consequences of silencing LAPNs are highly context-dependent; the phenotype was not expressed during swimming, treadmill stepping, exploratory locomotion, or walking on an uncoated, slick surface. These data reveal surprising flexibility and context-dependence in the control of interlimb coordination during locomotion.

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Thoracic spinal cord injury affects long propriospinal neurons that interconnect the cervical and lumbar enlargements. These neurons are crucial for coordinating forelimb and hindlimb movements in a speed-dependent manner. At the same time, recovery from spinal cord injury is usually studied over a very limited range of speeds. To overcome this limitation, we investigated overground locomotion in rats over the full range of speeds pre-injury and after recovery from thoracic hemisection or contusion injuries. Intact rats expressed a speed-dependent continuum of alternating (walk and trot) and non-alternating (canter, gallop, half-bound gallop, and bound) gaits. After a lateral hemisection injury, rats recovered the ability to locomote over a wide range of speeds but lost the ability to move using the highest-speed gaits (half-bound gallop and bound) and predominantly used the limb contralateral to injury as lead during canter and gallop. A moderate contusion injury resulted in a greater reduction in maximal speed, loss of non-alternating gaits, and emergence of novel alternating gaits. Analysis of the gait structure in phase space and the variability of limb coupling suggests substantial reorganization of intraspinal pathways mediating interlimb coordination following recovery of locomotion after lateral hemisection or midline contusion injuries. This reorganization appears as an increased reliance on local enlargement circuitry and suggests that speed-dependent gait changes in the forelimbs rely on ascending information from the lumbar circuitry that is impaired post-injury. These observations highlight how investigating the full repertoire of locomotor speeds can reveal otherwise hidden aspects of spinal circuitry and post-injury reorganization.

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