Abstract
Within the cervical and lumbar spinal enlargements, central pattern generator (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 inter-connect 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.
Highlights
Locomotion is a fundamental behavior that allows animals to move through the environment to forage, escape predators, or explore
We found no increase in the per-step angular rotation of the hindpaws during long ascending propriospinal neurons (LAPNs) silencing, suggesting that base-of-support remained unchanged despite the disrupted phase relationship between limb pairs at each girdle (Figure 3g)
Given their lumbar-to-cervical connectivity, we hypothesized that silencing LAPNs would disrupt hindlimb-forelimb coordination during locomotion
Summary
Locomotion is a fundamental behavior that allows animals to move through the environment to forage, escape predators, or explore. Its expression is initiated supraspinally by various brain nuclei that provide locomotor command cues to spinal circuits, the downstream effectors of movement (Caggiano et al, 2018) It is the responsibility of the spinal cord circuitry to organize limb movements into the stepping patterns that are defined as locomotor gaits (Orlovskiıet al., 1999). Two classes of inter-enlargement spinal neurons are thought to coordinate forelimb-hindlimb movements: long ascending propriospinal neurons (LAPNs) and long descending propriospinal neurons (LDPNs) (Miller and van der Meche, 1976; Miller et al, 1975; Juvin et al, 2005). Our data suggest that LAPNs form a flexible, task-specific network for securing interlimb coordination of each limb pair (at the forelimb and hindlimb girdles, respectively) in a highly context-driven manner
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