Propriospinal Circuitry Underlying Interlimb Coordination in Mammalian Quadrupedal Locomotion

TLDR

Quadrupeds can express coordinated forelimb and hindlimb locomotion soon after birth. The study investigates neural mechanisms of interlimb coordination using isolated neonatal rat spinal cords. The isolated spinal cord was stimulated with 5‑HT, NMA, and DA to elicit fictive locomotion. The experiments showed that cervical and lumbar locomotor generators are rhythmically independent yet can coordinate through a caudorostral propriospinal excitability gradient, with coordination enhanced by thoracic segment exposure and disrupted by inhibition blockade, yet a coordinated fictive walking pattern persisted even after mid‑sagittal cuts.

Abstract

Soon after birth, freely moving quadrupeds can express locomotor activity with coordinated forelimb and hindlimb movements. To investigate the neural mechanisms underlying this coordination, we used an isolated spinal cord preparation from neonatal rats. Under bath-applied 5-HT, N -methyl- d , l -aspartate (NMA), and dopamine (DA), the isolated cord generates fictive locomotion in which homolateral cervicolumbar extensor motor bursts occur in phase opposition, as does bursting in homologous (left-right) extensor motoneurons. This coordination corresponded to a walking gait monitored with EMG recordings in the freely behaving animal. Functional decoupling of the cervical and lumbar generators in vitro by sucrose blockade at the thoracic cord level revealed independent rhythmogenic capabilities with similar cycle frequencies in the two locomotor regions. When the cord was partitioned at different thoracic levels and 5-HT/NMA/DA was applied to the more caudal compartment, the ability of the lumbar generators to drive their cervical counterparts increased with the proportion of chemically exposed thoracic segments. Blockade of synaptic inhibition at the lumbar level caused synchronous bilateral lumbar rhythmicity that, surprisingly, also was able to impose bilaterally synchronous bursting at the unblocked cervical level. Furthermore, after a midsagittal section from spinal segments C1 to T7, and during additional blockade of cervical synaptic inhibition, the cord exposed to 5-HT/NMA/DA continued to produce a coordinated fictive walking pattern similar to that observed in control. Thus, in the newborn rat, a caudorostral propriospinal excitability gradient appears to mediate interlimb coordination, which relies more on asymmetric axial connectivity (both excitatory and inhibitory) between the lumbar and cervical generators than on differences in their inherent rhythmogenic capacities.