Interactions between dorsal and ventral root stimulation on the generation of locomotor-like activity in the neonatal mouse spinal cord

ABSTRACT

We investigated whether dorsal (DR) and ventral root (VR) stimulus trains engage common postsynaptic components to activate the central pattern generator (CPG) for locomotion in the neonatal mouse spinal cord. Ventral root stimulation did not activate the first order interneurons mediating the activation of the locomotor CPG by sacrocaudal afferent stimulation. Simultaneous stimulation of adjacent dorsal or ventral root pairs, subthreshold for evoking locomotor-like activity, did not summate to activate the CPG. This suggests that locomotor-like activity is triggered when a critical class of efferent or afferent axons is stimulated and does not depend on the number of stimulated axons or activated postsynaptic neurons. DR- and VR-evoked episodes exhibited differences in the coupling between VR pairs. In DR-evoked episodes the coupling between the ipsi- and contralateral flexor/extensor roots was similar and stronger than the bilateral extensor roots. In VR-evoked episodes, ipsilateral flexor/extensor coupling was stronger than both the contralateral flexor/extensor and the bilateral extensor coupling. For both types of stimulation, the coupling was greatest between the bilateral L1/L2 flexor-dominated roots. This indicates that the recruitment and/or the firing pattern of motoneurons differed in DR and VR-evoked episodes. However, the DR and VR trains do not appear to activate distinct CPGs because trains of DR and VR stimuli at frequencies too low to evoke locomotor-like activity, did so when they were interleaved. These results indicate that the excitatory actions of VR stimulation converge onto the CPG through an unknown pathway that is not captured by current models of the locomotor CPG.

Significance Statement: In 2005 we showed that stimulation of motor axons can activate the neural circuitry for locomotion in the neonatal mouse spinal cord. This was a surprising result because motoneurons are thought to be purely output elements of the spinal cord. Here we show that motor axons reach the locomotor circuitry by a different pathway to that employed by sensory axons. Despite this difference, both types of stimulation activate common locomotor circuitry. An understanding of how motor axons activate these circuits will provide novel insights into the organization of locomotor networks.