Xenopus laevis has a lateral line mechanosensory system throughout its full life cycle and a previous study on pre-feeding stage tadpoles revealed that it may play a role in motor responses to both water suction and water jets. Here, we investigated the physiology of the anterior lateral line system in newly hatched tadpoles and the motor outputs induced by its activation in response to brief suction stimuli. High-speed videoing showed tadpoles tended to turn and swim away when strong suction was applied close to the head. The lateral line neuromasts were revealed by using DASPEI staining, and their inactivation with neomycin eliminated tadpole motor responses to suction. In immobilised preparations, suction or electrically stimulating the anterior lateral line nerve reliably initiated swimming but the motor nerve discharges implicating turning was observed only occasionally. The same stimulation applied during ongoing fictive swimming produced a halting response. The anterior lateral line nerve showed spontaneous afferent discharges at rest and increased activity during stimulation. Efferent activities were only recorded during tadpole fictive swimming and were largely synchronous with the ipsilateral motor nerve discharges. Finally, calcium imaging identified neurons with fluorescence increase time-locked with suction stimulation in the hindbrain and midbrain. A cluster of neurons at the entry point of the anterior lateral line nerve in the dorsolateral hindbrain had the shortest latency in their responses, supporting their potential sensory interneuron identity. Future studies need to reveal how the lateral line sensory information is processed by the central circuit to determine tadpole motor behaviour.

Xenopus laevis has a lateral line mechanosensory system throughout its full life cycle. Previous studies of the tadpole lateral line system revealed that it may play a role in escape behaviour. In this study, we used DASPEI staining to reveal the location of tadpole lateral line neuromasts. Destroying these neuromasts with neomycin resulted in loss of escape responses in tadpoles. We then studied the physiology of anterior lateral line in immobilised tadpoles. Activating the neuromasts behind one eye could evoke asymmetrical motor nerve discharges when the tadpole was resting, suggestive of turning/escape, followed by fictive swimming. When the tadpole was already producing fictive swimming however, anterior lateral line activation reliably led to the termination of swimming. The anterior lateral line had spontaneous afferent discharges at rest, and when activated showed typical adaptation. There were also efferent activities during tadpole swimming, the activity of which was loosely in phase with ipsilateral motor nerve discharges, implying modulation by the motor circuit from the same side. Calcium imaging experiments located sensory interneurons in the primary anterior lateral line nucleus in the hindbrain. Future studies are needed to reveal how sensory information is processed by the central circuit to determine tadpole motor behaviour.Summary statementActivating tadpole anterior lateral line evokes escape responses followed by swimming and halts ongoing swimming. The afferent and efferent activities and sensory interneuron locations in the hindbrain are reported.

Developing spinal circuits generate patterned motor outputs while many neurons with high membrane resistances are still maturing. In the spinal cord of hatchling frog tadpoles of unknown sex, we found that the firing reliability in swimming of inhibitory interneurons with commissural and ipsilateral ascending axons was negatively correlated with their cellular membrane resistance. Further analyses showed that neurons with higher resistances had outward rectifying properties, low firing thresholds and little delay in firing evoked by current injections. Input synaptic currents these neurons received during swimming, either compound unitary current amplitudes or unitary synaptic current numbers, were scaled with their membrane resistances, but their own synaptic outputs were correlated with membrane resistances of their postsynaptic partners. Analyses of neuronal dendritic and axonal lengths and their activities in swimming and cellular input resistances did not reveal a clear correlation pattern. Incorporating these electrical and synaptic properties in a computer swimming model produced robust swimming rhythms whereas randomising input synaptic strengths led to the breakdown of swimming rhythms, coupled with less synchronised spiking in the inhibitory interneurons. We conclude that the recruitment of these developing interneurons in swimming can be predicted by cellular input resistances, but the order is opposite to the motor-strength based recruitment scheme depicted by Henneman’s size principle. This form of recruitment/integration order in development before the emergence of refined motor control is progressive potentially with neuronal acquisition of mature electrical and synaptic properties, among which the scaling of input synaptic strengths with cellular input resistance plays a critical role.SIGNIFICANCE STATEMENT:The mechanisms on how interneurons are recruited to participate circuit function in developing neuronal systems are rarely investigated. In two days old frog tadpole spinal cord, we found the recruitment of inhibitory interneurons in swimming is inversely correlated with cellular input resistances, opposite to the motor-strength based recruitment order depicted by Henneman’s size principle. Further analyses showed the amplitude of synaptic inputs neurons received during swimming was inversely correlated with cellular input resistances. Randomising/reversing the relation between input synaptic strengths and membrane resistances in modelling broke down swimming rhythms. Therefore, the recruitment or integration of these interneurons is conditional upon the acquisition of several electrical and synaptic properties including the scaling of input synaptic strengths with cellular input resistances.