Abstract

Xenopus laevis has a lateral line mechanosensory system throughout its full life cycle, and a previous study on prefeeding 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 immobilized 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 behavior.NEW & NOTEWORTHY We studied Xenopus tadpole motor responses to anterior lateral line stimulation using high-speed videos, electrophysiology and calcium imaging. Activating the lateral line reliably started swimming. At high stimulation intensities, turning was observed behaviorally but suitable motor nerve discharges were seen only occasionally in immobilized tadpoles. Suction applied during swimming produced a halting response. We analyzed afferent and efferent activities of the tadpole anterior lateral line nerve and located sensory interneurons using calcium imaging.

Highlights

  • Aquatic vertebrates including fish and amphibians use the distributed mechanosensory lateral line (LL) system to sense hydrodynamic disturbances [1,2,3,4]

  • The turning bends outside or inside the suction nozzle had similar duration (40 ± 5.8 ms, n = 13 trials from 10 animals), which was longer than the duration of body bends during tadpole swimming (22 ± 4.9 ms, n = 13 trials from 10 animals, paired t test, P < 0.001, Fig. 1H). These results show suction stimulation could initiate forward swimming or induce occasional flexion responses at lower suction levels, whereas turning behavior becomes common with stronger stimuli and when the tadpole is in the head-toward-nozzle configuration

  • The results show that the anterior lateral line nerve (aLLN) plays a role in tadpole turning behavior, initiation, and termination of swimming

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Summary

Introduction

Aquatic vertebrates including fish and amphibians use the distributed mechanosensory lateral line (LL) system to sense hydrodynamic disturbances [1,2,3,4]. The LL mechanosensory neuromasts can be either located superficially in the epidermis or embedded in the lateral line canals [20]. Hair cell ciliary bundles in the neuromasts act as mechanotransducers [22]. These consist of a single kinocilium and many stereovilli embedded inside a gelatinous cupula that bend with water flow [1, 23]. The LL information enters the brainstem via two cranial nerves, the anterior lateral line nerve (aLLN) innervating the head region, and the posterior lateral line nerve (pLLN) innervating the trunk. Both project to a conserved nucleus in the dorsolateral medulla, the medial octavolateralis nucleus (MON) [24,25,26,27,28,29,30]

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