The early development and physiology of Xenopus laevis tadpole lateral line system

Abstract

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.

Mechanosensory signal transmission in the arms and the nerve ring, an interarm connective, of Octopus bimaculoides

“…Both increasing the magnitude of the deformation of the arm tissue and the speed of application of the deformation led to a stronger response, namely increased the number of activity spikes and relatedly increased overall duration of post-stimulus activity during the hold period. Mechanosensory activity in response to larger deformation could last longer; this activity resembles slowly adapting responses found in various species including mammals, 21 Xenopus laevis , 22 and drosophila. 23 In a previous cephalopod study, only relatively fast adapting on-off responses were recorded in the arm when muscles were stimulated in an isolated axial nerve cord preparation.…”

Tadpoles rely on mechanosensory stimuli for communication when visual capabilities are poor

“…In X enopus tadpoles, the lateral line is involved in directional current detection as well as maintaining position or posture within a water column (Simmons, Costa, and Gerstein 2004). In pre-freeding stages of Xenopus tadpoles, the lateral line was shown to be important for responding to water jet and suction stimuli (Saccomanno et al 2021). Red-eyed treefrog, Agalychnis callidryas , embryos hatch prematurely to escape egg-predators, which was shown to be dependent on the lateral line system in early developmental stages prior to vestibular system development (Jung, Serrano-Rojas, and Warkentin 2020).…”

“…While less is known about the role of the lateral line in tadpoles, it has been implicated in responding to water currents (Brown and Simmons 2016; Simmons, Costa, and Gerstein 2004) and predator avoidance (Jung, Serrano-Rojas, and Warkentin 2020). In many species of frogs, the lateral line system is nearly or fully developed at hatching (Lannoo 1987; Zelena 1964; Saccomanno et al 2021; Jung, Serrano-Rojas, and Warkentin 2020; Roberts et al 2009) but degrades during metamorphosis (Wright 1951; Zelena 1964; Brown and Simmons 2016). As such, mechanosensation via the lateral line system is a potential communication channel during early-life stages that could play a role in detecting and recognizing social stimuli.…”