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

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...

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Autores principales: Saccomanno, Valentina, Love, Heather, Sylvester, Amy, Li, Wen-Chang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Physiological Society 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8794055/
https://www.ncbi.nlm.nih.gov/pubmed/34705593
http://dx.doi.org/10.1152/jn.00618.2020
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author Saccomanno, Valentina
Love, Heather
Sylvester, Amy
Li, Wen-Chang
author_facet Saccomanno, Valentina
Love, Heather
Sylvester, Amy
Li, Wen-Chang
author_sort Saccomanno, Valentina
collection PubMed
description 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.
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spelling pubmed-87940552022-11-01 The early development and physiology of Xenopus laevis tadpole lateral line system Saccomanno, Valentina Love, Heather Sylvester, Amy Li, Wen-Chang J Neurophysiol Research Article 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. American Physiological Society 2021-11-01 2021-10-27 /pmc/articles/PMC8794055/ /pubmed/34705593 http://dx.doi.org/10.1152/jn.00618.2020 Text en Copyright © 2021 The Authors https://creativecommons.org/licenses/by/4.0/Licensed under Creative Commons Attribution CC-BY 4.0 (https://creativecommons.org/licenses/by/4.0/) . Published by the American Physiological Society.
spellingShingle Research Article
Saccomanno, Valentina
Love, Heather
Sylvester, Amy
Li, Wen-Chang
The early development and physiology of Xenopus laevis tadpole lateral line system
title The early development and physiology of Xenopus laevis tadpole lateral line system
title_full The early development and physiology of Xenopus laevis tadpole lateral line system
title_fullStr The early development and physiology of Xenopus laevis tadpole lateral line system
title_full_unstemmed The early development and physiology of Xenopus laevis tadpole lateral line system
title_short The early development and physiology of Xenopus laevis tadpole lateral line system
title_sort early development and physiology of xenopus laevis tadpole lateral line system
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8794055/
https://www.ncbi.nlm.nih.gov/pubmed/34705593
http://dx.doi.org/10.1152/jn.00618.2020
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