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A sensation for inflation: initial swim bladder inflation in larval zebrafish is mediated by the mechanosensory lateral line

Larval zebrafish achieve neutral buoyancy by swimming up to the surface and taking in air through their mouths to inflate their swim bladders. We define this behavior as ‘surfacing’. Little is known about the sensory basis for this underappreciated behavior of larval fish. A strong candidate is the...

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Autores principales: Venuto, Alexandra, Thibodeau-Beganny, Stacey, Trapani, Josef G., Erickson, Timothy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10281257/
https://www.ncbi.nlm.nih.gov/pubmed/37272538
http://dx.doi.org/10.1242/jeb.245635
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author Venuto, Alexandra
Thibodeau-Beganny, Stacey
Trapani, Josef G.
Erickson, Timothy
author_facet Venuto, Alexandra
Thibodeau-Beganny, Stacey
Trapani, Josef G.
Erickson, Timothy
author_sort Venuto, Alexandra
collection PubMed
description Larval zebrafish achieve neutral buoyancy by swimming up to the surface and taking in air through their mouths to inflate their swim bladders. We define this behavior as ‘surfacing’. Little is known about the sensory basis for this underappreciated behavior of larval fish. A strong candidate is the mechanosensory lateral line, a hair cell-based sensory system that detects hydrodynamic information from sources such as water currents, predators, prey and surface waves. However, a role for the lateral line in mediating initial inflation of the swim bladder has not been reported. To explore the connection between the lateral line and surfacing, we used a genetic mutant (lhfpl5b(−/−)) that renders the zebrafish lateral line insensitive to mechanical stimuli. We observed that approximately half of these lateral line mutants over-inflate their swim bladders during initial inflation and become positively buoyant. Thus, we hypothesized that larval zebrafish use their lateral line to moderate interactions with the air–water interface during surfacing to regulate swim bladder inflation. To test the hypothesis that lateral line defects are responsible for swim bladder over-inflation, we showed that exogenous air is required for the hyperinflation phenotype and transgenic rescue of hair cell function restores normal inflation. We also found that chemical ablation of anterior lateral line hair cells in wild-type larvae causes hyperinflation. Furthermore, we show that manipulation of lateral line sensory information results in abnormal inflation. Finally, we report spatial and temporal differences in the surfacing behavior between wild-type and lateral line mutant larvae. In summary, we propose a novel sensory basis for achieving neutral buoyancy where larval zebrafish use their lateral line to sense the air–water interface and regulate initial swim bladder inflation.
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spelling pubmed-102812572023-06-21 A sensation for inflation: initial swim bladder inflation in larval zebrafish is mediated by the mechanosensory lateral line Venuto, Alexandra Thibodeau-Beganny, Stacey Trapani, Josef G. Erickson, Timothy J Exp Biol Research Article Larval zebrafish achieve neutral buoyancy by swimming up to the surface and taking in air through their mouths to inflate their swim bladders. We define this behavior as ‘surfacing’. Little is known about the sensory basis for this underappreciated behavior of larval fish. A strong candidate is the mechanosensory lateral line, a hair cell-based sensory system that detects hydrodynamic information from sources such as water currents, predators, prey and surface waves. However, a role for the lateral line in mediating initial inflation of the swim bladder has not been reported. To explore the connection between the lateral line and surfacing, we used a genetic mutant (lhfpl5b(−/−)) that renders the zebrafish lateral line insensitive to mechanical stimuli. We observed that approximately half of these lateral line mutants over-inflate their swim bladders during initial inflation and become positively buoyant. Thus, we hypothesized that larval zebrafish use their lateral line to moderate interactions with the air–water interface during surfacing to regulate swim bladder inflation. To test the hypothesis that lateral line defects are responsible for swim bladder over-inflation, we showed that exogenous air is required for the hyperinflation phenotype and transgenic rescue of hair cell function restores normal inflation. We also found that chemical ablation of anterior lateral line hair cells in wild-type larvae causes hyperinflation. Furthermore, we show that manipulation of lateral line sensory information results in abnormal inflation. Finally, we report spatial and temporal differences in the surfacing behavior between wild-type and lateral line mutant larvae. In summary, we propose a novel sensory basis for achieving neutral buoyancy where larval zebrafish use their lateral line to sense the air–water interface and regulate initial swim bladder inflation. The Company of Biologists Ltd 2023-06-05 /pmc/articles/PMC10281257/ /pubmed/37272538 http://dx.doi.org/10.1242/jeb.245635 Text en © 2023. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0 (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Venuto, Alexandra
Thibodeau-Beganny, Stacey
Trapani, Josef G.
Erickson, Timothy
A sensation for inflation: initial swim bladder inflation in larval zebrafish is mediated by the mechanosensory lateral line
title A sensation for inflation: initial swim bladder inflation in larval zebrafish is mediated by the mechanosensory lateral line
title_full A sensation for inflation: initial swim bladder inflation in larval zebrafish is mediated by the mechanosensory lateral line
title_fullStr A sensation for inflation: initial swim bladder inflation in larval zebrafish is mediated by the mechanosensory lateral line
title_full_unstemmed A sensation for inflation: initial swim bladder inflation in larval zebrafish is mediated by the mechanosensory lateral line
title_short A sensation for inflation: initial swim bladder inflation in larval zebrafish is mediated by the mechanosensory lateral line
title_sort sensation for inflation: initial swim bladder inflation in larval zebrafish is mediated by the mechanosensory lateral line
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10281257/
https://www.ncbi.nlm.nih.gov/pubmed/37272538
http://dx.doi.org/10.1242/jeb.245635
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