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Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement

Estimating the direction of ambient fluid flow is a crucial step during chemical plume tracking for flying and swimming animals. How animals accomplish this remains an open area of investigation. Recent calcium imaging with tethered flying Drosophila has shown that flies encode the angular direction...

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Autores principales: van Breugel, Floris, Jewell, Renan, Houle, Jaleesa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9428576/
https://www.ncbi.nlm.nih.gov/pubmed/36043287
http://dx.doi.org/10.1098/rsif.2022.0258
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author van Breugel, Floris
Jewell, Renan
Houle, Jaleesa
author_facet van Breugel, Floris
Jewell, Renan
Houle, Jaleesa
author_sort van Breugel, Floris
collection PubMed
description Estimating the direction of ambient fluid flow is a crucial step during chemical plume tracking for flying and swimming animals. How animals accomplish this remains an open area of investigation. Recent calcium imaging with tethered flying Drosophila has shown that flies encode the angular direction of multiple sensory modalities in their central complex: orientation, apparent wind (or airspeed) direction and direction of motion. Here, we describe a general framework for how these three sensory modalities can be integrated over time to provide a continuous estimate of ambient wind direction. After validating our framework using a flying drone, we use simulations to show that ambient wind direction can be most accurately estimated with trajectories characterized by frequent, large magnitude turns. Furthermore, sensory measurements and estimates of their derivatives must be integrated over a period of time that incorporates at least one of these turns. Finally, we discuss approaches that insects might use to simplify the required computations, and present a list of testable predictions. Together, our results suggest that ambient flow estimation may be an important driver underlying the zigzagging manoeuvres characteristic of plume tracking animals’ trajectories.
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spelling pubmed-94285762022-08-31 Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement van Breugel, Floris Jewell, Renan Houle, Jaleesa J R Soc Interface Life Sciences–Mathematics interface Estimating the direction of ambient fluid flow is a crucial step during chemical plume tracking for flying and swimming animals. How animals accomplish this remains an open area of investigation. Recent calcium imaging with tethered flying Drosophila has shown that flies encode the angular direction of multiple sensory modalities in their central complex: orientation, apparent wind (or airspeed) direction and direction of motion. Here, we describe a general framework for how these three sensory modalities can be integrated over time to provide a continuous estimate of ambient wind direction. After validating our framework using a flying drone, we use simulations to show that ambient wind direction can be most accurately estimated with trajectories characterized by frequent, large magnitude turns. Furthermore, sensory measurements and estimates of their derivatives must be integrated over a period of time that incorporates at least one of these turns. Finally, we discuss approaches that insects might use to simplify the required computations, and present a list of testable predictions. Together, our results suggest that ambient flow estimation may be an important driver underlying the zigzagging manoeuvres characteristic of plume tracking animals’ trajectories. The Royal Society 2022-08-31 /pmc/articles/PMC9428576/ /pubmed/36043287 http://dx.doi.org/10.1098/rsif.2022.0258 Text en © 2022 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Life Sciences–Mathematics interface
van Breugel, Floris
Jewell, Renan
Houle, Jaleesa
Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement
title Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement
title_full Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement
title_fullStr Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement
title_full_unstemmed Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement
title_short Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement
title_sort active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement
topic Life Sciences–Mathematics interface
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9428576/
https://www.ncbi.nlm.nih.gov/pubmed/36043287
http://dx.doi.org/10.1098/rsif.2022.0258
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