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Wing structure and neural encoding jointly determine sensing strategies in insect flight

Animals rely on sensory feedback to generate accurate, reliable movements. In many flying insects, strain-sensitive neurons on the wings provide rapid feedback that is critical for stable flight control. While the impacts of wing structure on aerodynamic performance have been widely studied, the imp...

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Detalles Bibliográficos
Autores principales: Weber, Alison I., Daniel, Thomas L., Brunton, Bingni W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8382179/
https://www.ncbi.nlm.nih.gov/pubmed/34379622
http://dx.doi.org/10.1371/journal.pcbi.1009195
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author Weber, Alison I.
Daniel, Thomas L.
Brunton, Bingni W.
author_facet Weber, Alison I.
Daniel, Thomas L.
Brunton, Bingni W.
author_sort Weber, Alison I.
collection PubMed
description Animals rely on sensory feedback to generate accurate, reliable movements. In many flying insects, strain-sensitive neurons on the wings provide rapid feedback that is critical for stable flight control. While the impacts of wing structure on aerodynamic performance have been widely studied, the impacts of wing structure on sensing are largely unexplored. In this paper, we show how the structural properties of the wing and encoding by mechanosensory neurons interact to jointly determine optimal sensing strategies and performance. Specifically, we examine how neural sensors can be placed effectively on a flapping wing to detect body rotation about different axes, using a computational wing model with varying flexural stiffness. A small set of mechanosensors, conveying strain information at key locations with a single action potential per wingbeat, enable accurate detection of body rotation. Optimal sensor locations are concentrated at either the wing base or the wing tip, and they transition sharply as a function of both wing stiffness and neural threshold. Moreover, the sensing strategy and performance is robust to both external disturbances and sensor loss. Typically, only five sensors are needed to achieve near-peak accuracy, with a single sensor often providing accuracy well above chance. Our results show that small-amplitude, dynamic signals can be extracted efficiently with spatially and temporally sparse sensors in the context of flight. The demonstrated interaction of wing structure and neural encoding properties points to the importance of understanding each in the context of their joint evolution.
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spelling pubmed-83821792021-08-24 Wing structure and neural encoding jointly determine sensing strategies in insect flight Weber, Alison I. Daniel, Thomas L. Brunton, Bingni W. PLoS Comput Biol Research Article Animals rely on sensory feedback to generate accurate, reliable movements. In many flying insects, strain-sensitive neurons on the wings provide rapid feedback that is critical for stable flight control. While the impacts of wing structure on aerodynamic performance have been widely studied, the impacts of wing structure on sensing are largely unexplored. In this paper, we show how the structural properties of the wing and encoding by mechanosensory neurons interact to jointly determine optimal sensing strategies and performance. Specifically, we examine how neural sensors can be placed effectively on a flapping wing to detect body rotation about different axes, using a computational wing model with varying flexural stiffness. A small set of mechanosensors, conveying strain information at key locations with a single action potential per wingbeat, enable accurate detection of body rotation. Optimal sensor locations are concentrated at either the wing base or the wing tip, and they transition sharply as a function of both wing stiffness and neural threshold. Moreover, the sensing strategy and performance is robust to both external disturbances and sensor loss. Typically, only five sensors are needed to achieve near-peak accuracy, with a single sensor often providing accuracy well above chance. Our results show that small-amplitude, dynamic signals can be extracted efficiently with spatially and temporally sparse sensors in the context of flight. The demonstrated interaction of wing structure and neural encoding properties points to the importance of understanding each in the context of their joint evolution. Public Library of Science 2021-08-11 /pmc/articles/PMC8382179/ /pubmed/34379622 http://dx.doi.org/10.1371/journal.pcbi.1009195 Text en © 2021 Weber et al 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/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Weber, Alison I.
Daniel, Thomas L.
Brunton, Bingni W.
Wing structure and neural encoding jointly determine sensing strategies in insect flight
title Wing structure and neural encoding jointly determine sensing strategies in insect flight
title_full Wing structure and neural encoding jointly determine sensing strategies in insect flight
title_fullStr Wing structure and neural encoding jointly determine sensing strategies in insect flight
title_full_unstemmed Wing structure and neural encoding jointly determine sensing strategies in insect flight
title_short Wing structure and neural encoding jointly determine sensing strategies in insect flight
title_sort wing structure and neural encoding jointly determine sensing strategies in insect flight
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8382179/
https://www.ncbi.nlm.nih.gov/pubmed/34379622
http://dx.doi.org/10.1371/journal.pcbi.1009195
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