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Temporal novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments

To survive, insects must effectively navigate odor plumes to their source. In natural plumes, turbulent winds break up smooth odor regions into disconnected patches, so navigators encounter brief bursts of odor interrupted by bouts of clean air. The timing of these encounters plays a critical role i...

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Autores principales: Jayaram, Viraaj, Sehdev, Aarti, Kadakia, Nirag, Brown, Ethan A., Emonet, Thierry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10205008/
https://www.ncbi.nlm.nih.gov/pubmed/37167321
http://dx.doi.org/10.1371/journal.pcbi.1010606
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author Jayaram, Viraaj
Sehdev, Aarti
Kadakia, Nirag
Brown, Ethan A.
Emonet, Thierry
author_facet Jayaram, Viraaj
Sehdev, Aarti
Kadakia, Nirag
Brown, Ethan A.
Emonet, Thierry
author_sort Jayaram, Viraaj
collection PubMed
description To survive, insects must effectively navigate odor plumes to their source. In natural plumes, turbulent winds break up smooth odor regions into disconnected patches, so navigators encounter brief bursts of odor interrupted by bouts of clean air. The timing of these encounters plays a critical role in navigation, determining the direction, rate, and magnitude of insects’ orientation and speed dynamics. Disambiguating the specific role of odor timing from other cues, such as spatial structure, is challenging due to natural correlations between plumes’ temporal and spatial features. Here, we use optogenetics to isolate temporal features of odor signals, examining how the frequency and duration of odor encounters shape the navigational decisions of freely-walking Drosophila. We find that fly angular velocity depends on signal frequency and intermittency–the fraction of time signal can be detected–but not directly on durations. Rather than switching strategies when signal statistics change, flies smoothly transition between signal regimes, by combining an odor offset response with a frequency-dependent novelty-like response. In the latter, flies are more likely to turn in response to each odor hit only when the hits are sparse. Finally, the upwind bias of individual turns relies on a filtering scheme with two distinct timescales, allowing rapid and sustained responses in a variety of signal statistics. A quantitative model incorporating these ingredients recapitulates fly orientation dynamics across a wide range of environments and shows that temporal novelty detection, when combined with odor motion detection, enhances odor plume navigation.
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spelling pubmed-102050082023-05-24 Temporal novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments Jayaram, Viraaj Sehdev, Aarti Kadakia, Nirag Brown, Ethan A. Emonet, Thierry PLoS Comput Biol Research Article To survive, insects must effectively navigate odor plumes to their source. In natural plumes, turbulent winds break up smooth odor regions into disconnected patches, so navigators encounter brief bursts of odor interrupted by bouts of clean air. The timing of these encounters plays a critical role in navigation, determining the direction, rate, and magnitude of insects’ orientation and speed dynamics. Disambiguating the specific role of odor timing from other cues, such as spatial structure, is challenging due to natural correlations between plumes’ temporal and spatial features. Here, we use optogenetics to isolate temporal features of odor signals, examining how the frequency and duration of odor encounters shape the navigational decisions of freely-walking Drosophila. We find that fly angular velocity depends on signal frequency and intermittency–the fraction of time signal can be detected–but not directly on durations. Rather than switching strategies when signal statistics change, flies smoothly transition between signal regimes, by combining an odor offset response with a frequency-dependent novelty-like response. In the latter, flies are more likely to turn in response to each odor hit only when the hits are sparse. Finally, the upwind bias of individual turns relies on a filtering scheme with two distinct timescales, allowing rapid and sustained responses in a variety of signal statistics. A quantitative model incorporating these ingredients recapitulates fly orientation dynamics across a wide range of environments and shows that temporal novelty detection, when combined with odor motion detection, enhances odor plume navigation. Public Library of Science 2023-05-11 /pmc/articles/PMC10205008/ /pubmed/37167321 http://dx.doi.org/10.1371/journal.pcbi.1010606 Text en © 2023 Jayaram 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
Jayaram, Viraaj
Sehdev, Aarti
Kadakia, Nirag
Brown, Ethan A.
Emonet, Thierry
Temporal novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments
title Temporal novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments
title_full Temporal novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments
title_fullStr Temporal novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments
title_full_unstemmed Temporal novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments
title_short Temporal novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments
title_sort temporal novelty detection and multiple timescale integration drive drosophila orientation dynamics in temporally diverse olfactory environments
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10205008/
https://www.ncbi.nlm.nih.gov/pubmed/37167321
http://dx.doi.org/10.1371/journal.pcbi.1010606
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