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Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes

We and others have shown that during odor plume navigation, walking Drosophila melanogaster bias their motion upwind in response to both the frequency of their encounters with the odor (Demir et al., 2020) and the intermittency of the odor signal, which we define to be the fraction of time the signa...

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Autores principales: Jayaram, Viraaj, Kadakia, Nirag, Emonet, Thierry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8871351/
https://www.ncbi.nlm.nih.gov/pubmed/35072625
http://dx.doi.org/10.7554/eLife.72415
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author Jayaram, Viraaj
Kadakia, Nirag
Emonet, Thierry
author_facet Jayaram, Viraaj
Kadakia, Nirag
Emonet, Thierry
author_sort Jayaram, Viraaj
collection PubMed
description We and others have shown that during odor plume navigation, walking Drosophila melanogaster bias their motion upwind in response to both the frequency of their encounters with the odor (Demir et al., 2020) and the intermittency of the odor signal, which we define to be the fraction of time the signal is above a detection threshold (Alvarez-Salvado et al., 2018). Here, we combine and simplify previous mathematical models that recapitulated these data to investigate the benefits of sensing both of these temporal features and how these benefits depend on the spatiotemporal statistics of the odor plume. Through agent-based simulations, we find that navigators that only use frequency or intermittency perform well in some environments – achieving maximal performance when gains are near those inferred from experiment – but fail in others. Robust performance across diverse environments requires both temporal modalities. However, we also find a steep trade-off when using both sensors simultaneously, suggesting a strong benefit to modulating how much each sensor is weighted, rather than using both in a fixed combination across plumes. Finally, we show that the circuitry of the Drosophila olfactory periphery naturally enables simultaneous intermittency and frequency sensing, enhancing robust navigation through a diversity of odor environments. Together, our results suggest that the first stage of olfactory processing selects and encodes temporal features of odor signals critical to real-world navigation tasks.
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spelling pubmed-88713512022-02-25 Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes Jayaram, Viraaj Kadakia, Nirag Emonet, Thierry eLife Neuroscience We and others have shown that during odor plume navigation, walking Drosophila melanogaster bias their motion upwind in response to both the frequency of their encounters with the odor (Demir et al., 2020) and the intermittency of the odor signal, which we define to be the fraction of time the signal is above a detection threshold (Alvarez-Salvado et al., 2018). Here, we combine and simplify previous mathematical models that recapitulated these data to investigate the benefits of sensing both of these temporal features and how these benefits depend on the spatiotemporal statistics of the odor plume. Through agent-based simulations, we find that navigators that only use frequency or intermittency perform well in some environments – achieving maximal performance when gains are near those inferred from experiment – but fail in others. Robust performance across diverse environments requires both temporal modalities. However, we also find a steep trade-off when using both sensors simultaneously, suggesting a strong benefit to modulating how much each sensor is weighted, rather than using both in a fixed combination across plumes. Finally, we show that the circuitry of the Drosophila olfactory periphery naturally enables simultaneous intermittency and frequency sensing, enhancing robust navigation through a diversity of odor environments. Together, our results suggest that the first stage of olfactory processing selects and encodes temporal features of odor signals critical to real-world navigation tasks. eLife Sciences Publications, Ltd 2022-01-24 /pmc/articles/PMC8871351/ /pubmed/35072625 http://dx.doi.org/10.7554/eLife.72415 Text en © 2022, Jayaram et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Jayaram, Viraaj
Kadakia, Nirag
Emonet, Thierry
Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes
title Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes
title_full Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes
title_fullStr Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes
title_full_unstemmed Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes
title_short Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes
title_sort sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8871351/
https://www.ncbi.nlm.nih.gov/pubmed/35072625
http://dx.doi.org/10.7554/eLife.72415
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