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

Aarti Sehdev, Viraaj Jayaram, View ORCID ProfileNirag Kadakia, Ethan Brown, View ORCID ProfileThierry Emonet
doi: https://doi.org/10.1101/2022.09.28.509840
Aarti Sehdev
1Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT, USA
2Quantitative Biology Institute, Yale University, New Haven, CT, USA
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Viraaj Jayaram
2Quantitative Biology Institute, Yale University, New Haven, CT, USA
3Department of Physics, Yale University, New Haven, CT, USA
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Nirag Kadakia
1Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT, USA
2Quantitative Biology Institute, Yale University, New Haven, CT, USA
4Swartz Foundation for Theoretical Neuroscience, Yale University, New Haven, CT, USA
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Ethan Brown
1Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT, USA
2Quantitative Biology Institute, Yale University, New Haven, CT, USA
5Yale College, Yale University, New Haven, CT, USA
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Thierry Emonet
1Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT, USA
2Quantitative Biology Institute, Yale University, New Haven, CT, USA
3Department of Physics, Yale University, New Haven, CT, USA
6Interdepartmental Neuroscience Program, Yale University, New Haven, CT, USA
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  • For correspondence: thierry.emonet@yale.edu
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ABSTRACT

To survive, insects must effectively navigate odors 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. Still, 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 – 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.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted September 28, 2022.
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Novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments
Aarti Sehdev, Viraaj Jayaram, Nirag Kadakia, Ethan Brown, Thierry Emonet
bioRxiv 2022.09.28.509840; doi: https://doi.org/10.1101/2022.09.28.509840
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Novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments
Aarti Sehdev, Viraaj Jayaram, Nirag Kadakia, Ethan Brown, Thierry Emonet
bioRxiv 2022.09.28.509840; doi: https://doi.org/10.1101/2022.09.28.509840

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