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- Title
Temporal novelty detection and multiple timescale integration drive Drosophila orientation dynamics in temporally diverse olfactory environments.
- Authors
Jayaram, Viraaj; Sehdev, Aarti; Kadakia, Nirag; Brown, Ethan A.; Emonet, Thierry
- 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. 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. Author summary: Olfactory navigation is essential for insects to find food and mates but challenging because complex wind flows break odor plumes up into discrete and intermittent packets. The timing of encounters with these packets is crucial for navigation, affecting when insects reorient. To decide where to reorient, insects extract directional information from the wind, the odor gradient, and the motion of the odor packets, by comparing signals between their two antennae. Here we ask how the frequency and duration of odor encounters drive reorientation. To isolate the role of odor timing we use a virtual reality setup in which freely walking flies experience a constant wind direction along with uniform flashes of light–virtual odor packets–that activate their odor sensors uniformly, thus removing all odor directional cues. We find that flies are much more likely to respond to an individual odor encounter if the time since the previous encounter is greater than ~2s. We show in simulations how this temporal novelty detection, when combined with odor motion-sensing, enhances navigation. In turbulent plumes odor packets tend to arrive in clumps. Our findings suggest flies can respond differently to the beginning of a clump than to fluctuations within to enhance navigation.
- Subjects
ELECTRONIC noses; EDIBLE insects; DROSOPHILA; ANGULAR velocity; INSECT food; VIRTUAL reality; SEMIOCHEMICALS
- Publication
PLoS Computational Biology, 2023, Vol 19, Issue 5, p1
- ISSN
1553-734X
- Publication type
Article
- DOI
10.1371/journal.pcbi.1010606