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

Abstract

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.