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 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.

Social foraging extends associative odor-food memory expression in an automated learning assay for Drosophila melanogaster.

Animals socially interact during foraging and share information about the quality and location of food sources. The mechanisms of social information transfer during foraging have been mostly studied at the behavioral level, and its underlying neural mechanisms are largely unknown. Fruit flies have become a model for studying the neural bases of social information transfer, because they provide a large genetic toolbox to monitor and manipulate neuronal activity, and they show a rich repertoire of social behaviors. Fruit flies aggregate, they use social information for choosing a suitable mating partner and oviposition site, and they show better aversive learning when in groups. However, the effects of social interactions on associative odor-food learning have not yet been investigated. Here, we present an automated learning and memory assay for walking flies that allows the study of the effect of group size on social interactions and on the formation and expression of associative odor-food memories. We found that both inter-fly attraction and the duration of odor-food memory expression increase with group size. This study opens up opportunities to investigate how social interactions during foraging are relayed in the neural circuitry of learning and memory expression.

Segregation of Unknown Odors From Mixtures Based on Stimulus Onset Asynchrony in Honey Bees.

Animals use olfaction to search for distant objects. Unlike vision, where objects are spaced out, olfactory information mixes when it reaches olfactory organs. Therefore, efficient olfactory search requires segregating odors that are mixed with background odors. Animals can segregate known odors by detecting short differences in the arrival of mixed odorants (stimulus onset asynchrony). However, it is unclear whether animals can also use stimulus onset asynchrony to segregate odorants that they had no previous experience with and which have no innate or learned relevance (unknown odorants). Using behavioral experiments in honey bees, we here show that stimulus onset asynchrony also improves segregation of those unknown odorants. The stimulus onset asynchrony necessary to segregate unknown odorants is in the range of seconds, which is two orders of magnitude larger than the previously reported stimulus asynchrony sufficient for segregating known odorants. We propose that for unknown odorants, segregating odorant A from a mixture with B requires sensory adaptation to B.

Olfactory Object Recognition Based on Fine-Scale Stimulus Timing in Drosophila.

Odorants of behaviorally relevant objects (e.g., food sources) intermingle with those from other sources. Therefore to determine whether an odor source is good or bad-without actually visiting it-animals first need to segregate the odorants from different sources. To do so, animals could use temporal stimulus cues, because odorants from one source exhibit correlated fluctuations, whereas odorants from different sources are less correlated. However, the behaviorally relevant timescales of temporal stimulus cues for odor source segregation remain unclear. Using behavioral experiments with free-flying flies, we show that (1) odorant onset asynchrony increases flies' attraction to a mixture of two odorants with opposing innate or learned valence and (2) attraction does not increase when the attractive odorant arrives first. These data suggest that flies can use stimulus onset asynchrony for odor source segregation and imply temporally precise neural mechanisms for encoding odors and for segregating them into distinct objects.