Alternation emerges as a multi-modal strategy for turbulent odor navigation

Foraging mammals exhibit a familiar yet poorly characterized phenomenon, "alternation", a momentary pause to sniff in the air often preceded by the animal rearing on its hind legs or raising its head. Intriguingly, rodents executing an olfactory search task spontaneously exhibit alternation in the presence of airflow, suggesting that alternation may serve an important role during turbulent plume-tracking. To test this hypothesis, we combine fully-resolved numerical simulations of turbulent odor transport and Bellman optimization methods for decision-making under partial observability. We show that an agent trained to minimize search time in a realistic odor plume exhibits extensive alternation together with the characteristic cast-and-surge behavior commonly observed in flying insects. Alternation is tightly linked with casting and occurs more frequently when the agent is far downwind of the source, where the likelihood of detecting airborne cues is higher relative to cues close to the ground. Casting and alternation emerge as complementary tools for effective exploration when cues are sparse. We develop a model based on marginal value theory to capture the interplay between casting, surging and alternation. More generally, we show how multiple sensorimotor modalities can be fruitfully integrated during complex goal-directed behavior.

Effects of Wing Kinematics on Modulating Odor Plume Structures in the Odor Tracking Flight of Fruit Flies

Insects rely on their olfactory system to forage, prey, and mate. They can sense odorant plumes emitted from sources of their interests with their bilateral odorant antennae, and track down odor sources using their highly efficient flapping-wing mechanism. The odor-tracking process typically consists of two distinct behaviors: surging upwind and zigzagging crosswind. Despite the extensive numerical and experimental studies on the flying trajectories and wing flapping kinematics during odor tracking flight, we have limited understanding of how the flying trajectories and flapping wings modulate odor plume structures. In this study, a fully coupled three-way numerical solver is developed, which solves the 3D Navier-Stokes equations coupled with equations of motion for the passive flapping wings, and the odorant convection-diffusion equation. This numerical solver is applied to investigate the unsteady flow field and the odorant transport phenomena of a fruit fly model in both surging upwind and zigzagging crosswind cases. The unsteady flow generated by flapping wings perturbs the odor plume structure and significantly impacts the odor intensity at the olfactory receptors (i.e., antennae). During zigzagging crosswind flight, the differences in odor perception time and peak odor intensity at the receptors potentially help create stereo odorant mapping to track odor source. Our simulation results will provide new insights into the mechanism of how fruit flies perceive odor landscape and inspire the future design of odor-guided micro aerial vehicles (MAVs) for surveillance and detection missions.

Navigating a diversity of turbulent plumes is enhanced by sensing complementary temporal features of odor signals

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, i.e. 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 tradeoff 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.

Correlated decision making across multiple phases of olfactory guided search in Drosophila

All motile organisms must search for food, often requiring the exploration of heterogeneous environments across a wide range of spatial scales. Recent field and laboratory experiments with the fruit fly, Drosophila, have revealed that they employ different strategies across these regimes, including kilometer scale straight-path flights between resource clusters, zig-zagging trajectories to follow odor plumes, and local search on foot after landing. However, little is known about the extent to which experiences in one regime might influence decisions in another. To determine how a flies’ odor plume tracking during flight is related to their behavior after landing, I tracked the behavior of individually labelled fruit flies as they explored an array of three odor emitting, but food-barren, objects. The distance flies travelled on the objects in search of food was correlated with the time elapsed between their visits, suggesting that their in-flight plume tracking and on-foot local search behaviors are interconnected through a lossy memory-like process.

Walking Drosophila navigate complex plumes using stochastic decisions biased by the timing of odor encounters

ABSTRACTInsects find food, mates, and egg-laying sites by tracking odor plumes swept by complex wind patterns. Previous studies have shown that moths and flies localize plumes by surging upwind at odor onset and turning cross- or downwind at odor offset. Less clear is how, once within the expanding cone of the odor plume, insects use their brief encounters with individual odor packets, whose location and timing are random, to progress towards the source. Experiments and theory have suggested that the timing of odor encounters might assist navigation, but connecting behaviors to individual encounters has been challenging. Here, we imaged complex odor plumes simultaneous with freely-walking flies, allowing us to quantify how behavior is shaped by individual odor encounters. Combining measurements, dynamical models, and statistical inference, we found that within the plume cone, individual encounters did not trigger reflexive surging, casting, or counterturning. Instead, flies turned stochastically with stereotyped saccades, whose direction was biased upwind by the timing of prior odor encounters, while the magnitude and rate of saccades remained constant. Odor encounters did not strongly affect walking speed. Instead, flies used encounter timing to modulate the rate of transitions between walks and stops. When stopped, flies initiated walks using information from multiple odor encounters, suggesting that integrating evidence without losing position was part of the strategy. These results indicate that once within the complex odor plume, where odor location and timing are unpredictable, animals navigate with biased random walks shaped by the entire sequence of encounters.

Olfactory receptor neurons use gain control and complementary kinetics to encode intermittent odorant stimuli

Insects find food and mates by navigating odorant plumes that can be highly intermittent, with intensities and durations that vary rapidly over orders of magnitude. Much is known about olfactory responses to pulses and steps, but it remains unclear how olfactory receptor neurons (ORNs) detect the intensity and timing of natural stimuli, where the absence of scale in the signal makes detection a formidable olfactory task. By stimulating Drosophila ORNs in vivo with naturalistic and Gaussian stimuli, we show that ORNs adapt to stimulus mean and variance, and that adaptation and saturation contribute to naturalistic sensing. Mean-dependent gain control followed the Weber-Fechner relation and occurred primarily at odor transduction, while variance-dependent gain control occurred at both transduction and spiking. Transduction and spike generation possessed complementary kinetic properties, that together preserved the timing of odorant encounters in ORN spiking, regardless of intensity. Such scale-invariance could be critical during odor plume navigation.