Fly navigational responses to odor motion and gradient cues are tuned to plume statistics

Abstract

Odor cues guide animals to food and mates. Different environmental conditions can create differently patterned odor plumes, making navigation more challenging. Prior work has shown that animals turn upwind when they detect odor and cast crosswind when they lose it. Animals with bilateral olfactory sensors can also detect directional odor cues, such as odor gradient and odor motion. It remains unknown how animals use these two directional odor cues to guide crosswind navigation in odor plumes with distinct statistics. Here, we investigate this problem theoretically and experimentally. We show that these directional odor cues provide complementary information for navigation in different plume environments. We numerically analyzed real plumes to show that odor gradient cues are more informative about crosswind directions in relatively smooth odor plumes, while odor motion cues are more informative in turbulent or complex plumes. Neural networks trained to optimize crosswind turning converge to distinctive network structures that are tuned to odor gradient cues in smooth plumes and to odor motion cues in complex plumes. These trained networks improve the performance of artificial agents navigating plume environments that match the training environment. By recording Drosophila fruit flies as they navigated different odor plume environments, we verified that flies show the same correspondence between informative cues and plume types. Fly turning in the crosswind direction is correlated with odor gradients in smooth plumes and with odor motion in complex plumes. Overall, these results demonstrate that these directional odor cues are complementary across environments, and that animals exploit this relationship. SignificanceMany animals use smell to find food and mates, often navigating complex odor plumes shaped by environmental conditions. While upwind movement upon odor detection is well established, less is known about how animals steer crosswind to stay in the plume. We show that directional odor cues--gradients and motion--guide crosswind navigation differently depending on plume structure. Gradients carry more information in smooth plumes, while motion dominates in turbulent ones. Neural network trained to optimize crosswind navigation reflect this distinction, developing gradient sensitivity in smooth environments and motion sensitivity in complex ones. Experimentally, fruit flies adjust their turning behavior to prioritize the most informative cue in each context. These findings likely generalize to other animals navigating similarly structured odor plumes.