A vector-based strategy for olfactory navigation in Drosophila

Abstract

Odors serve as essential cues for navigation. Although tracking an odor plume has been modeled as a reflexive process, it remains unclear whether animals can use memories of their past odor encounters to infer the spatial structure of their chemical environment or their location within it. Here we developed a virtual-reality olfactory paradigm that allows head-fixed Drosophila to navigate structured chemical landscapes, offering insight into how memory mechanisms shape their navigational strategies. We found that flies track an appetitive odor corridor by following its boundary, alternating between rapid counterturns to exit the plume and directed returns to its edge. Using a combination of behavioral modeling, functional calcium imaging, and neural perturbations, we demonstrate that this edge-tracking strategy relies on vector-based computations within the Drosophila central complex in which flies store and dynamically update memories of the direction to return them to the plumes boundary. Consistent with this, we find that FC2 neurons within the fan-shaped body, which encode a flys navigational goal, signal the direction back to the odor boundary when flies are outside the plume. Together, our studies suggest that flies leverage the plumes boundary as a dynamic landmark to guide their navigation, analogous to the memory-based strategies other insects use for long-distance migration or homing to their nests. Plume tracking thus uses components of a conserved navigational toolkit, enabling flies to use memory mechanisms to navigate through a complex shifting chemical landscape.