Spatial learning in feature-impoverished environments in Drosophila

The ability to return to memorized goal locations is essential for animal survival. While it is well documented that animals use visual landmarks to locate goals1,2, how they navigate spatial learning tasks in environments lacking such landmarks remains poorly understood. Here, using a high-throughput spatial learning task we developed to investigate this question in Drosophila, we found that Drosophila can simultaneously use self-generated olfactory cues and self-motion cues to learn a spatial goal under visually challenging conditions. Specifically, flies mark a rewarded goal location with self-deposited scents, to which they assign a positive value, and use these scents and their self-motion cues to guide them back to the goal. This learning process is mediated by the mushroom body (MB) - an olfactory learning center responsible for associating odors with reinforcement3 - and by PFN neurons, which encode egocentric translational velocity4,5, a self-motion cue. Intriguingly, when the environment is enriched with prominent external olfactory landmarks, flies shift to prioritizing landmarks over self-generated cues - a strategy adjustment reflected in both the critical circuit involved and an altered transcriptome in the brain. Our findings demonstrate that Drosophila can dynamically adapt to environmental complexities when solving spatial learning tasks by creating and integrating internal and external cues, revealing an unexpected level of sophistication in their cognitive capacities.