Goal learning, memory, and drift in the Drosophila head direction system
Heading information is represented in head direction systems across species, including Drosophila. However, how navigation decisions are made and how goal memories are represented, particularly during rest, is little understood. Here, using a navigation learning assay for flies walking in virtual reality, we describe neural dynamics for direction selection and memory. Neurons in the fan-shaped body, a navigation and memory related structure, continually drift when the animal is at rest, shifted by 180{degrees} compared to walking directions. Optogenetic activation during rest biases subsequent walking direction. Learning leads to changes in drift during rest, revealing a memory of goal direction. Downstream neurons correct the 180{degrees} shift, therefore reactivating walking directions during rest. The connectome reveals a compact circuit architecture for reactivation, as validated using computational modeling. Thus, drift drives behavior, reactivates walking directions during rest, and is shaped by memory, suggesting similarities for memory consolidation in navigation circuits across species.