Goal learning, memory, and drift in the Drosophila head direction system

Selecting and memorizing goal direction are essential for navigation behavior. Heading information is represented in the head direction systems across species, including Drosophila. However, how navigation decisions are made and how goal memories are represented in these systems is little understood. Here, using a navigation learning assay for flies walking in virtual reality during two-photon imaging, we describe neural dynamics for direction selection and memory. We find that neurons which encode walking direction in the fan-shaped body, a navigation and learning related area in the center of the fly brain, show continuing autonomous activity or directional drift when the animal is at rest. Drift during rest centers around opposite directions to activity during walking, suggesting different computations between these two behavioral states. Targeted optogenetic activation of these neurons during rest is sufficient to induce a subsequent directional navigation preference. Learning leads to changes in drift distributions during rest depending on goal direction, revealing a memory in the network. The flys head direction system thus offers a compact architecture for direction selection, learning, and memory. Changes in neural representations due to goal learning and between rest and walking suggest similarities in navigation circuits across species.