Generation of stable heading representations in diverse visual scenes

Many animals rely on an internal heading representation when navigating in varied environments(1–10). How this representation is linked to the sensory cues defining different surroundings is unclear. In the fly brain, heading is represented by ‘compass neurons’ that innervate a ring-shaped structure, the ellipsoid body(3,11,12). Each compass neuron receives inputs from visual-feature-selective ‘ring neurons’(13–16), providing the ideal substrate for the extraction of directional information from a visual scene. We combine two-photon calcium imaging and optogenetics in tethered flying flies with circuit modeling to show how the correlated activity of compass and visual neurons drives plasticity(17–22), that flexibly transforms two-dimensional visual cues into a stable heading representation. We also describe how this plasticity enables the fly to convert a partial heading representation established from orienting within part of a novel setting into a complete heading representation. Our results provide mechanistic insight into memory-related computations essential for flexible navigation in varied surroundings.