Generation of stable heading representations in diverse visual scenes

Summary:

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.