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Many animals navigate using a combination of visual landmarks and path integration. In mammalian brains, head direction cells integrate these two streams of information by representing an animal's heading relative to landmarks, yet maintaining their directional tuning in darkness based on self-motion cues. Here we use two-photon calcium imaging in head-fixed Drosophila melanogaster walking on a ball in a virtual reality arena to demonstrate that landmark-based orientation and angular path integration are combined in the population responses of neurons whose dendrites tile the ellipsoid body, a toroidal structure in the centre of the fly brain. The neural population encodes the fly's azimuth relative to its environment, tracking visual landmarks when available and relying on self-motion cues in darkness. When both visual and self-motion cues are absent, a representation of the animal's orientation is maintained in this network through persistent activity, a potential substrate for short-term memory. Several features of the population dynamics of these neurons and their circular anatomical arrangement are suggestive of ring attractors, network structures that have been proposed to support the function of navigational brain circuits.
Visual landmarks can provide animals with a reliable indicator of their whereabouts1. In the absence of such cues, many animals track their position relative to a reference point by continuously monitoring their own motion, a process called path integration2. Estimates of position based purely on self-motion cues, however, can accumulate error over time. Successful navigation then, requires animals to flexibly combine these distinct sources of information1. In mammalian brains this process of integration is evident in head direction cells3, which are neurons sensitive to an animal's heading relative to visual cues in its surroundings that maintain their representation of heading in total darkness using self-motion cues4. With their smaller brains and identifiable neurons, insects offer tractable systems to examine the integrative neural computations underlying navigation5. Indeed, many insects (for example, desert ants and honeybees6,7) are known to navigate using landmarks and path integration1. Experiments in a variety of insects indicate the involvement of the central complex (CX)-a brain region conserved across insects-in such behaviour. In the fruitfly, behavioural genetics experiments have suggested that theCXis required for several components of navigation, including memory for visual landmarks8, patterns9 and places10, and directional motor control11. Electrophysiological recordings in...