Visual circuitry for distance estimation in Drosophila

Abstract

Animals must infer the three-dimensional structure of their environment from two-dimensional images on their retinas. In particular, visual cues like motion parallax and binocular disparity can be used to judge distances to objects. Studies across several animal models have found neural signals that correlate with visual distance, but the causal role of these neurons in distance estimation as well as the range of possible neural properties that can inform distance estimation have remained poorly understood. Here, we developed a novel high-throughput behavioral assay to identify neurons in the Drosophila visual system that are involved in distance estimation during free locomotion. We found that silencing the primary motion detectors in the fly visual system eliminated their ability to perceive distance, consistent with a reliance on motion parallax to judge distance. Through a targeted silencing screen of visual neurons during behavior and through in vivo two-photon microscopy, we identified a visual projection neuron that encodes the parallax signal in the relative motion of foreground and background. Interestingly, it differs from previously identified parallax-tuned neurons in its lack of direction selectivity both to moving bars and to moving backgrounds. This non-canonical tuning is interpretable in the context of parallax signals that the fly would likely encounter during naturalistic walking behavior. Our results demonstrate how both direction selective and non-direction selective feature-detecting neurons can contribute to distance estimation using parallax cues, providing a framework for considering broader classes of parallax-encoding neurons in distance estimation across visual systems.