Connecting the eye to the brain: retina structure shapes neuron function in Drosophila motion vision

The changes in the visual scene caused by movement generate optic flows, which are used by animals to guide navigation. In flies, optic flow is first estimated in small patches by directionally selective T4 neurons, then integrated by downstream “self-motion” neurons. Because of the limitations of conventional methods, the diversity of self-motion neurons and the visual patterns that flies can detect remains largely unknown. Here we scanned a whole fly head using µCT to determine the ommatidia’s viewing directions. We then reconstructed hundreds of T4 neurons and all their columnar input Mi1 neurons in a whole brain EM volume. We computed the T4 preferred directions (PDs) in a global anatomical reference frame established by the Mi1 neurons. Using the 1-to-1 mapping between the ommatidia and columnar neurons, we then mapped T4 PDs to the eye coordinates. We observed a stereotypical arborization pattern of T4 dendrites, and a retina location-dependent directional tuning of the PDs, providing a simple anatomical basis for previously unexplained observations about the structure of encoded optic flow fields. Finally, we identified and reconstructed the complete set of self-motion neurons in the same EM volume. Using the T4 PD map, we computationally predicted the receptive fields of these self-motion neurons and the body motion they encode. These predictions compare favorably with available physiology measurements, and readily provide experimentally testable hypotheses for future studies.