Comprehensive Characterization of the Major Presynaptic Elements to the Drosophila OFF Motion Detector

Estimating motion is a fundamental task for the visual system of sighted animals. In Drosophila, direction-selective T4 and T5 cells respond to moving brightness increments (ON) and decrements (OFF), respectively. Current algorithmic models of the circuit are based on the interaction of two differentially filtered signals. However, electron microscopy studies have shown that T5 cells receive their major input from four classes of neurons: Tm1, Tm2, Tm4, and Tm9. Using two-photon calcium imaging, we demonstrate that T5 is the first direction-selective stage within the OFF pathway. The four cells provide an array of spatiotemporal filters to T5. Silencing their synaptic output in various combinations, we find that all input elements are involved in OFF motion detection to varying degrees. Our comprehensive survey challenges the simplified view of how neural systems compute the direction of motion and suggests that an intricate interplay of many signals results in direction selectivity. •All Drosophila OFF motion pathway Tm cells are activated by brightness decrements•None of the four cell types are direction selective•Tm1, Tm2, Tm4, and Tm9 display a variety of temporal filter properties•The four Tm cells are involved in OFF motion processing to different degrees Serbe et al. use calcium imaging, electrophysiology, and behavior to assess the roles of columnar elements in the OFF motion vision pathway of Drosophila. Here, the complex interaction of four cell types shapes the flies’ responses to motion stimuli.