Feature detecting columnar neurons mediate object tracking saccades in Drosophila

Tracking visual objects while stabilizing the visual background is complicated by the different computational requirements for object tracking and motion vision. In fruit fly, directionally selective motion detectors T4 and T5 cells supply wide-field neurons of the lobula plate, which control smooth gaze stabilization behavior. Here, we hypothesized that an anatomically parallel pathway supplied by T3, which encodes small moving objects and innervates the lobula, drives body saccades toward objects. We combined physiological and behavioral experiments to show that T3 neurons respond omnidirectionally to contrast changes induced by the visual stimuli that elicit tracking saccades, and silencing T3 reduced the frequency of tracking saccades. By contrast, optogenetic manipulation of T3 increased the number of tracking saccades. Our results represent the first evidence that parallel motion detection and feature detection pathways coordinate smooth gaze stabilization and saccadic object tracking behavior during flight.