Lobula-specific visual projection neurons are involved in perception of motion-defined second-order motion in Drosophila

A wide variety of animal species including humans and fruit flies see second-order motion although they lack coherent spatiotemporal correlations in luminance. Recent electrophysiological recordings, together with intensive psychophysical studies, are bringing to light the neural underpinnings of second-order motion perception in mammals. However, where and how the higher-order motion signals are processed in the fly brain is poorly understood. Using the rich genetic tools available in Drosophila and examining optomotor responses in fruit flies to several stimuli, we revealed that two lobula-specific visual projection neurons, specifically connecting the lobula and the central brain, are involved in the perception of motion-defined second-order motion, independent of whether the second-order feature is moving perpendicular or opposite to the local first-order motion. By contrast, blocking these neurons has no effect on first-order and flicker-defined second-order stimuli in terms of response delay. Our results suggest that visual neuropils deep in the optic lobe and the central brain, whose functional roles in motion processing were previously unclear, may be specifically required for motion-defined motion processing.