The perception of visual motion is critical for animal navigation, and flies are a prominent model system for exploring this neural computation. In Drosophila, the T4 cells of the medulla are directionally selective and necessary for ON motion behavioral responses. To examine the emergence of directional selectivity, we developed genetic driver lines for the neuron types with the most synapses onto T4 cells. Using calcium imaging, we found that these neuron types are not directionally selective and that selectivity arises in the T4 dendrites. By silencing each input neuron type, we identified which neurons are necessary for T4 directional selectivity and ON motion behavioral responses. We then determined the sign of the connections between these neurons and T4 cells using neuronal photoactivation. Our results indicate a computational architecture for motion detection that is a hybrid of classic theoretical models.

Highlights d Ionotropic signal amplification occurs in select olfactory receptor neurons (ORNs) d Amplification is mediated by Pickpocket 25 (PPK25), a DEG/ENaC member d Receptor-mediated influx of Ca 2+ , serving as a second messenger, activates PPK25 d A reproductive hormone dynamically regulates PPK25 expression to impact courtship Authors

SignificanceAnimal visual systems are typically thought of by analogy to cameras—sensory systems providing continuous information streams that are processed through fixed algorithms. However, studies in flies and mice have shown that visual neurons are dynamically and adaptively retuned by the behavioral state of the animal. In Drosophila, prominent higher-order neurons in the visual system respond more strongly to fast-moving stimuli once the animal starts walking or flying. In this study, we systematically investigated the neurobiological mechanism governing the behavioral-state modulation of directionally selective neurons in Drosophila. We show that behavioral activity modifies the physiological properties of critical neurons in this visual motion circuit and that neuromodulation by central feedback neurons recapitulates these effects.