Spatio-temporal relays control layer identity of direction-selective neuron subtypes in Drosophila

Visual motion detection in sighted animals is essential to guide behavioral actions ensuring their survival. In Drosophila , motion direction is first detected by T4/T5 neurons. Their axons innervate one of the four lobula plate layers. How T4/T5 neurons with layer-specific representation of motion-direction preferences are specified during development is unknown. We show that diffusible Wingless (Wg) between adjacent neuroepithelia induces its own expression to form secondary signaling centers. These activate Decapentaplegic (Dpp) signaling in adjacent lateral tertiary neuroepithelial domains dedicated to producing layer 3/4-specific T4/T5 neurons. T4/T5 neurons derived from the core domain devoid of Dpp signaling adopt the default layer 1/2 fate. Dpp signaling induces the expression of the T-box transcription factor Optomotor-blind (Omb), serving as a relay to postmitotic neurons. Omb-mediated repression of Dachshund transforms layer 1/2- into layer 3/4-specific neurons. Hence, spatio-temporal relay mechanisms, bridging the distances between neuroepithelial domains and their postmitotic progeny, implement T4/T5 neuron-subtype identity. Direction-selective T4/T5 neurons show layer-specific projections in the fly visual circuit. Examining the mechanisms behind their development, the authors found that a relay of Wnt and Bmp signaling across neuroepithelial domains and transcription factor interactions specify T4/T5 subtype identity.