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Direction-selective T4/T5 neurons exist in four subtypes, each tuned to visual motion along one of the four cardinal directions. Along with their directional tuning, neurons of each T4/T5 subtype orient their dendrites and project their axons in a subtype-specific manner. Directional tuning, thus, appears strictly linked to morphology in T4/T5 neurons. How the four T4/T5 subtypes acquire their distinct morphologies during development remains largely unknown. Here, we investigated when and how the dendrites of the four T4/T5 subtypes acquire their specific orientations, and profiled the transcriptomes of all T4/T5 neurons during this process. This revealed a simple and stable combinatorial code of transcription factors defining the four T4/T5 subtypes during their development. Changing the combination of transcription factors of specific T4/T5 subtypes resulted in predictable and complete conversions of subtype-specific properties, i.e. dendrite orientation and matching axon projection pattern. Therefore, a combinatorial code of transcription factors coordinates the development of dendrite and axon morphologies to generate anatomical specializations that differentiate subtypes of T4/T5 motion-sensing neurons., Summary: Morphological and transcriptomic analyses allowed the identification of a combinatorial code of transcription factors that controls the development of subtype-specific morphologies in motion-detecting neurons of the Drosophila visual system.

In the Drosophila visual system, T4/T5 neurons represent the first stage of computation of the direction of visual motion. T4 and T5 neurons exist in four subtypes, each responding to motion in one of the four cardinal directions and projecting axons into one of the four lobula plate layers. However, all T4/T5 neurons share properties essential for sensing motion. How T4/T5 neurons acquire their properties during development is poorly understood. We reveal that the transcription factors SoxN and Sox102F control the acquisition of properties common to all T4/T5 neuron subtypes, i.e. the layer specificity of dendrites and axons. Accordingly, adult flies are motion blind after disruption of SoxN or Sox102F in maturing T4/T5 neurons. We further find that the transcription factors Ato and Dac are redundantly required in T4/T5 neuron progenitors for SoxN and Sox102F expression in T4/T5 neurons, linking the transcriptional programmes specifying progenitor identity to those regulating the acquisition of morphological properties in neurons. Our work will help to link structure, function and development in a neuronal type performing a computation that is conserved across vertebrate and invertebrate visual systems., Summary: RNA interference identifies SoxN and Sox102F as key regulators of the morphological properties of a neuronal type of the fruit fly visual system that computes the direction of motion.

Avoidance of predators or impending collisions is important for survival. Approaching objects can be mimicked by expanding flow-fields. Tethered flying fruit flies, when confronted with an expansion flow-field, reliably turn away from the pole of expansion when presented laterally, or perform a landing response when presented frontally. Here, we show that the response to an expansion flow-field is independent of the overall luminance change and edge acceleration. As we demonstrate by blocking local motion-sensing neurons T4 and T5, the response depends crucially on the neural computation of appropriately aligned local motion vectors, using the same hardware that also controls the optomotor response to rotational flow-fields.