Transcriptional control of morphological properties of direction-selective T4/T5 neurons inDrosophila

Abstract

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.

A combinatorial code of transcription factors specifies subtypes of visual motion-sensing neurons in Drosophila

“…In particular, Grain acts together with different transcription factors in T4/T5b and T4/T5c subtypes to coordinate dendrite and axon morphogenesis in order to differentiate their morphologies from those of T4/T5a and T4/T5d, respectively. The coordinate regulation of different aspects of neuron morphogenesis by the same set of transcription factors might provide a general strategy to ensure the establishment of precise neuron wiring patterns during development (Enriquez et al, 2015;Santiago and Bashaw, 2017;Schilling et al, 2019). Furthermore, the combinations of transcription factors controlling the development of subtype-specific properties do not appear to regulate morphological…”

“…Finally, we tested whether grain loss of function in T4/T5b (normally Dac + /Ab + /Grain + ) and T4/T5c (normally Omb + /Pros + /Grain + ) results in neurons with morphological properties of T4/T5a (Dac + /Ab + /Grain -) and T4/T5d (Omb + /Pros + /Grain -) subtypes. To this end, we first performed a knockdown of grain in all developing T4/T5 neurons with RNA interference (RNAi) and the R39H12-Gal4, which drives expression in T4/T5 neurons of all subtypes from late third instar (L3) larval stage on (Schilling et al, 2019). This resulted in adult T4/T5 neurons with dendrites showing no defects in their neuropil-and layer-specific innervation but with axons failing to form four layers in the lobula plate ( Fig.…”

“…the restriction of dendrites and axons to single neuropil layers. The acquisition of these morphological properties is controlled postmitotically by two transcription factors of the SOX family, SoxN and Sox102F (Contreras et al, 2018;Schilling et al, 2019). Therefore, distinct sets of transcription factors control differentially subtype-specific properties and properties that are shared by all T4/T5 subtypes, shedding light on the developmental strategies that ensure that each neuron acquires its complete morphological signature.…”

“…SoxN and Sox102F expression in all T4/T5 subtypes arises from temporal patterning of the neuroblasts precursors of T4/T5 neurons (Apitz and Salecker, 2015;Schilling et al, 2019). Spatial patterning of the neuroepithelium that generates T4/T5-producing neuroblasts results in the specific expression of omb in neuroblasts that are precursors of T4/T5c,d neurons.…”

“…The T4/T5 neuronal population of the Drosophila visual system provides a unique model for the study of this process. All T4/T5 neurons must acquire common morphological properties that set them apart from other visual interneurons and are important for their function as local motion sensors (Maisak et al, 2013;Shinomiya et al, 2015;Schilling et al, 2019). However, among the T4/T5 neurons, distinct subtypes with anatomical specializations relevant for the detection of motion along different directions must be specified (Fischbach and Dittrich, 1989;Maisak et al, 2013).…”