Abstract
ABSTRACTIn 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.
Highlights
The formation of neural circuits comprising neurons with specific morphological and physiological properties is key for the proper function of the brain
Silencing SoxN or Sox102F in T4/T5 neurons impairs the optomotor response To find molecular players involved in the terminal differentiation of T4/T5 neurons, we pursued a candidate gene approach focusing on transcription factors revealed to be highly expressed in T4/T5 neurons by a transcriptome analysis (Pankova and Borst, 2016)
Sox102F expression was severely reduced in T4/T5 neurons upon SoxN knockdown with the R40E11Gal4 line (Fig. 3A-C, Fig. S3A-C), and in SoxN mutant T4/T5 neurons generated by mosaic analysis with a repressible cell marker (MARCM) (Fig. 3G-J)
Summary
The formation of neural circuits comprising neurons with specific morphological and physiological properties is key for the proper function of the brain. The Drosophila optic lobe has emerged as a powerful model in which to study this process. It consists of four neuropils downstream of the retina: lamina, medulla, lobula and lobula plate, all made of repeating columns that process signals from specific points in space and are arranged in a retinotopic fashion. The medulla, lobula and lobula plate are subdivided into layers that process distinct visual features in parallel (Maisak et al, 2013; Strother et al, 2014). The four neuropils of the optic lobe contain more than 100 different neuronal types (Fischbach and Dittrich, 1989), some of which have been studied in great anatomical and functional detail. Whereas T4 neurons have their dendrites in the medulla and receive input from neurons encoding brightness increments, T5
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