A region-specific neurogenesis mode requires migratory progenitors in the Drosophila visual system

Brain areas each generate specific neuron subtypes during development. However, underlying regional variations in neurogenesis strategies and regulatory mechanisms remain poorly understood. In Drosophila, neurons in four optic lobe ganglia originate from two neuroepithelia, the outer (Opc) and inner (Ipc) proliferation centers. Using genetic manipulations, we demonstrate that one Ipc neuroepithelial domain progressively transforms into migratory progenitors that mature into neural stem cells/neuroblasts within a second domain. Progenitors emerge by an epithelial-mesenchymal transition-like mechanism, requiring the Snail-family member Escargot and, in subdomains, Decapentaplegic signaling. The proneural factors Lethal of scute and Asense differentially control progenitor supply and maturation into neuroblasts. These switch expression from Asense to a third proneural protein, Atonal. Dichaete and Tailless mediate this transition essential for generating two neuron populations at defined positions. We propose that this neurogenesis mode is central for setting-up a new proliferative zone to facilitate spatio-temporal matching of neurogenesis and connectivity across ganglia.