Postembryonic development of amplifying neuroblast lineages in the "Drosophila" brain : proliferation, differentiation and projection patterns

Abstract

We identified a novel mode of neurogenesis in the larval brain of Drosophila that involves the amplification of neuroblast proliferation through intermediate progenitors (IPs). These intermediate neural progenitors are generated by asymmetric division of a subset of the Drosophila brain neuroblasts, which we refer to as dorsomedial neuroblasts (DM neuroblasts). These neuroblasts divide asymmetrically to self-renew, but unlike the other brain neuroblasts do not segregate the cell fate determinant Prospero to the daughter cells. As a result, in contrast to conventional ganglion mother cells (GMC), intermediate progenitors undergo multiple divisions and express molecular markers of self-renewing neuroblasts. The novel IPs described here have remarkable similarities to the IPs that have been identified recently in mammalian brain development. We analyzed the type and fate of cells generated in the DM lineages. With a combination of neuronal and glial cell markers we show that the DM lineages generate not only neurons but also glial cells. The DM neuroblasts thus represent the first identified multipotent precursor cells in the fly brain during postembryonic development. We also show that the adult-specific neurons of each DM lineage form several spatially separated axonal fascicles some of which project along larval brain commissural structures which are primordia of future adult midline neuropil. By taking advantage of a DM-specific Gal4 reporter line we identify and follow DM-derived neuronal cells into early pupal stages and demonstrate that neurons of the DM lineages make a major contribution to the developing central complex, in that the numerous columnar elements are likely to be DM lineage-derived. These findings suggest that the amplification of proliferation which characterizes DM lineages may be an important requirement for generating the large number of neurons required in highly complex neuropil structures such as the central complex in the Drosophila brain.