Drosophila embryonic type II neuroblasts: origin, temporal patterning, and contribution to the adult central complex

Abstract

neuroblasts are an excellent model for investigating how neuronal diversity is generated. Most brain neuroblasts generate a series of ganglion mother cells (GMCs) that each make two neurons (type I lineage), but 16 brain neuroblasts generate a series of intermediate neural progenitors (INPs) that each produce 4-6 GMCs and 8-12 neurons (type II lineage). Thus, type II lineages are similar to primate cortical lineages, and may serve as models for understanding cortical expansion. Yet the origin of type II neuroblasts remains mysterious: do they form in the embryo or larva? If they form in the embryo, do their progeny populate the adult central complex, as do the larval type II neuroblast progeny? Here, we present molecular and clonal data showing that all type II neuroblasts form in the embryo, produce INPs and express known temporal transcription factors. Embryonic type II neuroblasts and INPs undergo quiescence, and produce embryonic-born progeny that contribute to the adult central complex. Our results provide a foundation for investigating the development of the central complex, and tools for characterizing early-born neurons in central complex function.

Origin and specification of type II neuroblasts in the Drosophila embryo

“…As we have not been able to distinguish between embryonic INPs generated during different temporal windows, we cannot say whether all INPs express the same temporal series of genes or whether this is determined by the factors expressed by the NB at the time the INP is generated. In an article published while this manuscript was being reviewed (Walsh and Doe, 2017), the authors report that, unlike our observations, there was no expression of Ey in the embryonic INPs. This apparent contradiction could be explained if INPs generated by the same NB in different temporal windows express either a different temporal cascade or bypass some of the components of the cascade.…”

Sequence heterochrony led to a gain of functionality in an immature stage of the central complex: A fly–beetle insight

“…These neurons are required for the formation of the typical columnar architecture of the CB and PB [15,16,24,28]. Work in S. gregaria and D. melanogaster provided insights into how the complex innervation architecture develops and specifically, how fascicle switching leads to X-shaped crossings of neurites called decussations, which represent the cellular substrate of the columnar architecture of the CB [7,12,13,15,[29][30][31]. An overview on the relevant developmental processes is summarized in Fig 1B. The low number of neural cells in insect brains compared with vertebrates, the conservation of neural lineages building up the brain, and their experimental accessibility makes insects an excellent choice to study the mechanisms of brain diversification during development.…”

Light stimuli and circadian clock affect neural development inDrosophila melanogaster

“…To distinguish Type II NBs, UAS::mCD8-GFP was expressed under the control of wor-Gal4, ase-Gal80 (Neumüller et al 2011). Additionally, anti-Deadpan (Dpn) and anti-Asense (Ase) antibodies were used to differentiate between progenies of Type II NBs, as Dpn is expressed only in mINPs and Type II NBs, whereas Ase labels iINPs, GMCs and is also co-expressed in mINPs (Bowman et al 2008, Walsh & Doe 2017. To ensure whether the growth defect is restricted to a certain type of NBs or it is a general effect, we also measured NB size.…”

“…Type II NBs and their lineages were marked with GFP by using UAS::mCD8-GFP line under the control of the wor-Gal4, ase-Gal80 driver line (Neumueller et al 2011). To specify between all types of the Type II NB lineages anti-Dpn and anti-Ase antibodies were used (Bowman et al 2008, Walsh & Doe 2017. MB NB derived GMCs and mINPs were counted with Amira® software using the Landmark selection.…”