Postembryonic lineages of the Drosophila brain: I. Development of the lineage-associated fiber tracts

Abstract

Neurons of the Drosophila central brain fall into approximately 100 paired groups, termed lineages. Each lineage is derived from a single asymmetrically-dividing neuroblast. Embryonic neuroblasts produce 1,500 primary neurons (per hemisphere) that make up the larval CNS followed by a second mitotic period in the larva that generates approximately 10,000 secondary, adult-specific neurons. Clonal analyses based on previous works using lineage-specific Gal4 drivers have established that such lineages form highly invariant morphological units. All neurons of a lineage project as one or a few axon tracts (secondary axon tracts, SATs) with characteristic trajectories, thereby representing unique hallmarks. In the neuropil, SATs assemble into larger fiber bundles (fascicles) which interconnect different neuropil compartments. We have analyzed the SATs and fascicles formed by lineages during larval, pupal, and adult stages using antibodies against membrane molecules (Neurotactin/Neuroglian) and synaptic proteins (Bruchpilot/N-Cadherin). The use of these markers allows one to identify fiber bundles of the adult brain and associate them with SATs and fascicles of the larval brain. This work lays the foundation for assigning the lineage identity of GFP-labeled MARCM clones on the basis of their close association with specific SATs and neuropil fascicles, as described in the accompanying paper (Wong et al., 2013. Postembryonic lineages of the Drosophila brain: II. Identification of lineage projection patterns based on MARCM clones. Submitted.).

A conserved plan for wiring up the fan-shaped body in the grasshopper and Drosophila

“…At the same time we have analysed the commissural organization itself at these stages (Figs. 4–6) using the nomenclature applicable to the grasshopper (Boyan et al 1993) and Drosophila (Pereanu et al 2010; Lovick et al, 2013). Our analysis leads us to the conclusion that in setting up the columnar neuroarchitecture of the fan-shaped body, comparable choices are being made by subsets of axons from equivalent lineages in both the grasshopper and Drosophila , consistent with a conserved wiring plan for this brain region.…”

“…It is therefore now possible to assign distinctive (adult) commissural identities to the four embryonic commissural systems as summarized in Fig. 4c–e (and see Lovick et al 2013; Hartenstein et al 2015). The ventro-anterior system includes the antennal lobe commissure (ALC; defined by lineages BAmd1/BAmd2), as well as the subellipsoid body commissure (SuEC, defined by DALcl1) and the lateral accessory lobe commissure (LALC, defined by CM1; the SuEC and LALC cannot yet be spatially separated in the late embryo/early L1).…”

“…The w, x, y, z (CM4, DPMpm2, DPMpm1 and DPMm1, respectively) lineages proliferate as type II lineages, generating approximately 450 neurons each (Bello et al 2008). Similar to their primary counterparts, secondary W, X, Y, Z lineages form multiple axon tracts (Pereanu and Hartenstein 2006; Cardona et al 2010; Lovick et al 2013; Yang et al 2013), which are likely to correspond to the individual W, X, Y, Z sublineages. For each lineage, one pair of parallel, closely apposed tracts, joins the prFB.…”

“…These cell clusters form part of four bilateral lineages called W, X, Y, Z in the grasshopper (Boyan and Williams 1997) and DPMm1/DM1, DPMpm1/DM2, DPMpm2/DM3, CM4/DM4 in Drosophila (Ito et al, 2013; Lovick et al, 2013; Wong et al, 2013; Yang et al, 2013; Yu et al, 2013; for simplicity sake, we will refer to the lineages as W, X, Y, Z for both species from here on onward). Based on the finding that their spatial arrangement and developmental characteristics are very similar in flies and locusts, the lineages are assumed to be homologous (Boyan et al, 2015).…”

“…Developmental studies have revealed that the intricate columnar wiring of the fan-shaped body is established quite rapidly, but at stages which also vary with the lifestyle of the insect. In the grasshopper, it develops fully during embryogenesis (Boyan et al 2008b, 2015), while in flies, it happens during pupal stages (Renn et al 1999; Young and Armstrong 2010; Lovick et al, 2013; Riebli et al 2013; Wolff et al 2015; Lovick et al, 2017). The columnar neuroarchitecture itself is generated by a sophisticated mechanism of axogenesis known as “fascicle switching” in which a subset of W-Z axons of the embryonic grasshopper (Boyan et al 2008b) and larval Drosophila (Young and Armstrong 2010; Riebli et al 2013) brain decussates at stereotypic locations along the brain commissure, resulting in a discrete set of fiber bundles oriented orthogonally to the commissure.…”