Postembryonic lineages of the Drosophila brain: II. Identification of lineage projection patterns based on MARCM clones

Abstract

The Drosophila central brain is largely composed of lineages, units of sibling neurons derived from a single progenitor cell or neuroblast. During the early embryonic period neuroblast generate the primary neurons that constitute the larval brain. Neuroblasts reactivate in the larva, adding to their lineages a large number of secondary neurons which, according to previous studies in which selected lineages were labeled by stably expressed markers, differentiate during metamorphosis, sending terminal axonal and dendritic branches into defined volumes of the brain neuropil. We call the overall projection pattern of neurons forming a given lineage the “projection envelope” of that lineage. By inducing MARCM clones at the early larval stage, we labeled the secondary progeny of each neuroblast. For the supraesophageal ganglion excluding mushroom body (the part of the brain investigated in the present work) we obtained 81 different types of clones, Based on the trajectory of their secondary axon tracts (described in the accompanying paper), we assigned these clones to specific lineages defined in the larva. Since a labeled clone reveals all aspects (cell bodies, axon tracts, terminal arborization) of a lineage, we were able to describe projection envelopes for all secondary lineages of the supraesophageal ganglion. This work provides a framework by which the secondary neurons (forming the vast majority of adult brain neurons) can be assigned to genetically and developmentally defined groups. It also represents a step towards the goal to establish, for each lineage, the link between its mature anatomical and functional phenotype, and the genetic make-up of the neuroblast it descends from.

Hydroxyurea-mediated neuroblast ablation establishes birth dates of secondary lineages and addresses neuronal interactions in the developing Drosophila brain

“…Similar to primary neurons, secondary neurons of a given lineage form coherent clusters of neuronal cell bodies and project axons which bundle together as the secondary axon tract (SAT). Secondary axon tracts form a stereotyped, conspicuous pattern that is visible from the larva through metamorphosis into the adult stage (Lovick et al, 2013; Wong et al, 2013). Differentiation of secondary neurons (i.e.…”

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

“…Of these, four - termed W, X, Y, Z - have been identified as generating progeny whose axons project via the w, x, y, z tracts to the protocerebral bridge and then to the midbrain where they form a columnar fiber system within the fan-shaped body (see Boyan and Reichert 2011). Note that W-Z include numerous other populations of neurons whose projections, some of them commissural, are outside the central complex (see Wong et al, 2013, for description of these projections in Drosophila ). The location of W-Z in the protocerebrum of the grasshopper (Fig.…”

“…According to Pereanu and Hartenstein (2006), Wong et al (2013) and Hartenstein et al (2015) W = CM4, X = DPMpm2, Y = DPMpm1, and Z = DPMm1 respectively. A number of other authors (see citations in Riebli et al 2013) on the other hand, refer to W = DM4, X = DM3, Y = DM2 and Z = DM1.…”

“…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).…”

Insights into brain development and disease from neurogenetic analyses in Drosophila melanogaster

“…Through their proliferative activity, neuroblasts each generate a family-like lineage of neural progeny (figure 2). Thus, the central brain is a complex aggregation of approximately 100 pairs of neuroblast lineages Ito et al 2013;Wong et al 2013). The neurons in each of these lineages generally manifest similar, albeit not identical, neuroanatomical features.…”