Patterns of growth, axonal extension and axonal arborization of neuronal lineages in the developing Drosophila brain

Abstract

The Drosophila central brain is composed of approximately 100 paired lineages, with most lineages comprising 100–150 neurons. Most lineages have a number of important characteristics in common. Typically, neurons of a lineage stay together as a coherent cluster and project their axons into a coherent bundle visible from late embryo to adult. Neurons born during the embryonic period form the primary axon tracts (PATs) that follow stereotyped pathways in the neuropile. Apoptotic cell death removes an average of 30–40% of primary neurons around the time of hatching. Secondary neurons generated during the larval period form secondary axon tracts (SATs) that typically fasciculate with their corresponding primary axon tract. SATs develop into the long fascicles that interconnect the different compartments of the adult brain. Structurally, we distinguish between three types of lineages: PD lineages, characterized by distinct, spatially separate proximal and distal arborizations; C lineages with arborizations distributed continuously along the entire length of their tract; D lineages that lack proximal arborizations. Arborizations of many lineages, in particular those of the PD type, are restricted to distinct neuropile compartments. We propose that compartments are ‘scaffolded” by individual lineages, or small groups thereof. Thereby, the relatively small number of primary neurons of each primary lineage set up the compartment map in the late embryo. Compartments grow during the larval period simply by an increase in arbor volume of primary neurons. Arbors of secondary neurons form within or adjacent to the larval compartments, resulting in smaller compartment subdivisions and additional, adult specific compartments.

Origin ofDrosophilamushroom body neuroblasts and generation of divergent embryonic lineages

“…Since cell numbers in the DiI-labeled MBNB clones (on average 29-45 cells at st17 and 36-48 cells in L1) differ drastically from those reported previously in flip-out clones (~14 cells at late st16 and ~8 cells in L1) (Larsen et al, 2009), the latter appear to encompass only part of an embryonic lineage. It is likely that this part represents the late-born cells, as recombination in an NB depends on a critical level of heat shock flippase, which does not become enriched before the early-born part of a lineage has developed (Larsen et al, 2009). Also, MARCM fails to disclose entire NB lineages in the late embryo, as clonal reporter expression additionally relies on the loss of the GAL80 repressor after recombination, which seems to persist throughout embryonic development (Luo, 2005).…”

“…Accordingly, -neurons do not undergo programmed cell death in the embryo (this study), nor, presumably, during postembryonic stages (Technau and Heisenberg, 1982). This is remarkable because ~30-40% of embryonic brain neurons die around the time of larval hatching (Larsen et al, 2009). Interestingly, appetitive olfactory learning in L1 relies on a set of ~100 embryonic-born -neurons (included in the 201y-Gal4 and NP1131-Gal4 lines), indicating that the underlying neuronal circuits at the level of the MBs are established during embryogenesis (Pauls et al, 2010).…”

“…About 100 postembryonic cell lineages (per hemisphere) have been recognized in the larval brain (e.g. Cardona et al, 2010;Kumar et al, 2009;Lai et al, 2008;Larsen et al, 2009;Lichtneckert et al, 2007;Pereanu and Hartenstein, 2006;Yu et al, 2009;Yu et al, 2010), suggesting that almost all embryonic brain NBs become reactivated postembryonically. However, the assignment to individually identified NBs (Urbach and Technau, 2003a) and an analysis of the embryonic components of these brain lineages are still pending.…”

Lipoprotein Particles Cross the Blood–Brain Barrier inDrosophila

“…The neuropil increases in volume during early larval stages as primary neurons further extend neurites and increase their arborization. At the same time, continuous division of neuroblasts in the cortex generates what will become new secondary neurons (Larsen et al, 2009). To assess requirements for lipophorins in the brain at this stage, we used RNA interference to reduce lipophorin production in the fat body (supplemental Fig.…”

The impact of odor–reward memory on chemotaxis in larval Drosophila

“…Larvae of the fruit fly Drosophila melanogaster possess a brain of only 10,000 neurons (Bossing et al 1996;Larsen et al 2009). Nonetheless, these animals display diverse capabilities of orientation including chemo-, photo-, and thermotaxis (Luo et al 2010;Gomez-Marin et al 2011;Louis 2012, 2014;Kane et al 2013;Klein et al 2015) as well as associative learning and memory (for review, see Diegelmann et al 2013;Schleyer et al 2013).…”