Developmental origins and architecture of Drosophila leg motoneurons

Abstract

Motoneurons are key points of convergence within motor networks, acting as the "output channels" that directly control sets of muscles to maintain posture and generate movement. Here we use genetic mosaic techniques to reveal the origins and architecture of the leg motoneurons of Drosophila. We show that a small number of leg motoneurons are born in the embryo but most are generated during larval life. These postembryonic leg motoneurons are produced by five neuroblasts per hemineuromere, and each lineage generates stereotyped lineage-specific projection patterns. Two of these postembryonic neuroblasts generate solely motoneurons that are the bulk of the leg motoneurons. Within the largest lineage, lineage 15, we see distinct birth-order differences in projection patterns. A comparison of the central projections of leg motoneurons and the muscles they innervate reveals a stereotyped architecture and the existence of a myotopic map. Timeline analysis of axonal outgrowth reveals that leg motoneurons reach their sites of terminal arborization in the leg at the time when their dendrites are elaborating their subtype-specific shapes. Our findings provide a comprehensive description of the origin, development, and architecture of leg motoneurons that will aid future studies exploring the link between the assembly and organization of connectivity within the leg motor system of Drosophila.

Differing Strategies Despite Shared Lineages of Motor Neurons and Glia to Achieve Robust Development of an Adult Neuropil in Drosophila

“…Type 3 clones labeled NG and a single motor neuron that targeted a body wall muscle at the base of the coxa (n = 16) (Figure 4F). Notably, this motor neuron was previously described to be derived from Lin A (Brierley et al, 2012), a conclusion that we confirm and revise below.…”

“…Remarkably, in twin clones where GFP labels Lin A motor neurons, the RFP + progeny are composed of Repo + NG and a single motor neuron that targets a body wall muscle at the base of the coxa (Figures 5L–5M), the same motor neuron that was observed in our cis 2 MARCM experiments (Figure 4D). This motor neuron has also been described previously to be part of Lin A (Brierley et al, 2012). Similar results were obtained when Lin A QMARCM/MARCM clones were generated in L2 or early L3, consistent with the timing inferred from our lineage tracing experiments (data not shown).…”

“…Previous studies have revealed that each of the 47 leg motor neurons have a specific birth date and morphology, characterized by their axonal targeting, dendritic arbor, and cell body position (Baek and Mann, 2009; Brierley et al, 2012). We recently characterized Lin B, a lineage that produces only 7 motor neurons, and described a post-mitotic code of mTFs that controls individual motor neuron morphologies (Enriquez et al, 2015).…”

“…For example, the ~50 motor neurons (MNs) that innervate each leg in adult Drosophila are born from invariant NB lineages and have highly stereotyped birthdates and morphologies (Baek and Mann, 2009; Brierley et al, 2012). These stereotyped morphologies can be seen both in the muscles these motor neurons target and in their elaborate dendritic arbors that establish a very large number of synapses in dense neuropils present in each thoracic neuromere of the ventral nerve cord (VNC) (Court et al, 2017).…”

Microtubule Acetylation Is Required for Mechanosensation in Drosophila

“…The internal patch pipette solution contained (in mM): 140 potassium aspartate, 10 HEPES, 1 EGTA, 4 MgATP, 0.5 Na 3 GTP, 1 KCl, and 13 biocytin hydrazide (pH 7.2, osmolarity adjusted to ~265 mOsm). We distinguished MNs from other glutamatergic neurons by the characteristic and reliable positions of their cell bodies (Baek and Mann, 2009; Brierley et al, 2012), as well as their intrinsic properties (input resistance, resting membrane potential, and spike waveform).…”