Abstract
Understanding information flow through neuronal circuits requires knowledge of their synaptic organization. In this study, we utilized fluorescent pre- and postsynaptic markers to map synaptic organization in the Drosophila antennal lobe, the first olfactory processing center. Olfactory receptor neurons (ORNs) produce a constant synaptic density across different glomeruli. Each ORN within a class contributes nearly identical active zone number. Active zones from ORNs, projection neurons (PNs), and local interneurons have distinct subglomerular and subcellular distributions. The correct number of ORN active zones and PN acetylcholine receptor clusters requires the Teneurins, conserved transmembrane proteins involved in neuromuscular synapse organization and synaptic partner matching. Ten-a acts in ORNs to organize presynaptic active zones via the spectrin cytoskeleton. Ten-m acts in PNs autonomously to regulate acetylcholine receptor cluster number and transsynaptically to regulate ORN active zone number. These studies advanced our ability to assess synaptic architecture in complex CNS circuits and their underlying molecular mechanisms.
Highlights
Understanding how neural circuits process information requires knowing the neuroanatomical connectivity and electrophysiological properties of individual neurons, and the organization of synapses between specific neuronal types
We identified distinct rules that govern the number, density, and spatial organization of olfactory synapses for multiple classes of neurons. To understand how these rules are implemented at the molecular level, we investigated the function of the Teneurins, evolutionarily conserved type II transmembrane proteins recently shown to regulate synaptic partner matching and neuromuscular synaptic organization (Hong et al, 2012; Mosca et al, 2012)
We found that all three types of neurons had distinct mean nearest neighbor distance (NND) values (Figure 3G–I): Olfactory receptor neurons (ORNs) had the closest puncta and local interneurons (LNs) the furthest with projection neurons (PNs) falling in between the two
Summary
Understanding how neural circuits process information requires knowing the neuroanatomical connectivity and electrophysiological properties of individual neurons, and the organization of synapses between specific neuronal types. Serial-section electron microscopy (EM) has offered remarkable resolution in studying CNS synapses in the context of circuits, including the entire Caenorhabditis elegans nervous system (White et al, 1986), the mouse olfactory bulb (Hinds and Hinds, 1976a, 1976b), retina (Briggman et al, 2011; Helmstaedter et al, 2013), and visual cortex (Bock et al, 2011), and the Drosophila visual system (Meinertzhagen and O'Neil, 1991; Takemura et al, 2013) These approaches are labor intensive and not amenable to analysis following genetic perturbation, at varying developmental stages, or with intact samples. Current work in Drosophila has sought to fulfill this need (Kremer et al, 2010; Christiansen et al, 2011; Berger-Muller et al, 2013; Chen et al, 2014)
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