Synaptic organization in the adult Drosophila mushroom body calyx

Abstract

Insect mushroom bodies are critical for olfactory associative learning. We have carried out an extensive quantitative description of the synaptic organization of the calyx of adult Drosophila melanogaster, the main olfactory input region of the mushroom body. By using high-resolution confocal microscopy, electron microscopy-based three-dimensional reconstructions, and genetic labeling of the neuronal populations contributing to the calyx, we resolved the precise connections between large cholinergic boutons of antennal lobe projection neurons and the dendrites of Kenyon cells, the mushroom body intrinsic neurons. Throughout the calyx, these elements constitute synaptic complexes called microglomeruli. By single-cell labeling, we show that each Kenyon cell's claw-like dendritic specialization is highly enriched in filamentous actin, suggesting that this might be a site of plastic reorganization. In fact, Lim kinase (LimK) overexpression in the Kenyon cells modifies the shape of the microglomeruli. Confocal and electron microscopy indicate that each Kenyon cell claw enwraps a single bouton of a projection neuron. Each bouton is contacted by a number of such claw-like specializations as well as profiles of gamma-aminobutyric acid-positive neurons. The dendrites of distinct populations of Kenyon cells involved in different types of memory are partially segregated within the calyx and contribute to different subsets of microglomeruli. Our analysis suggests, though, that projection neuron boutons can contact more than one type of Kenyon cell. These findings represent an important basis for the functional analysis of the olfactory pathway, including the formation of associative olfactory memories.

DrosophilaLarvae Establish Appetitive Olfactory Memories via Mushroom Body Neurons of Embryonic Origin

“…5A-D, upper rows). These results suggest that these four lines express GAL4 in different sets of embryonicand larval-born ␥ neurons that have presynaptic and postsynaptic sites in the calyces, as recently reported for the adult MBs (Leiss et al, 2009), while being exclusively presynaptic in the lobes. c305a crossed to UAS-nsyb::GFP very weakly labeled both calyx and lobes (Fig.…”

Transmission, Development, and Plasticity of Synapses

“…Antennal lobe projection neurons (PNs) send axonal projections to the mushroom body calyx, where they form specialized synaptic clusters called microglomeruli. Within a microglomerulus, synapses are characterized by large presynaptic boutons surrounded by claw-like dendritic specializations from multiple Kenyon cells (Yasuyama et al 2002;Leiss et al 2009). AZs, PSDs, and components of the synaptic cleft can be clearly resolved at these mushroom body input synapses, providing a model to examine AZ organization at a central cholinergic synapse (Kremer et al 2010;Nakayama et al 2014).…”

What the fly’s nose tells the fly’s brain

“…Each Kenyon cell has about six claws (16), so one Kenyon cell collects information from only about 6 of the 50 glomeruli. The single APL neuron (only one on each side of the brain) sends its dendrites into the mushroom body lobes to collect the output from all of the Kenyon cell axons, and this APL neuron inhibits all Kenyon cells by sending its axons to the calycal microglomeruli to terminate on Kenyon cell dendrites (18)(19)(20).…”