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.