Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila

Abstract

The larval brain of Drosophila is a useful model to study olfactory processing because of its cellular simplicity. The early stages of central olfactory processing involve the detection of odor features, but the coding mechanisms that transform them into a representation in higher brain centers is not clear. Here we examine the pattern of connectivity of the main neurons that process olfactory information in the calyx (dendritic region) of the mushroom bodies, a higher brain center essential for associative olfactory learning. The larval calyx has a glomerular organization. We generated a map of calyx glomeruli, using both anatomical criteria and the pattern of innervation by subsets of its input neurons (projection neurons), molecularly identified by GAL4 markers. Thus, we show that projection neurons innervate calyx glomeruli in a stereotypic manner. By contrast, subsets of mushroom body neurons (Kenyon cells) that are labeled by GAL4 markers show no clear preference for specific glomeruli. Clonal subsets of Kenyon cells show some preference for subregions of the calyx, implying that they receive distinct input. However, at the level of individual glomeruli, dendritic terminals of larval-born Kenyon cells innervate about six glomeruli, apparently randomly. These results are consistent with a model in which Kenyon cells process olfactory information by integrating different inputs from several calyx glomeruli in a combinatorial manner.