The banana code—natural blend processing in the olfactory circuitry of Drosophila melanogaster

Marco Schubert,Silke Sachse,Bill S Hansson

doi:10.3389/fphys.2014.00059

Marco Schubert, Silke Sachse + Show 1 more

Open Access

https://doi.org/10.3389/fphys.2014.00059

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Abstract

Odor information is predominantly perceived as complex odor blends. For Drosophila melanogaster one of the most attractive blends is emitted by an over-ripe banana. To analyze how the fly's olfactory system processes natural blends we combined the experimental advantages of gas chromatography and functional imaging (GC-I). In this way, natural banana compounds were presented successively to the fly antenna in close to natural occurring concentrations. This technique allowed us to identify the active odor components, use these compounds as stimuli and measure odor-induced Ca2+ signals in input and output neurons of the Drosophila antennal lobe (AL), the first olfactory neuropil. We demonstrate that mixture interactions of a natural blend are very rare and occur only at the AL output level resulting in a surprisingly linear blend representation. However, the information regarding single components is strongly modulated by the olfactory circuitry within the AL leading to a higher similarity between the representation of individual components and the banana blend. This observed modulation might tune the olfactory system in a way to distinctively categorize odor components and improve the detection of suitable food sources. Functional GC-I thus enables analysis of virtually any unknown natural odorant blend and its components in their relative occurring concentrations and allows characterization of neuronal responses of complete neural assemblies. This technique can be seen as a valuable complementary method to classical GC/electrophysiology techniques, and will be a highly useful tool in future investigations of insect-insect and insect-plant chemical interactions.

Highlights

The natural environment displays a myriad of vital cues coded in complex odor blends, which often are composed of a large number of single odor components
A question of general importance arises: Does the olfactory system process and encode simultaneously occurring components as blend-specific information? And does this representation evolve over the different levels of olfactory processing? We addressed these questions by analyzing physiological responses to a natural odor blend and its single odor components in the antennal lobe (AL) of the vinegar fly Drosophila melanogaster
By combining the experimental advantages of gas chromatography and Ca2+ imaging, we measured the representation of single banana compounds and the complete banana blend at different levels of olfactory processing in the Drosophila olfactory system

Summary

Introduction

The natural environment displays a myriad of vital cues coded in complex odor blends, which often are composed of a large number of single odor components. Information processing of simultaneous input regarding several different odor compounds forming a specific and behaviorally relevant representation is so far poorly understood. A question of general importance arises: Does the olfactory system process and encode simultaneously occurring components as blend-specific information? We addressed these questions by analyzing physiological responses to a natural odor blend and its single odor components in the antennal lobe (AL) of the vinegar fly Drosophila melanogaster. Each group of OSNs, carrying the same type of OR, converge onto one or a few specific olfactory glomeruli (Gao et al, 2000; Vosshall et al, 2000; Couto et al, 2005; Fishilevich and Vosshall, 2005; Silbering et al, 2011). Since each OSN type targets its own specific glomerulus, the detection of odor molecules leads to a specific mosaic of glomerular activity patterns (Fiala et al, 2002; Ng et al, 2002; Wang et al, 2003; Silbering et al, 2008)

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