A striking commonality across insects and vertebrates is the recurring presence of parallel olfactory subsystems, suggesting that such an organization has a highly adaptive value. Conceptually, two different categories of parallel systems must be distinguished. In one, specific sensory organs or processing streams analyze different chemical stimuli (segregate parallel systems). In the other, similar odor stimuli are processed but analyzed with respect to different features (dual parallel systems). Insects offer many examples for both categories. For example, segregate parallel systems for different chemical stimuli are realized in specialized neuronal streams for processing sex pheromones and CO₂. Dual parallel streams related to similar or overlapping odor stimuli are prominent in Hymenoptera. Here, a clear separation of sensory tracts to higher-order brain centers is present despite no apparent differences regarding the classes or categories of olfactory stimuli being processed. In this paper, we review the situation across insect species and offer hypotheses for the function and evolution of parallel olfactory systems.

The primary olfactory brain center, the antennal lobe (AL) in insects or the olfactory bulb in vertebrates, is a notable example of a neural network for sensory processing. While physiological properties of the input, the olfactory receptor neurons, have become clearer, the operation of the network itself remains cryptic. Therefore we measured spatio-temporal odor-response patterns in the output neurons of the olfactory glomeruli using optical imaging in the honeybee Apis mellifera. We mapped these responses to identified glomeruli, which are the structural and functional units of the AL. Each odor evoked a complex spatio-temporal activity pattern of excited and inhibited glomeruli. These properties were odor- and glomerulus-specific and were conserved across individuals. We compared the spatial pattern of excited glomeruli to previously published signals, which derived mainly from the receptor neurons, and found that they appeared more confined, showing that inhibitory connections enhance the contrast between glomeruli in the AL. To investigate the underlying mechanisms, we applied GABA and the GABA-receptor antagonist picrotoxin (PTX). The results show the presence of two separate inhibitory networks: one is GABAergic and modulates overall AL activity, the other is PTX-insensitive and glomerulus-specific. Inhibitory connections of the latter network selectively inhibit glomeruli with overlapping response profiles, in a way akin to “lateral” inhibition in other sensory systems. Selectively inhibited glomeruli need not be spatial neighbors. The net result is a globally modulated, contrast-enhanced and predictable representation of odors in the olfactory output neurons.

Odors elicit complex patterns of activated olfactory sensory neurons. Knowing the complete olfactome, i.e. the responses in all sensory neurons for all relevant odorants, is desirable to understand olfactory coding. The DoOR project combines all available Drosophila odorant response data into a single consensus response matrix. Since its first release many studies were published: receptors were deorphanized and several response profiles were expanded. In this study, we add unpublished data to the odor-response profiles for four odorant receptors (Or10a, Or42b, Or47b, Or56a). We deorphanize Or69a, showing a broad response spectrum with the best ligands including 3-hydroxyhexanoate, alpha-terpineol, 3-octanol and linalool. We include all of these datasets into DoOR, provide a comprehensive update of both code and data, and new tools for data analyses and visualizations. The DoOR project has a web interface for quick queries (http://neuro.uni.kn/DoOR), and a downloadable, open source toolbox written in R, including all processed and original datasets. DoOR now gives reliable odorant-responses for nearly all Drosophila olfactory responding units, listing 693 odorants, for a total of 7381 data points.