An olfactogenetic approach identifies olfactory neurons and brain centers directing negative oviposition decisions in Drosophila.

The sense of smell influences behaviors in animals, yet how odors are represented in the brain remains unclear. The nose contains different types of olfactory sensory neurons (OSNs), each expressing a particular odorant receptor, and OSNs expressing the same receptors converge their axons on a brain region called a glomerulus. In Drosophila , second order neurons (projection neurons) typically innervate a single glomerulus and send stereotyped axonal projections to the lateral horn. One of the greatest challenges to studying olfaction is the lack of methods allowing activation of specific types of olfactory neurons in an ethologically relevant setting. Most odorants activate many olfactory neurons, and many olfactory neurons are activated by a variety of odorants. As such, it is difficult to identify if individual types of olfactory neurons directly influence a behavior. To address this, we developed a genetic method in Drosophila called olfactogenetics in which a narrowly tuned odorant receptor, Or56a, is ectopically expressed in different olfactory neuron types. Stimulation with geosmin (the only known Or56a ligand), in an Or56a mutant background leads to specific activation of only the target olfactory neuron type. We used this approach to identify which types of olfactory neurons can directly guide oviposition decisions. We identified 5 OSN-types (Or71a, Or47b, Or49a, Or67b, and Or7a) that, when activated alone, suppress oviposition. Projection neurons partnering with these OSNs share a region of innervation in the lateral horn, suggesting that oviposition site-selection might be encoded in this brain region.