Good and bad odors –correlates of valence in the Drosophila olfactory system - Bill Hanson

How are attractive and repellent odors coded in the Drosophila peripheral and central nervous system? Does e.g. the glomerular topography of the insect antennal lobe have any significance? We know that male insects optimized to detect conspecific intersexual pheromones have a specific part of the antenna and the lobe devoted to this task, but we know very little regarding the importance of specific sensory neurons and antennal lobe regions beyond this. Besides sex attractants, brains have to decide whether and how to respond to detected stimuli based on, often, complex sensory input. The vinegar fly Drosophila melanogaster evaluates potential food sources largely based on olfactory cues. We performed a comprehensive behavioral screen using Drosophila and established the innate valence of 110 odors. By observing neuronal activation patterns evoked by behaviorally positive and negative odors from the antenna to the antennal lobe, we could identify aversive-specific projection neuron activation patterns in the glomerular array of the lobe (Knaden et al., 2012). The representation of odor valence is thus formed already at the output level of the antennal lobe. Secondly, we studied coding of one specific odor, geosmin, emitted by harmful microbes. By using a large array of methods, including a novel paradigm to test for behavioral responses, we could show that a single neural line from the periphery and past the antennal lobe delivers the message regarding the presence of geosmin. Activation of this line is necessary and sufficient for a very strong aversive behavior to be elicited by geosmin (Stensmyr et al., 2012). Thirdly, by using two-photon imaging we observed calcium dynamics in the lateral horn of the fly brain. This is a target of output neurons of the antennal lobe. In the lateral horn we found a very clear distinction between attractive and repellent odors, and could by genetic manipulations change the perceived valence of odors.

In all we studied how odors involved in food attraction – and avoidance – are coded in the Drosophila peripheral and central nervous system. The results have an important bearing on our understanding of food choice in these insects.

These studies were financed by the Max Planck Society.

Knaden M, Strutz A, Ahsan J, Sachse S, Hansson BS (2012) Spatial representation of odorant valence in an insect brain. Cell Reports 1:392-399

Stensmyr MC, Dweck HKM, Farhan A, Ibba I, Strutz A, Mukunda L, Linz J, Grabe V, Steck K, Lavista-Llanos S, Wicher D, Sachse S, Knaden M, Becher PG, Seki Y, Hansson BS (2012) A conserved dedicated olfactory circuit for detecting harmful molds in Drosophila. Cell 151:1345-1357