Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants

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Abstract

The fruitfly Drosophila melanogaster exhibits a robust and innate olfactory-based avoidance behaviour to CO2, a component of odour emitted from stressed flies1. Specialized neurons in the antenna and a dedicated neuronal circuit in the higher olfactory system mediate CO2 detection and avoidance1,2. However, fruitflies need to overcome this avoidance response in some environments that contain CO2 such as ripening fruits and fermenting yeast, which are essential food sources. Very little is known about the molecular and neuronal basis of this unique, context-dependent modification of innate olfactory avoidance behaviour. Here we identify a new class of odorants present in food that directly inhibit CO2-sensitive neurons in the antenna. Using an in vivo expression system we establish that the odorants act on the Gr21a/Gr63a CO2 receptor3. The presence of these odorants significantly and specifically reduces CO2-mediated avoidance behaviour, as well as avoidance mediated by ‘Drosophila stress odour’. We propose a model in which behavioural avoidance to CO2 is directly influenced by inhibitory interactions of the novel odours with CO2 receptors. Furthermore, we observe differences in the temporal dynamics of inhibition: the effect of one of these odorants lasts several minutes beyond the initial exposure. Notably, animals that have been briefly pre-exposed to this odorant do not respond to the CO2 avoidance cue even after the odorant is no longer present. We also show that related odorants are effective inhibitors of the CO2 response in Culex mosquitoes that transmit West Nile fever and filariasis. Our findings have broader implications in highlighting the important role of inhibitory odorants in olfactory coding, and in their potential to disrupt CO2-mediated host-seeking behaviour in disease-carrying insects like mosquitoes.

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Figure 1: Inhibitory odours dramatically reduce response to CO2.
Figure 2: Inhibitory odorants directly affect CO 2 response of Gr21a/Gr63a in a heterologous system.
Figure 3: Avoidance behaviour to CO 2 and Drosophila stress odour is abolished by inhibitory odorants.
Figure 4: Inhibitory odours dramatically reduce CO 2 response in Culex quinquefasciatus mosquitoes.

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Acknowledgements

We thank W. van der Goes van Naters for help with setting up our electrophysiology rig, P. Atkinson and A. Kahlon for providing mosquitoes, J. Millar for providing reagents, and A. Dahanukar for commenting on the manuscript.

Author Contributions S.L.T. planned and performed the experiments and co-wrote the manuscript. A.R. planned the experiments, supervised the project and co-wrote the manuscript.

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Correspondence to Anandasankar Ray.

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Turner, S., Ray, A. Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants. Nature 461, 277–281 (2009) doi:10.1038/nature08295

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