The odour of acids has a distinct quality that is perceived as sharp, pungent and often irritating1. How acidity is sensed and translated into an appropriate behavioural response is poorly understood. Here we describe a functionally segregated population of olfactory sensory neurons in the fruitfly, Drosophila melanogaster, that are highly selective for acidity. These olfactory sensory neurons express IR64a, a member of the recently identified ionotropic receptor (IR) family of putative olfactory receptors2. In vivo calcium imaging showed that IR64a+ neurons projecting to the DC4 glomerulus in the antennal lobe are specifically activated by acids. Flies in which the function of IR64a+ neurons or the IR64a gene is disrupted had defects in acid-evoked physiological and behavioural responses, but their responses to non-acidic odorants remained unaffected. Furthermore, artificial stimulation of IR64a+ neurons elicited avoidance responses. Taken together, these results identify cellular and molecular substrates for acid detection in the Drosophila olfactory system and support a labelled-line mode of acidity coding at the periphery.
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We thank M. Dus for helpful discussions and technical support for making anti-IR64a antibody; M. Kim for technical assistance; J. Treisman, N. Ringstad, C. Desplan, M. Warman, G. Fishell, M. Chesler, A. Wong, L. Vosshall and D. Anderson for discussions and comments on the manuscript; and R. Lehmann for sharing her two-photon microscope. This work was initiated in D. Anderson’s laboratory at California Institute of Technology. G.S.B.S. thanks H.-R. Song for support. Financial support was provided by a National Research Service Award fellowship (M.A.), the Boehringer Ingelheim Foundation (R. Bell), the Centre National de la Recherche Scientifique (Y.G.), a European Research Council Starting Independent Researcher Grant (R. Benton), the Swiss National Science Foundation (R. Benton), the Alfred P. Sloan Foundation (G.S.), the Whitehall Foundation (G.S.), a Whitehead President Award (G.S.) and NIH grant 1RO1GM089746 (G.S).
The authors declare no competing financial interests.
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Ai, M., Min, S., Grosjean, Y. et al. Acid sensing by the Drosophila olfactory system. Nature 468, 691–695 (2010) doi:10.1038/nature09537
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