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A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila

Abstract

All animals exhibit innate behaviours in response to specific sensory stimuli that are likely to result from the activation of developmentally programmed neural circuits. Here we observe that Drosophila exhibit robust avoidance to odours released by stressed flies. Gas chromatography and mass spectrometry identifies one component of this ‘Drosophila stress odorant (dSO)’ as CO2. CO2 elicits avoidance behaviour, at levels as low as 0.1%. We used two-photon imaging with the Ca2+-sensitive fluorescent protein G-CaMP to map the primary sensory neurons governing avoidance to CO2. CO2 activates only a single glomerulus in the antennal lobe, the V glomerulus; moreover, this glomerulus is not activated by any of 26 other odorants tested. Inhibition of synaptic transmission in sensory neurons that innervate the V glomerulus, using a temperature-sensitive Shibire gene (Shits)1, blocks the avoidance response to CO2. Inhibition of synaptic release in the vast majority of other olfactory receptor neurons has no effect on this behaviour. These data demonstrate that the activation of a single population of sensory neurons innervating one glomerulus is responsible for an innate avoidance behaviour in Drosophila.

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Figure 1: Drosophila exhibits innate avoidance of odorants released by stressed flies.
Figure 2: CO2 is a component of dSO.
Figure 3: CO2 avoidance is mediated by ORNs that project to the V glomerulus.
Figure 4: A dSO-unresponsive enhancer trap line is also defective in its CO2 response.

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Acknowledgements

We thank J.-S. Chang for technical assistance, L. Vosshall for providing Or83b-Gal4 and Or47b-Gal4 flies and for other unpublished information, D. Armstrong for Gal4 enhancer trap lines 103Y, 253Y, c747 and c761, T. Kitamoto for UAS-Shits flies, U. Heberlein for the HU protocol and R. I. Wilson for discussion of unpublished data and comments on the manuscript. G.S.B.S. is a recipient of a National Research Service Award. A.C.H. is supported by a Howard Hughes Predoctoral fellowship. This work was supported by the HHMI (R.A. and D.J.A.) and by the NSF (S.B.). R.A. and D.J.A. are Investigators of the Howard Hughes Medical Institute.Author contributions S.B., R.A. and D.J.A. made equally minimal contributions to this work.

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Correspondence to David J. Anderson.

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Supplementary Figure S1

Dose-response curve for avoidance response to CO2 (a) and dose-response curve for activation of GR21A+ neurons to CO2 (b). (DOC 197 kb)

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Suh, G., Wong, A., Hergarden, A. et al. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431, 854–859 (2004). https://doi.org/10.1038/nature02980

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