Letters to Nature

Nature 431, 854-859 (14 October 2004) | doi:10.1038/nature02980; Received 13 July 2004; Accepted 1 September 2004; Published online 15 September 2004

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

Greg S. B. Suh1,2, Allan M. Wong1,3, Anne C. Hergarden1,2, Jing W. Wang1,3, Anne F. Simon2,4, Seymour Benzer2, Richard Axel1,3 & David J. Anderson1,2

  1. Howard Hughes Medical Institute, California Institute of Technology, Pasadena, California 91125, USA
  2. Division of Biology 216-76 and 156-29, California Institute of Technology, Pasadena, California 91125, USA
  3. Columbia University College of Physicians and Surgeons 701 West 168th Street, New York 10032, USA
  4. Present address: Brain Research Institute University of California, Los Angeles, California, USA

Correspondence to: David J. Anderson1,2 Email: wuwei@caltech.edu

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 (Shi ts)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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