The Drosophila pheromone cVA activates a sexually dimorphic neural circuit (original) (raw)

Nature volume 452, pages 473–477 (2008)Cite this article

Abstract

Courtship is an innate sexually dimorphic behaviour that can be observed in naive animals without previous learning or experience, suggesting that the neural circuits that mediate this behaviour are developmentally programmed1. In Drosophila, courtship involves a complex yet stereotyped array of dimorphic behaviours that are regulated by FruM, a male-specific isoform of the fruitless gene2,3,4,5. FruM is expressed in about 2,000 neurons in the fly brain, including three subpopulations of olfactory sensory neurons and projection neurons (PNs). One set of Fru+ olfactory neurons expresses the odorant receptor Or67d and responds to the male-specific pheromone _cis_-vaccenyl acetate (cVA)6,7,8,9,10. These neurons converge on the DA1 glomerulus in the antennal lobe. In males, activation of Or67d+ neurons by cVA inhibits courtship of other males, whereas in females their activation promotes receptivity to other males7. These observations pose the question of how a single pheromone acting through the same set of sensory neurons can elicit different behaviours in male and female flies. Anatomical or functional dimorphisms in this neural circuit might be responsible for the dimorphic behaviour. We therefore developed a neural tracing procedure that employs two-photon laser scanning microscopy to activate the photoactivatable green fluorescent protein11. Here we show, using this technique, that the projections from the DA1 glomerulus to the protocerebrum are sexually dimorphic. We observe a male-specific axonal arbor in the lateral horn whose elaboration requires the expression of the transcription factor FruM in DA1 projection neurons and other Fru+ cells. The observation that cVA activates a sexually dimorphic circuit in the protocerebrum suggests a mechanism by which a single pheromone can elicit different behaviours in males and in females.

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Acknowledgements

We thank G. Struhl, L. Vosshall, B. Sabatini, B. Bloodgood and members of the Axel laboratory for discussions about the experiments in this manuscript; J. Meier for technical assistance; J. Rafter for assistance in measuring the microscope point-spread function; A. Gerber for assistance with warping techniques; and P. J. Kisloff for assistance in the preparation of this manuscript. Financial support was provided by the Helen Hay Whitney Foundation (S.R.D., V.R.) and the Howard Hughes Medical Institute, the Mathers Foundation and the Gates Foundation (R.A.).

Author information

Author notes

  1. Sandeep Robert Datta and Maria Luisa Vasconcelos: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biophysics and Howard Hughes Medical Institute, College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA,
    Sandeep Robert Datta, Maria Luisa Vasconcelos, Vanessa Ruta, Sean Luo, Allan Wong, Jorge Flores, Karen Balonze & Richard Axel
  2. Division of Biology 216-76 and Howard Hughes Medical Institute, California Institute of Technology, Pasadena, California 91125, USA,
    Allan Wong
  3. Research Institute of Molecular Pathology (IMP), Dr Bohr-gasse 7, A-1030 Vienna, Austria,
    Ebru Demir & Barry J. Dickson

Authors

  1. Sandeep Robert Datta
  2. Maria Luisa Vasconcelos
  3. Vanessa Ruta
  4. Sean Luo
  5. Allan Wong
  6. Ebru Demir
  7. Jorge Flores
  8. Karen Balonze
  9. Barry J. Dickson
  10. Richard Axel

Corresponding author

Correspondence toRichard Axel.

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Supplementary Information

The file contains Supplementary Figures 1-5 with Legends and Supplementary Methods with additional references. (PDF 734 kb)

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Datta, S., Vasconcelos, M., Ruta, V. et al. The Drosophila pheromone cVA activates a sexually dimorphic neural circuit.Nature 452, 473–477 (2008). https://doi.org/10.1038/nature06808

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Editorial Summary

Scent's different directions

Despite dramatic behavioural differences between the sexes, surprisingly few anatomic features have been observed that differentiate the male and female brain in any species. Work in the Drosophila fruit fly has now uncovered a striking difference in male and female responses to the insect pheromone cVA (_cis_-vaccenyl acetate). Males release the pheromone, which is detected by both sexes via apparently identical neural circuits in their antennae. The scent induces females to become receptive to males, but in rival males it inhibits courtship behaviour. The single neuron tracing technique developed to make this discovery should be applicable to study the nervous systems of other genetically tractable species, such as the mouse.