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
2. Division of Biology 216-76 and Howard Hughes Medical Institute, California Institute of Technology, Pasadena, California 91125, USA
3. Research Institute of Molecular Pathology (IMP), Dr Bohr-gasse 7, A-1030 Vienna, Austria
4. These authors contributed equally to this work.

Correspondence to: Richard Axel¹ Correspondence and requests for materials should be addressed to R.A. (Email: ra27@columbia.edu).

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 Fru^M, a male-specific isoform of the fruitless gene^{2, 3, 4, 5}. Fru^M 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 Fru^M 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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