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A dimorphic pheromone circuit in Drosophila from sensory input to descending output

Abstract

Drosophila show innate olfactory-driven behaviours that are observed in naive animals without previous learning or experience, suggesting that the neural circuits that mediate these behaviours are genetically programmed. Despite the numerical simplicity of the fly nervous system, features of the anatomical organization of the fly brain often confound the delineation of these circuits. Here we identify a neural circuit responsive to cVA, a pheromone that elicits sexually dimorphic behaviours1,2,3,4. We have combined neural tracing using an improved photoactivatable green fluorescent protein (PA-GFP) with electrophysiology, optical imaging and laser-mediated microlesioning to map this circuit from the activation of sensory neurons in the antennae to the excitation of descending neurons in the ventral nerve cord. This circuit is concise and minimally comprises four neurons, connected by three synapses. Three of these neurons are overtly dimorphic and identify a male-specific neuropil that integrates inputs from multiple sensory systems and sends outputs to the ventral nerve cord. This neural pathway suggests a means by which a single pheromone can elicit different behaviours in the two sexes.

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Figure 1: Photoactivation identifies dimorphic lateral horn neurons.
Figure 2: DC1 neurons synapse with DA1 PNs and are selectively tuned to cVA.
Figure 3: DC1 and descending neurons innervate Fru+ dimorphic neuropil.
Figure 4: DC1 neurons excite DN1, a cVA-responsive, male-specific descending neuron.

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Acknowledgements

We thank T. Jessell, C. Zuker and members of the Axel laboratory for discussion and comments on this manuscript; J. Flores for technical assistance; B. Dickson for reagents; P. Kisloff for assistance in the preparation of this manuscript; and M. Gutierrez and A. Nemes for general laboratory support. This work was funded in part by a grant from the Foundation for the National Institutes of Health through the Grand Challenges in Global Health Initiative. Further financial support was provided by the Helen Hay Whitney Foundation (V.R. and S.R.D.), the Burroughs Welcome Fund (S.R.D.) and the Howard Hughes Medical Institute (R.A. and L.L.L.).

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V.R., S.R.D., M.L.V. and R.A. conceived of the project and contributed to its progression. V.R. performed all the experiments, with the early participation of M.L.V. S.R.D. developed new photoactivatable fluorophores. L.L.L. developed GCaMP3. J.F. performed immunochemistry. R.A. provided guidance and wrote the paper with V.R., S.R.D., M.L.V. and L.L.L.

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Correspondence to Richard Axel.

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The authors declare no competing financial interests.

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Ruta, V., Datta, S., Vasconcelos, M. et al. A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468, 686–690 (2010). https://doi.org/10.1038/nature09554

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