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Dopamine neurons modulate pheromone responses in Drosophila courtship learning

Abstract

Learning through trial-and-error interactions allows animals to adapt innate behavioural ‘rules of thumb’ to the local environment, improving their prospects for survival and reproduction. Naive Drosophila melanogaster males, for example, court both virgin and mated females, but learn through experience to selectively suppress futile courtship towards females that have already mated1. Here we show that courtship learning reflects an enhanced response to the male pheromone cis-vaccenyl acetate (cVA), which is deposited on females during mating and thus distinguishes mated females from virgins. Dissociation experiments suggest a simple learning rule in which unsuccessful courtship enhances sensitivity to cVA. The learning experience can be mimicked by artificial activation of dopaminergic neurons, and we identify a specific class of dopaminergic neuron that is critical for courtship learning. These neurons provide input to the mushroom body (MB) γ lobe, and the DopR1 dopamine receptor is required in MBγ neurons for both natural and artificial courtship learning. Our work thus reveals critical behavioural, cellular and molecular components of the learning rule by which Drosophila adjusts its innate mating strategy according to experience.

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Figure 1: Experience enhances the behavioural response to cVA.
Figure 2: Activation of dopaminergic neurons is necessary and sufficient for learning.
Figure 3: Courtship learning requires synaptic transmission of aSP13 neurons.
Figure 4: DopR1 functions in MBγ neurons.

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Acknowledgements

We thank E. Leitner for performing the gas chromatography–mass spectrometry analysis; P. Garrity, U. Heberlein, M. Heisenberg, E. Kubli, S. Waddell, the Drosophila Genetic Resource Centre, the Bloomington Stock Center and the VDRC for fly stocks; K. Jandrasits and Z. Portik-Dobos for technical assistance; M. Zimmer for critical comments on the manuscript. Basic research at the Institute of Molecular Pathology is funded in part by Boehringer Ingelheim GmbH. This work was additionally supported by grants from the European Research Council (B.J.D.) and the Austrian Science Fund (K.K.). E.V. was supported by a European Molecular Biology Organization long-term postdoctoral fellowship.

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Contributions

K.K. and B.J.D. designed the experiments and performed the data analysis. K.K. performed most behavioural experiments. B.J.D. wrote the manuscript together with K.K. E.V. generated the DopR1 and DopR2 mutants, and A.K. generated the Or47b and Gr68a mutants. S.K. and J.Y.Y. performed the antibody stainings.

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Correspondence to Krystyna Keleman or Barry J. Dickson.

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The authors declare no competing financial interests.

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Keleman, K., Vrontou, E., Krüttner, S. et al. Dopamine neurons modulate pheromone responses in Drosophila courtship learning. Nature 489, 145–149 (2012). https://doi.org/10.1038/nature11345

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