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Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila

Nature Neuroscience volume 14, pages 896–902 (2011)Cite this article

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Abstract

When two socially naive Drosophila males meet, they will fight. However, prior social grouping of males reduces their aggression. We found olfactory communication to be important for modulating Drosophila aggression. Although acute exposure to the male-specific pheromone 11-cis-vaccenyl acetate (cVA) elicited aggression through Or67d olfactory receptor neurons (ORNs), chronic cVA exposure reduced aggression through Or65a ORNs. Or65a ORNs were not acutely involved in aggression, but blockade of synaptic transmission of Or65a ORNs during social grouping or prior chronic cVA exposure eliminated social modulation of aggression. Artificial activation of Or65a ORNs by ectopic expression of the Drosophila gene TrpA1 was sufficient to reduce aggression. Social suppression of aggression requires subsets of local interneurons in the antennal lobe. Our results indicate that activation of Or65a ORNs is important for social modulation of male aggression, demonstrate that the acute and chronic effects of a single pheromone are mediated by two distinct types of ORNs, reveal a behaviorally important role for interneurons and suggest a chemical method to reduce aggression in animals.

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Figure 1: Social regulation of aggression mimicked by male odor or cVA.
Figure 2: Electrophysiological responses to cVA in isolated, grouped and cVA-primed flies.
Figure 3: Aggression-suppressing effect of chronic cVA exposure mediated by Or65a ORNs.
Figure 4: Aggression-suppressing effect of chronic male exposure mediated by Or65a ORNs.
Figure 5: Or65a ORNs not required for aggression per se.
Figure 6: Aggression suppressed by chronic activation of Or65a ORNs.
Figure 7: Local circuit plasticity in antennal lobe required for social modulation of aggression.

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Acknowledgements

We are grateful to B. Dickson (Research Institute of Molecular Pathology), P. Garrity (Brandeis University), T. Lee (Janelia Farm Research Campus), L. Luo (Stanford University), P. Shen (University of Georgia) and L. Vosshall (Rockefeller University) for providing stocks, W. Guo, C. Zhou and other members of the Rao laboratory for helpful discussions and technical assistance, and J. Tan and M. Luo for help with electrophysiology. This work was supported by the Ministry of Science and Technology (973 program No.2010CB833900).

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Author notes

  1. Weiwei Liu and Xinhua Liang: These authors contributed equally to this work.

Authors and Affiliations

  1. Institute of Neuroscience, Shanghai Institutes of Biological Sciences and Graduate School of the Chinese Academy of Sciences, Shanghai, China

    Xinhua Liang

  2. Beijing Normal University College of Life Sciences, Beijing, China

    Weiwei Liu

  3. National Institute of Biological Sciences, Beijing, China

    Weiwei Liu, Xinhua Liang & Yi Rao

  4. Peking University School of Chemistry and Molecular Engineering, Beijing, China

    Jianxian Gong & Zhen Yang

  5. State Key Laboratory of Integrated Management of Pest Insects and Rodents in Agriculture, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

    Yao-Hua Zhang & Jian-Xu Zhang

  6. Peking University School of Life Sciences State Key Laboratory of Membrane Biology, Beijing, China

    Yi Rao

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Contributions

Y.R. conceived the project. Y.R., W.L. and X.L. designed the experiments. W.L. and X.L. performed the experiments. J.G. and Z.Y. synthesized cVA. Y.-H.Z. and J.-X.Z. performed the experiments shown in Supplementary Figure 1. W.L., X.L. and Y.R. wrote the paper.

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Correspondence to Yi Rao.

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Liu, W., Liang, X., Gong, J. et al. Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat Neurosci 14, 896–902 (2011). https://doi.org/10.1038/nn.2836

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