Select Drosophila glomeruli mediate innate olfactory attraction and aversion

Abstract

Fruitflies show robust attraction to food odours, which usually excite several glomeruli. To understand how the representation of such odours leads to behaviour, we used genetic tools to dissect the contribution of each activated glomerulus. Apple cider vinegar triggers robust innate attraction at a relatively low concentration, which activates six glomeruli. By silencing individual glomeruli, here we show that the absence of activity in two glomeruli, DM1 and VA2, markedly reduces attraction. Conversely, when each of these two glomeruli was selectively activated, flies showed as robust an attraction to vinegar as wild-type flies. Notably, a higher concentration of vinegar excites an additional glomerulus and is less attractive to flies. We show that activation of the extra glomerulus is necessary and sufficient to mediate the behavioural switch. Together, these results indicate that individual glomeruli, rather than the entire pattern of active glomeruli, mediate innate behavioural output.

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Figure 1: Flies are robustly attracted to apple cider vinegar, which excites six glomeruli.
Figure 2: Silencing DM1 or VA2 reduces attraction to 3 p.p.m. vinegar.
Figure 3: Restoring Or83b in DM1 and VA2 ORNs returns attraction to control levels.
Figure 4: Vinegar becomes less attractive and activates an additional glomerulus at high concentrations.
Figure 5: DM5 mediates the decrease in attraction in response to 32 p.p.m. vinegar.
Figure 6: DM1 and DM5 mediate attraction and aversion in response to ethyl butyrate.

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Acknowledgements

We would like to thank D. Anderson, R. Axel, C. Zuker and M. Gallio for comments on the manuscript. We thank M. Hilker for help with the design of the four-field olfactometer. We thank C. Root for generating the data presented in Supplementary Fig. 4. We thank L. Vosshall, B. Dickson and T. Lee for providing fly stocks. This work was partially supported by a research grant from the Whitehall Foundation to J.W.W. and a grant from the National Institute of Deafness and other Communication Disorders to J.W.W. (R01DC009597). J.W.W. is a Beckman Young Investigator, a Hellman Faculty scholar, and a Searle scholar.

Author Contributions J.L.S. and J.W.W. designed experiments, analysed the data, and wrote the manuscript. J.L.S. carried out the experiments.

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Correspondence to Jing W. Wang.

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Semmelhack, J., Wang, J. Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459, 218–223 (2009). https://doi.org/10.1038/nature07983

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