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Circadian rhythms in olfactory responses of Drosophila melanogaster

Abstract

The core mechanism of circadian timekeeping in arthropods and vertebrates consists of feedback loops involving several clock genes, including period (per) and timeless (tim)1,2. In the fruitfly Drosophila, circadian oscillations in per expression occur in chemosensory cells of the antennae, even when the antennae are excised and maintained in isolated organ culture3. Here we demonstrate a robust circadian rhythm in Drosophila in electrophysiological responses to two classes of olfactory stimuli. These rhythms are observed in wild-type flies during light–dark cycles and in constant darkness, but are abolished in per or tim null-mutant flies (per01 and tim01) which lack rhythms in adult emergence and locomotor behaviour. Olfactory rhythms are also abolished in the per 7.2:2 transgenic line in which per expression is restricted to the lateral neurons of the optic lobe4. Because per 7.2:2 flies do not express per in peripheral oscillators, our results provide evidence that peripheral circadian oscillators are necessary for circadian rhythms in olfactory responses. As olfaction is essential for food acquisition, social interactions and predator avoidance in many animals, circadian regulation of olfactory systems could have profound effects on the behaviour of organisms that rely on this sensory modality.

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Figure 1: Characteristics of EAG responses to ethyl acetate in wild-type (Canton-S) female Drosophila melanogaster.
Figure 2: Olfactory responses at different times of day in different strains of D.melanogaster.
Figure 3: Mean olfactory responses at different times of day in Drosophila free-running in constant light (LL).
Figure 4: Olfactory responses in wild-type (squares) and per 7.2:2 transgenic Drosophila (diamonds) during day 2 of DD.

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Acknowledgements

This work was supported by grants from the NIH to S.E.D. and P.E.H. B.K. received support from the BRAIN program. We thank L.Dryer and N. Glossop for discussions and comments on the manuscript. S.E.D. and P.E.H. are NHTS.

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Correspondence to Stuart E. Dryer.

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Krishnan, B., Dryer, S. & Hardin, P. Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 400, 375–378 (1999). https://doi.org/10.1038/22566

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