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Coupled oscillators control morning and evening locomotor behaviour of Drosophila

Nature volume 431, pages 862–868 (2004)Cite this article

Abstract

Daily rhythms of physiology and behaviour are precisely timed by an endogenous circadian clock1,2. These include separate bouts of morning and evening activity, characteristic of Drosophila melanogaster and many other taxa, including mammals3,4,5. Whereas multiple oscillators have long been proposed to orchestrate such complex behavioural programmes6, their nature and interplay have remained elusive. By using cell-specific ablation, we show that the timing of morning and evening activity in Drosophila derives from two distinct groups of circadian neurons: morning activity from the ventral lateral neurons that express the neuropeptide PDF, and evening activity from another group of cells, including the dorsal lateral neurons. Although the two oscillators can function autonomously, cell-specific rescue experiments with circadian clock mutants indicate that they are functionally coupled.

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Figure 1: Suppression of GAL4 activity with GAL80 in Drosophila circadian neurons, as examined with a UAS-ANFGFP reporter.
Figure 2: Genetic ablation of different groups of circadian neurons causes the loss of different locomotor activity components.
Figure 3: Targeted genetic ablation removes specific circadian neurons.
Figure 4: Functional disruption of the two oscillators.
Figure 5: Coupling of the two Drosophila oscillators CRY+PDF- and PDF+ underlies the coordination of the two daily activity peaks.

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Acknowledgements

We thank A. Sehgal for providing the UAS-per2-4 flies and L. Luo for tubulinP-GAL80 plasmid, as well as J. Levine, R. Allada, L. Griffith, P. Emery and M.R. laboratory members for discussion and critical comments on the manuscript. We are grateful to J. Hall, P. Nawathean and M. McDonald for their support and advice. We also thank E. Dougherty for assistance in confocal microscopy, and H. Felton for administrative assistance. The work was supported in part by grants from the NIH to M.R.

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Author notes

  1. Dan Stoleru and Ying Peng: These authors contributed equally to this work

Authors and Affiliations

  1. Howard Hughes Medical Institute and National Center for Behavioural Genomics, Department of Biology, Brandeis University, Waltham, Massachusetts, 02454, USA

    Dan Stoleru, Ying Peng, José Agosto & Michael Rosbash

Authors
  1. Dan Stoleru
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  2. Ying Peng
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  4. Michael Rosbash
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Correspondence to Michael Rosbash.

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Supplementary information

Supplementary Table S1

Quantitative description of GFP-expressing clock neurons with different combinations of circadian drivers. (DOC 36 kb)

Supplementary Table S2

Rescue of Pdf-GAL4/UAS-hid behavioral phenotype by Pdf-GAL80. (DOC 35 kb)

Supplementary Table S3

Rescue of cry-GAL4/UAS-hid behavioral phenotype by cry-GAL80. (DOC 46 kb)

Supplementary Table S4

Characterization of circadian locomotor behavior with selective oscillator ablation. (DOC 28 kb)

Supplementary Table S5

Circadian locomotor behavior with disabled oscillators. (DOC 27 kb)

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Stoleru, D., Peng, Y., Agosto, J. et al. Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431, 862–868 (2004). https://doi.org/10.1038/nature02926

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