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Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain

Nature volume 431, pages 869–873 (2004)Cite this article

Abstract

In Drosophila, a ‘clock’ situated in the brain controls circadian rhythms of locomotor activity. This clock relies on several groups of neurons that express the Period (PER) protein, including the ventral lateral neurons (LNvs), which express the Pigment-dispersing factor (PDF) neuropeptide, and the PDF-negative dorsal lateral neurons (LNds)1. In normal cycles of day and night, adult flies exhibit morning and evening peaks of activity1,2; however, the contribution of the different clock neurons to the rest–activity pattern remains unknown. Here, we have used targeted expression of PER to restore the clock function of specific subsets of lateral neurons in arrhythmic per0 mutant flies. We show that PER expression restricted to the LNvs only restores the morning activity, whereas expression of PER in both the LNvs and LNds also restores the evening activity. This provides the first neuronal bases for ‘morning’ and ‘evening’ oscillators in the Drosophila brain. Furthermore, we show that the LNvs alone can generate 24 h activity rhythms in constant darkness, indicating that the morning oscillator is sufficient to drive the circadian system.

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Figure 1: Locomotor activity in light/dark cycles.
Figure 2: PER immunoreactivity of lateral neurons in light/dark cycles.
Figure 3: PER immunoreactivity of lateral neurons in constant darkness.
Figure 4: Locomotor activity in constant darkness.

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Acknowledgements

This work was supported by ACI ‘Biologie du développement et physiologie intégrative’ from the Ministère de la Recherche. F.R. is supported by INSERM, and R.X. is supported by Fondation des Treilles and previously by CNRS and Fondation Electricité de France. We thank M. Boudinot for the continuously improving Faas software, L. Collet for artwork, A. Klarsfeld and A. Lamouroux for critical reading of the manuscript, and J. Champagnat for his support. We thank J. Hall, P. Taghert and T. Siegmund for providing pdf-Gal4, C929-Gal4 and Mai179-Gal4 lines, respectively, as well as R. Stanewsky for anti-PER serum. We are grateful to H. Otsuna and K. Ito for sharing unpublished observations with the Mz520-Gal4 line, and to M. Rosbash and colleagues for communicating their unpublished manuscript.

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  1. These authors contributed equally to this work

Authors and Affiliations

  1. Institut de Neurobiologie Alfred Fessard (NGI, CNRS UPR 2216), Centre National de la Recherche Scientifique, av. de la terrasse, 91198, Gif-sur-Yvette, France

    Brigitte Grima, Elisabeth Chélot, Ruohan Xia & François Rouyer

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  1. Brigitte Grima
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  2. Elisabeth Chélot
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Correspondence to François Rouyer.

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Supplementary information

Supplementary Table 1

Gal4-driven Per expression in the lateral neurons in LD conditions. (DOC 28 kb)

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Grima, B., Chélot, E., Xia, R. et al. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431, 869–873 (2004). https://doi.org/10.1038/nature02935

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