Letter | Published:

Circadian clock neurons constantly monitor environmental temperature to set sleep timing

Nature volume 555, pages 98102 (01 March 2018) | Download Citation

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Abstract

Circadian clocks coordinate behaviour, physiology and metabolism with Earth’s diurnal cycle1,2. These clocks entrain to both light and temperature cycles3, and daily environmental temperature oscillations probably contribute to human sleep patterns4. However, the neural mechanisms through which circadian clocks monitor environmental temperature and modulate behaviour remain poorly understood. Here we elucidate how the circadian clock neuron network of Drosophila melanogaster processes changes in environmental temperature. In vivo calcium-imaging techniques demonstrate that the posterior dorsal neurons 1 (DN1ps), which are a discrete subset of sleep-promoting clock neurons5, constantly monitor modest changes in environmental temperature. We find that these neurons are acutely inhibited by heating and excited by cooling; this is an unexpected result when considering the strong correlation between temperature and light, and the fact that light excites clock neurons6. We demonstrate that the DN1ps rely on peripheral thermoreceptors located in the chordotonal organs7,8 and the aristae9. We also show that the DN1ps and their thermosensory inputs are required for the normal timing of sleep in the presence of naturalistic temperature cycles. These results identify the DN1ps as a major gateway for temperature sensation into the circadian neural network, which continuously integrates temperature changes to coordinate the timing of sleep and activity.

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Change history

  • 28 February 2018

    Source Data for Extended Data Fig. 7 was added.

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Acknowledgements

This work was supported by a Damon Runyon Cancer Foundation postdoctoral fellowship (DR2231-15) to S.Y., a National Science Foundation (NSF) CBET grant (1509691) to P.R. and E.M., a University of Michigan M-cubed grant to E.M., P.R. and O.T.S., and a National Institutes of Health NINDS grant (R01NS077933) and an NSF IOS grant (1354046) to O.T.S. We thank N. Glossop, P. Hardin, M. Rosbash and R. Stanewsky for fly stocks. We also thank M. Rosbash, L. Griffith and P. Garrity for discussions about our work and M. de la Paz Fernández for reading the manuscript.

Author information

Author notes

    • Andrew Bahle

    Present address: Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.

    • Swathi Yadlapalli
    •  & Chang Jiang

    These authors contributed equally to this work.

Affiliations

  1. Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48109, USA

    • Swathi Yadlapalli
    • , Andrew Bahle
    •  & Orie T. Shafer
  2. Department of Mechanical Engineering, University of Michigan, Ann Arbor, Michigan 48109, USA

    • Chang Jiang
    • , Pramod Reddy
    •  & Edgar Meyhofer

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Contributions

The work was conceived by S.Y. and O.T.S. The calcium-imaging and behavioural experiments were performed by S.Y. and C.J., under the supervision of O.T.S. C.J. and S.Y. designed and built the Peltier and CaMPARI setups under the guidance of P.R. and E.M. S.Y., C.J. and A.B. conducted CaMPARI experiments. Data analysis was performed by S.Y. and C.J. The manuscript was written by S.Y., C.J. and O.T.S. with input from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Orie T. Shafer.

Reviewer Information Nature thanks P. Emery, R. Stanewsky and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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DOI

https://doi.org/10.1038/nature25740

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