A Mechanosensory Pathway to the Drosophila Circadian Clock
Coordinating the Clock
In flies, the mechanosensory chordotonal organs help to coordinate the effects of temperature on circadian cycles. Simoni et al. (p. 525) provide a mechanism by which mechanosensory input is processed to help to synchronize the biological clock in Drosophila melanogaster. The chordotonal organs, which have similarities to the mammalian ear, were also required for sensation of a vibration stimulus and its effects on the endogenous brain clock. The chordotonal organs, present in the joints of the limbs, provide neuronal signals that allow the animal to sense its position or posture—and thus might mediate feedback of a range of behaviors onto the endogenous biological clock.
Abstract
Circadian clocks attune the physiology of virtually all living organisms to the diurnal cycles of their environments. In metazoan animals, multiple sensory input pathways have been linked to clock synchronization with the environmental cycle (entrainment). Extrinsic entrainment cues include light and temperature. We show that (12-hour:12-hour) cycles of vibration and silence (VS) are sufficient to synchronize the daily locomotor activity of wild-type Drosophila melanogaster. Behavioral synchronization to VS cycles required a functional clock and functional chordotonal organs and was accompanied by phase-shifts of the daily oscillations of PERIOD protein concentrations in brain clock neurons. The feedback from mechanosensory—and particularly, proprioceptive—organs may help an animal to keep its circadian clock in sync with its own, stimulus-induced activities.
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Supplementary Material
Summary
Materials and Methods
Figs. S1 to S10
Table S1
Resources
File (simoni-sm.pdf)
References and Notes
1
Panda S., Hogenesch J. B., Kay S. A., Circadian rhythms from flies to human. Nature 417, 329–335 (2002).
2
Sehadova H., Glaser F. T., Gentile C., Simoni A., Giesecke A., Albert J. T., Stanewsky R., Temperature entrainment of Drosophila’s circadian clock involves the gene nocte and signaling from peripheral sensory tissues to the brain. Neuron 64, 251–266 (2009).
3
L. H. Field, T. Matheson, in Advances in Insect Physiology (Academic Press, San Diego, 1998), vol. 27, pp. 1–228.
4
Kernan M. J., Pflugers Archiv-European. Pflugers Arch. Eur. J. Physiol. 454, 703 (2007).
5
Glaser F. T., Stanewsky R., Synchronization of the Drosophila circadian clock by temperature cycles. Cold Spring Harb. Symp. Quant. Biol. 72, 233–242 (2007).
6
Hamblen-Coyle M. J., Wheeler D. A., Rutila J. E., Rosbash M., Hall J. C., Behavior of period-altered circadian rhythm mutants of Drosophila in light: Dark cycles (Diptera: Drosophilidae). J. Insect Behav. 5, 417–446 (1992).
7
Materials and methods are available as supplementary materials on Science Online.
8
Gentile C., Sehadova H., Simoni A., Chen C., Stanewsky R., Cryptochrome antagonizes synchronization of Drosophila’s circadian clock to temperature cycles. Curr. Biol. 23, 185–195 (2013).
9
Levine J. D., Funes P., Dowse H. B., Hall J. C., Advanced analysis of a cryptochrome mutation’s effects on the robustness and phase of molecular cycles in isolated peripheral tissues of Drosophila. BMC Neurosci. 3, 5 (2002).
10
Konopka R. J., Benzer S., Clock mutants of Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 68, 2112–2116 (1971).
11
Citri Y., Colot H. V., Jacquier A. C., Yu Q., Hall J. C., Baltimore D., Rosbash M., A family of unusually spliced biologically active transcripts encoded by a Drosophila clock gene. Nature 326, 42–47 (1987).
12
Zerr D. M., Hall J. C., Rosbash M., Siwicki K. K., Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J. Neurosci. 10, 2749–2762 (1990).
13
Kavlie R. G., Kernan M. J., Eberl D. F., Hearing in Drosophila requires TilB, a conserved protein associated with ciliary motility. Genetics 185, 177–188 (2010).
14
Glaser F. T., Stanewsky R., Temperature synchronization of the Drosophila circadian clock. Curr. Biol. 15, 1352–1363 (2005).
15
Veleri S., Brandes C., Helfrich-Förster C., Hall J. C., Stanewsky R., A self-sustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr. Biol. 13, 1758–1767 (2003).
16
Golombek D. A., Rosenstein R. E., Physiology of circadian entrainment. Physiol. Rev. 90, 1063–1102 (2010).
17
Mrosovsky N., Locomotor activity and non-photic influences on circadian clocks. Biol. Rev. Camb. Philos. Soc. 71, 343–372 (1996).
18
Mistlberger R. E., Skene D. J., Social influences on mammalian circadian rhythms: Animal and human studies. Biol. Rev. Camb. Philos. Soc. 79, 533–556 (2004).
19
Levine J. D., Funes P., Dowse H. B., Hall J. C., Resetting the circadian clock by social experience in Drosophila melanogaster. Science 298, 2010–2012 (2002).
20
Turek F. W., Losee-Olson S., A benzodiazepine used in the treatment of insomnia phase-shifts the mammalian circadian clock. Nature 321, 167–168 (1986).
21
Zimmerman W. F., Pittendrigh C. S., Pavlidis T., Temperature compensation of the circadian oscillation in drosophila pseudoobscura and its entrainment by temperature cycles. J. Insect Physiol. 14, 669–684 (1968).
22
Stokkan K. A., Yamazaki S., Tei H., Sakaki Y., Menaker M., Entrainment of the circadian clock in the liver by feeding. Science 291, 490–493 (2001).
23
Mrosovsky N., Salmon P. A., A behavioural method for accelerating re-entrainment of rhythms to new light-dark cycles. Nature 330, 372–373 (1987).
24
van Oosterhout F., Lucassen E. A., Houben T., vanderLeest H. T., Antle M. C., Meijer J. H., Amplitude of the SCN clock enhanced by the behavioral activity rhythm. PLOS ONE 7, e39693 (2012).
25
Mrosovsky N., Salmon P. A., Triazolam and phase-shifting acceleration re-evaluated. Chronobiol. Int. 7, 35–41 (1990).
26
Kamikouchi A., Albert J. T., Göpfert M. C., Mechanical feedback amplification in Drosophila hearing is independent of synaptic transmission. Eur. J. Neurosci. 31, 697–703 (2010).
27
Gegear R. J., Casselman A., Waddell S., Reppert S. M., Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454, 1014–1018 (2008).
28
Yoshii T., Ahmad M., Helfrich-Förster C., Cryptochrome mediates light-dependent magnetosensitivity of Drosophila’s circadian clock. PLOS Biol. 7, e1000086 (2009).
29
Wolfgang W., Simoni A., Gentile C., Stanewsky R., The Pyrexia transient receptor potential channel mediates circadian clock synchronization to low temperatures cycles in Drosophila melanogaster. Proc. Biol. Sci. 280, 20130959 (2013).
30
Gallio M., Ofstad T. A., Macpherson L. J., Wang J. W., Zuker C. S., The coding of temperature in the Drosophila brain. Cell 144, 614–624 (2011).
31
Sayeed O., Benzer S., Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 93, 6079–6084 (1996).
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Science
Volume 343 | Issue 6170
31 January 2014
31 January 2014
Copyright
Copyright © 2014, American Association for the Advancement of Science.
Submission history
Received: 9 September 2013
Accepted: 11 December 2013
Published in print: 31 January 2014
Acknowledgments
This work was supported by grants from the Biotechnology and Biological Sciences Research Council (BB/H001204/1 to R.S. and BB/G004455/1 to J.T.A.), the Human Frontier Science Program (to J.T.A.), and the European Union FP6 Integrated Project “EUCLOCK” (to R.S.). M.P.T. received funding from the Engineering and Physical Sciences Research Council (EP/F500351/1). Additional data, including raw data, are presented in the supplementary materials. The authors thank CoMPLEX students W. Ashworth and M. Ransley for their help, W. Potter for technical support, and P. Dayan from the Gatsby Computational Neuroscience Unit at University College London for valuable discussions.
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