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Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro

Nature Neuroscience volume 3, pages 372–376 (2000)Cite this article

Abstract

Daily biological rhythms are governed by an innate timekeeping mechanism, or ‘circadian clock’. In mammals, a clock in the suprachiasmatic nucleus (SCN) comprises multiple autonomous single-cell oscillators, but it is unclear how SCN cells interact to form a tissue with coherent metabolic and electrical rhythms that might account for circadian animal behaviors. Here we demonstrate that the circadian rhythm of SCN electrophysiological activity, recorded as a single daytime peak in hamster hypothalamic coronal slices, shows two distinct peaks when slices are cut in the horizontal plane. Substantiating an idea initially derived from behavioral observations, the properties of these two peaks indicate functional organization of SCN tissue as a clock with two oscillating components.

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Figure 1: Coronal and horizontal slices of hamster SCN.
Figure 2: Rhythms of SCN neuronal activity in coronal and horizontal slices.
Figure 3: Prior photoperiod affects the morning and evening peaks differently.
Figure 4: In vitro glutamate shifts the morning and evening peaks independently.

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References

  1. Pittendrigh, C. S. & Daan, S. A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: a clock for all seasons. J. Comp. Physiol. A 106, 333–355 (1976).

    Article  Google Scholar 

  2. Daan, S. & Berde, C. Two coupled oscillators: simulations of the circadian pacemaker in mammalian activity rhythms. J. Theor. Biol. 70, 297–313 ( 1978).

    Article  CAS  Google Scholar 

  3. Illnerová, H. & Vanĕc̆ek, J. Two-oscillator structure of the pacemaker controlling the circadian rhythm of N-acetyltransferase in the rat pineal gland. J. Comp. Physiol. A 145, 539–548 (1982).

    Article  Google Scholar 

  4. Elliott, J. A. & Tamarkin, L. Complex circadian regulation of pineal melatonin and wheel-running in Syrian hamsters. J. Comp. Physiol. A 174, 469–484 (1994).

    Article  CAS  Google Scholar 

  5. Honma, K., Honma, S. & Hiroshige, T. Response curve, free-running period, and activity time in circadian locomotor rhythm of rats. Jpn. J. Physiol. 35, 643–658 (1985).

    Article  CAS  Google Scholar 

  6. Meijer, J. H. & DeVries, M. J. Light-induced phase shifts in onset and offset of running-wheel activity in the Syrian hamster. J. Biol. Rhythms 10, 4–16 (1995).

    Article  CAS  Google Scholar 

  7. Inouye, S. T. & Kawamura, H. Persistence of circadian rhythmicity in a mammalian hypothalamic “island” containing the suprachiasmatic nucleus. Proc. Natl. Acad. Sci. USA 76, 5962–5966 (1979).

    Article  CAS  Google Scholar 

  8. Meijer, J. H., Watanabe, K., Schaap, J., Albus, H. & Détári, L. Light responsiveness of the suprachiasmatic nucleus: long-term multiunit and single-unit recordings in freely moving rats. J. Neurosci. 18, 9078– 9087 (1998).

    Article  CAS  Google Scholar 

  9. Yamazaki, S., Kerbeshian, M. C., Hocker, C. G., Block, G. D. & Menaker, M. Rhythmic properties of the hamster suprachiasmatic nucleus in vivo. J. Neurosci. 18, 10709–10723 (1998).

    Article  CAS  Google Scholar 

  10. Gillette, M. U. et al. in Circadian Clocks and Their Adjustment (eds. Chadwick, D. J. & Ackrill, K.) 134–153 (Wiley, Chichester, 1995).

    Google Scholar 

  11. Bouskila, Y. & Dudek, F. E. Neuronal synchronization without calcium-dependent synaptic transmission in the hypothalamus. Proc. Natl. Acad. Sci. USA 90, 3207–3210 (1993).

    Article  CAS  Google Scholar 

  12. Gribkoff, V. K., Pieschl, R. L., Wisialowski, T. A., van den Pol, A. N. & Yocca, F. D. Phase shifting of circadian rhythms and depression of neuronal activity in the rat suprachiasmatic nucleus by neuropeptide Y: mediation by different receptor subtypes. J. Neurosci. 18, 3014–3022 (1998).

    Article  CAS  Google Scholar 

  13. Meijer, J. H., Schaap, J., Watanabe, K. & Albus, H. Multiunit activity recordings in the suprachiasmatic nuclei: in vivo versus in vitro models. Brain Res. 753, 322– 327 (1997).

    Article  CAS  Google Scholar 

  14. Prosser, R. A. In vitro circadian rhythms of the mammalian suprachiasmatic nuclei: comparison of multi-unit and single-unit neuronal activity recordings. J. Biol. Rhythms 13, 30–38 (1998).

    Article  CAS  Google Scholar 

  15. Tcheng, T. K. & Gillette, M. U. A novel carbon fiber bundle microelectrode and modified brain slice chamber for recording long-term multiunit activity from brain slices. J. Neurosci. Methods 69 , 163–169 (1996).

    Article  CAS  Google Scholar 

  16. Liu, C. et al. Molecular dissection of two distinct actions of melatonin on the suprachiasmatic circadian clock. Neuron 19, 91–102 (1997).

    Article  CAS  Google Scholar 

  17. Mrugala, M. M., Zlomanczuk, P., Jagota, A. & Schwartz, W. J. Rhythmic multiunit neural activity in slices of hamster suprachiasmatic nucleus reflect prior photoperiod. Am. J. Physiol. (in press).

  18. Sumová, A., Trávníc̆ková, Z., Peters, R., Schwartz, W. J. & Illnerová, H. The rat suprachiasmatic nucleus is a clock for all seasons. Proc. Natl. Acad. Sci. USA 92, 7754–7758 (1995).

    Article  Google Scholar 

  19. Vuillez, P., Jacob, N., Teclemariam-Mesbah, R. & Pévet, P. In Syrian and European hamsters, the duration of sensitive phase to light of the suprachiasmatic nuclei depends on the photoperiod. Neurosci. Lett. 208, 37–40 ( 1996).

    Article  CAS  Google Scholar 

  20. Illnerová, H. & Vanĕc̆ek, J. Entrainment of the circadian rhythm in rat pineal N acetyltransferase activity under extremely long and short photoperiods. J. Pineal Res. 2, 67–78 ( 1985.

    Article  Google Scholar 

  21. Ebling, F. J. The role of glutamate in the photic regulation of the suprachiasmatic nucleus. Prog. Neurobiol. 50, 109– 132 (1996).

    Article  CAS  Google Scholar 

  22. Ding, J. M. et al. Resetting the biological clock: mediation of nocturnal circadian shifts by glutamate and NO. Science 266, 1713–1717 (1994).

    Article  CAS  Google Scholar 

  23. Franken, P., Cao, V., Heller, H. C. & Miller, J. D. The glutamate induced phase shift in the SCN slice: a two pulse study. Brain Res. 818, 34–40 ( 1999).

    Article  CAS  Google Scholar 

  24. Mason, R. The effects of continuous light exposure on Syrian hamster suprachiasmatic (SCN) neuronal discharge activity in vitro. Neurosci. Lett. 123, 160–163 ( 1991).

    Article  CAS  Google Scholar 

  25. Zlomanczuk, P., Margraf, R. R. & Lynch, G. R. In vitro electrical activity in the suprachiasmatic nucleus following splitting and masking of wheel-running behavior. Brain Res. 559, 94–99 ( 1991).

    Article  CAS  Google Scholar 

  26. Pickard, G. E. The afferent connections of the suprachiasmatic nucleus of the golden hamster with emphasis on the retinohypothalamic projection. J. Comp. Neurol. 211, 65–83 ( 1982).

    Article  CAS  Google Scholar 

  27. Kalsbeek, A., Teclemariam-Mesbah R. & Pévet, P. Efferent projections of the suprachiasmatic nucleus in the golden hamster (Mesocricetus auratus). J. Comp. Neurol. 332, 293–314 (1993).

    Article  CAS  Google Scholar 

  28. Morin, L. P., Goodless-Sanchez N., Smale, L. & Moore, R. Y. Projections of the suprachiasmtic nuclei, subparaventricular zone and retrochiasmatic area in the golden hamster. Neuroscience 61, 391–410 (1994).

    Article  CAS  Google Scholar 

  29. Shinohara, K., Honma, S., Katsuno, Y., Abe, H. & Honma, K. Two distinct oscillators in the rat suprachiasmatic nucleus in vitro. Proc. Natl. Acad. Sci. USA 92, 7396– 7400 (1995).

    Article  CAS  Google Scholar 

  30. Welsh, D. K., Logothetis, D. E., Meister, M. & Reppert, S. M. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14, 697–706 (1995).

    Article  CAS  Google Scholar 

  31. Herzog, E. D., Takahashi, J. S. & Block, G. D. Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nat. Neurosci. 1, 708– 713 (1998).

    Article  CAS  Google Scholar 

  32. Honma, S., Shirakawa, T., Katsuno, Y., Namihira, M. & Honma, K. Circadian periods of single suprachiasmatic neurons in rats. Neurosci. Lett. 250, 157 –160 (1998).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank David Paydarfar and Piotr Zlomanczuk for suggestions on the manuscript. This research is supported by the National Institute of Neurological Disorders and Stroke. The contents of this publication are solely the responsibility of the authors and do not necessarily represent the official views of the NINDS.

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Author notes

  1. Anita Jagota

    Present address: Department of Animal Sciences, School of Life Science, Uniersity of Hyderabad, Hyderabad, India, 500046

Authors and Affiliations

  1. Department of Neurology, University of Massachusetts Medical School, 55 Lake Avenue North, Worcester , 01655, Massachusetts, USA

    Anita Jagota, Horacio O. de la Iglesia & William J. Schwartz

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  1. Anita Jagota
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  2. Horacio O. de la Iglesia
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  3. William J. Schwartz
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Correspondence to William J. Schwartz.

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Jagota, A., de la Iglesia, H. & Schwartz, W. Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro. Nat Neurosci 3, 372–376 (2000). https://doi.org/10.1038/73943

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