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Chronobiology International
The Journal of Biological and Medical Rhythm Research
Volume 20, 2003 - Issue 2
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Original

Electrophysiology of the Circadian Pacemaker in Mammals

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Pages 171-188 | Published online: 07 Jul 2009

References

  • Abrahamson E. E., Moore R. Y. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res. 2001; 916: 172–191
  • Akasu T., Shoji S. cAMP-dependent inward rectifier current in neurons of the rat suprachiasmatic nucleus. Pflüeg. Arch. 1994; 429: 117–125
  • Akasu T., Shoji S., Ishimatsu M. Forskolin enhances inward rectifier current in neurons of rat suprachiasmatic nucleus. Kurume Med. J. 1992; 39: 213–217
  • Akasu T., Shoji S., Hasuo H. Inward rectifier and low-threshold calcium currents contribute to the spontaneous firing mechanism in neurons of the rat suprachiasmatic nucleus. Pflüeg. Arch. 1993; 425: 109–116
  • Albus H., Bonnefont X., Chaves I., Yasui A., Doczy J., van der Horst G. T. J., Meijer J. H. Cryptochrome-deficient mice lack circadian electrical activity in the suprachiasmatic nuclei. Curr. Biol. 2002; 12: 1130–1133
  • Allen G., Rappe J., Earnest D. J., Cassone V. M. Oscillating on borrowed time: diffusible signals from immortalized suprachiasmatic nucleus cells regulate circadian rhythmicity in cultured fibroblasts. J. Neurosci. 2001; 21: 7937–7943
  • Bae K., Jin X., Maywood E. S., Hastings M. H., Reppert S. M., Weaver D. R. Differential functions of mPer1, mPer2, and mPer3 in the SCN circadian clock. Neuron 2001; 30: 525–536
  • Balsalobre A., Damiola F., Schibler U. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 1998; 93: 929–937
  • Biello S. M., Golombek D. A., Schak K. M., Harrington M. E. Circadian phase shifts to neuropeptide Y in vitro: cellular communication and signal transduction. J. Neurosci. 1997; 17: 8468–8475
  • Block G. D., Khalsa S. B., McMahon D. G., Michel S., Guesz M. Biological clocks in the retina: cellular mechanisms of biological timekeeping. Int. Rev. Cytol. 1993; 146: 83–144
  • Bouskila Y., Dudek F. E. Neuronal synchronization without calcium-dependent synaptic transmission in the hypothalamus. Proc. Natl. Acad. Sci. USA 1993; 90: 3207–3210
  • Bouskila Y., Dudek F. E. A rapidly activating type of outward rectifier K7+ current and A-current in rat suprachiasmatic nucleus neurones. J. Physiol. 1995; 488: 339–350
  • Cahill G. M., Menaker M. Responses of the suprachiasmatic nucleus to retinohypothalamic tract volleys in a slice preparation of the mouse hypothalamus. Brain Res. 1989; 479: 65–75
  • Castel M., Morris J. F. Morphological heterogeneity of the GABAergic network in the suprachiasmatic nucleus, the brain's circadian pacemaker. J. Anat. 2000; 196(Pt 1)1–13
  • Chen G., van den Pol A. N. Multiple NPY receptors coexist in pre- and postsynaptic sites: inhibition of GABA release in isolated self-innervating SCN neurons. J. Neurosci. 1996; 16: 7711–7724
  • Chen D., Buchanan G. F., Ding J. M., Hannibal J., Gillette M. U. Pituitary adenylyl cyclase-activating peptide: a pivotal modulator of glutamatergic regulation of the suprachiasmatic circadian clock. Proc. Natl. Acad. Sci. USA 1999; 96: 13468–13473
  • Cheng M., Bullock C., Li C., Lee A., Bermak J., Belluzzi J., Weaver D., Leslie F., Zhou Q. Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 2002; 417: 405–410
  • Colwell C. S. Circadian modulation of calcium levels in cells in the suprachiasmatic nucleus. Eur. J. Neurosci. 2000a; 12: 571–576
  • Colwell C. S. Rhythmic coupling among cells in the suprachiasmatic nucleus. J. Neurobiol. 2000b; 43: 379–388
  • Colwell C. S. NMDA-evoked calcium transients and currents in the suprachiasmatic nucleus: gating by the circadian system. Eur. J. Neurosci. 2001; 13: 1420–1428
  • Daan S., Albrecht U., van der Horst G. T., Illnerova H., Roenneberg T., Wehr T. A., Schwartz W. J. Assembling a clock for all seasons: are there M and E oscillators in the genes?. J. Biol. Rhythms 2001; 16: 105–116
  • Ding J. M., Chen D., Weber E. T., Faiman L. E., Rea M. A., Gillette M. U. Resetting the biological clock: mediation of nocturnal circadian shifts by glutamate and NO. Science 1994; 266: 1713–1717
  • Ding J. M., Buchanan G. F., Tischkau S. A., Chen D., Kuriashkina L., Faiman L. E., Alster J. M., McPherson P. S., Campbell K. P., Gillette M. U. A neuronal ryanodine receptor mediates light-induced phase delays of the circadian clock. Nature 1998; 394: 381–384
  • van Esseveldt K. E., Lehman M. N., Boer G. J. The suprachiasmatic nucleus and the circadian time-keeping system revisited. Brain Res. Brain Res. Rev. 2000; 33: 34–77
  • Gerkema M. P., Van der Zee E. A., Feitsma L. E. Expression of circadian rhythmicity correlates with the number of arginine-vasopressin-immunoreactive cells in the suprachiasmatic nucleus of common voles, Microtus arvalis. Brain Res. 1994; 639: 93–101
  • Green D. J., Gillette R. Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res. 1982; 245: 198–200
  • 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. 1998; 18: 3014–3022
  • Gribkoff V. K., Pieschl R. L., Wisialowski T. A., Park W. K., Strecker G. J., de Jeu M. T., Pennartz C. M., Dudek F. E. A reexamination of the role of GABA in the mammalian suprachiasmatic nucleus. J. Biol. Rhythms 1999; 14: 126–130
  • Groos G. A., Hendriks J. Regularly firing neurones in the rat suprachiasmatic nucleus. Experientia 1979; 35: 1597–1598
  • Groos G., Hendriks J. Circadian rhythms in electrical discharge of rat suprachiasmatic neurones recorded in vitro. Neurosci. Lett. 1982; 34: 283–288
  • Guldner F. H., Wolff J. R. Complex synaptic arrangements in the rat suprachiasmatic nucleus: a possible basis for the “Zeitgeber” and non-synaptic synchronization of neuronal activity. Cell Tissue Res. 1996; 284: 203–214
  • Hall J. C. Circadian pacemakers blowing hot and cold—but they're clocks, not thermometers. Cell 1997; 90: 9–12
  • Hall A. C., Earle-Cruikshanks G., Harrington M. E. Role of membrane conductances and protein synthesis in subjective day phase advances of the hamster circadian clock by neuropeptide Y. Eur. J. Neurosci. 1999; 11: 3424–3432
  • Hamada T., Liou S. Y., Fukushima T., Maruyama T., Watanabe S., Mikoshiba K., Ishida N. The role of inositol trisphosphate-induced Ca2+ release from IP3- receptor in the rat suprachiasmatic nucleus on circadian entrainment mechanism. Neurosci. Lett. 1999; 263: 125–128
  • Harrington M. E., Hoque S., Hall A., Golombek D., Biello S. Pituitary adenylate cyclase activating peptide phase shifts circadian rhythms in a manner similar to light. J. Neurosci. 1999; 19: 6637–6642
  • Hastings M. Modeling the molecular calendar. J. Biol. Rhythms 2001; 16: 117–123, discussion 124
  • Herzog E. D., Geusz M. E., Khalsa S. B., Straume M., Block G. D. Circadian rhythms in mouse suprachiasmatic nucleus explants on multimicroelectrode plates. Brain Res. 1997; 757: 285–290
  • Herzog E. D., Takahashi J. S., Block G. D. Clock controls circadian periods in isolated suprachiasmatic nucleus neurons. Nat. Neurosci. 1998; 1: 708–713
  • Honma S., Ikeda M., Abe H., Tanahashi Y., Namihira M., Honma K., Nomura M. Circadian oscillation of BMAL1, a partner of a mammalian clock gene clock, in rat suprachiasmatic nucleus. Biochem. Biophys. Res. Commun. 1998; 250: 83–87
  • Honma S., Shirakawa T., Nakamura W., Honma K. Synaptic communication of cellular oscillations in the rat suprachiasmatic neurons. Neurosci. Lett. 2000; 294: 113–116
  • Honma S., Kawamoto T., Takagi Y., Fujimoto K., Sato F., Noshiro M., Kato Y., Honma K-I. Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature 2002; 419: 841–844
  • Inouye S. T., Kawamura H. Persistence of circadian rhythmicity in a mammalian hypothalamic “island” containing the suprachiasmatic nucleus. Proc. Natl. Acad. Sci. USA 1979; 76: 5962–5966
  • Inouye S. T., Kawamura H. Characteristics of a circadian pacemaker in the suprachiasmatic nucleus. J. Comp. Physiol. [A] 1982; 146: 153–160
  • Jacomy H., Burlet A., Bosler O. Vasoactive intestinal peptide neurons as synaptic targets for vasopressin neurons in the suprachiasmatic nucleus. Double-label immunocytochemical demonstration in the rat. Neuroscience 1999; 88: 859–870
  • Jagota A., de la Iglesia H. O., Schwartz W. J. Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro. Nat. Neurosci. 2000; 3: 372–376
  • Jahnsen H., Llinas R. Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J. Physiol. (Lond) 1984; 349: 227–247
  • Jansen K., Van der Zee E. A., Gerkema M. P. Being circadian or not: vasopressin release in cultured SCN mirrors behavior in adult voles. Neuroreport 2000; 11: 3555–3558
  • de Jeu M. T., Pennartz C. M. Functional characterization of the H-current in SCN neurons in subjective day and night: a whole-cell patch-clamp study in acutely prepared brain slices. Brain Res. 1997; 767: 72–80
  • de Jeu M., Pennartz C. Circadian modulation of GABA function in the rat suprachiasmatic nucleus: excitatory effects during the night phase. J. Neurophysiol. 2002; 87: 834–844
  • de Jeu M., Hermes M., Pennartz C. Circadian modulation of membrane properties in slices of rat suprachiasmatic nucleus. Neuroreport 1998; 9: 3725–3729
  • Jiang Z. G., Nelson C. S., Allen C. N. Melatonin activates an outward current and inhibits Ih in rat suprachiasmatic nucleus neurons. Brain Res. 1995; 687: 125–132
  • Jiang Z. G., Yang Y., Liu Z. P., Allen C. N. Membrane properties and synaptic inputs of suprachiasmatic nucleus neurons in rat brain slices. J. Physiol. (Lond) 1997a; 499(Pt 1)141–159
  • Jiang Z. G., Yang Y. Q., Allen C. N. Tracer and electrical coupling of rat suprachiasmatic nucleus neurons. Neuroscience 1997b; 77: 1059–1066
  • Kalsbeek A., van der Vliet J., Buijs R. M. Decrease of endogenous vasopressin release necessary for expression of the circadian rise in plasma corticosterone: a reverse microdialysis study. J. Neuroendocrinol. 1996; 8: 299–307
  • Kim Y. I., Dudek F. E. Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: inhibitory synaptic mechanisms. J. Physiol. (Lond) 1992; 458: 247–260
  • Kim Y. I., Dudek F. E. Membrane properties of rat suprachiasmatic nucleus neurons receiving optic nerve input. J. Physiol. (Lond) 1993; 464: 229–243
  • King D. P., Takahashi J. S. Molecular genetics of circadian rhythms in mammals. Annu. Rev. Neurosci. 2000; 23: 713–742
  • Lakin-Thomas P. L. Circadian rhythms: new functions for old clock genes. Trends Genet. 2000; 16: 135–142
  • Liu C., Reppert S. M. GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 2000; 25: 123–128
  • Liu C., Weaver D. R., Strogatz S. H., Reppert S. M. Cellular construction of a circadian clock: period determination in the suprachiasmatic nuclei. Cell 1997; 91: 855–860
  • Lowrey P. L., Shimomura K., Antoch M. P., Yamazaki S., Zemenides P. D., Ralph M. R., Menaker M., Takahashi J. S. Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science 2000; 288: 483–492
  • Lundkvist G. B., Kristensson K., Hill R. H. The suprachiasmatic nucleus exhibits diurnal variations in spontaneous excitatory postsynaptic activity. J. Biol. Rhythms 2002; 17: 40–51
  • Meijer J. H., Watanabe K., Detari L., Schaap J. Circadian rhythm in light response in suprachiasmatic nucleus neurons of freely moving rats. Brain Res. 1996; 741: 352–355
  • Meijer J. H., Schaap J., Watanabe K., Albus H. Multiunit activity recordings in the suprachiasmatic nuclei: in vivo versus in vitro models. Brain Res. 1997; 753: 322–327
  • Meijer J. H., Watanabe K., Schaap J., Albus H., Detari L. Light responsiveness of the suprachiasmatic nucleus: long-term multiunit and single-unit recordings in freely moving rats. J. Neurosci. 1998; 18: 9078–9087
  • Michel S., Geusz M. E., Zaritsky J. J., Block G. D. Circadian rhythm in membrane conductance expressed in isolated neurons. Science 1993; 259: 239–241
  • Moga M. M., Moore R. Y. Organization of neural inputs to the suprachiasmatic nucleus in the rat. J. Comp. Neurol. 1997; 389: 508–534
  • Moore R. Y. Entrainment pathways and the functional organization of the circadian system. Prog. Brain Res. 1996; 111: 103–119
  • Moore R. Y., Speh J. C. GABA is the principal neurotransmitter of the circadian system. Neurosci. Lett. 1993; 150: 112–116
  • Nakamura W., Honma S., Shirakawa T., Honma K.-I. Clock mutation lengthens the circadian period without damping rhythms in individual SCN neurons. Nat. Neurosci. 2002; 5: 399–400
  • Obrietan K., van den Pol A. GABAB receptor-mediated regulation of glutamate-activated calcium transients in hypothalamic and cortical neuron development. J. Neurophysiol. 1999; 82: 94–102
  • Palm I. F., Van Der Beek E. M., Wiegant V. M., Buijs R. M., Kalsbeek A. Vasopressin induces a luteinizing hormone surge in ovariectomized, estradiol-treated rats with lesions of the suprachiasmatic nucleus. Neuroscience 1999; 93: 659–666
  • Parpura V., Haydon P. G. From the cover: physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc. Natl. Acad. Sci. USA 2000; 97: 8629–8634
  • Pennartz C. M., Bierlaagh M. A., Geurtsen A. M. Cellular mechanisms underlying spontaneous firing in rat suprachiasmatic nucleus: involvement of a slowly inactivating component of sodium current. J. Neurophysiol. 1997; 78: 1811–1825
  • Pennartz C. M., De Jeu M. T., Geurtsen A. M., Sluiter A. A., Hermes M. L. Electrophysiological and morphological heterogeneity of neurons in slices of rat suprachiasmatic nucleus. J. Physiol. (Lond) 1998; 506(Pt 3)775–793
  • Pennartz C., de Jeu M., Bos N., Schaap J., Geurtsen A. Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock. Nature 2002; 416: 286–290
  • van den Pol A. N. The hypothalamic suprachiasmatic nucleus of rat: intrinsic anatomy. J. Comp. Neurol. 1980; 191: 661–702
  • van den Pol A. N., Dudek F. E. Cellular communication in the circadian clock, the suprachiasmatic nucleus. Neuroscience 1993; 56: 793–811
  • van den Pol A. N., Gorcs T. Synaptic relationships between neurons containing vasopressin, gastrin-releasing peptide, vasoactive intestinal polypeptide, and glutamate decarboxylase immunoreactivity in the suprachiasmatic nucleus: dual ultrastructural immunocytochemistry with gold-substituted silver peroxidase. J. Comp. Neurol. 1986; 252: 507–521
  • Preitner N., Damiola F., Molina L. L., Zakany J., Duboule D., Albrecht U., Schibler U. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 2002; 110: 251–260
  • Reppert S. M., Weaver D. R. Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 2001; 63: 647–676
  • Reppert S. M., Weaver D. R. Coordination of circadian timing in mammals. Nature 2002; 418: 935–941
  • Sah P. Ca2+-activated K+ currents in neurones: types, physiological roles and modulation. Trends Neurosci. 1996; 19: 150–154
  • Schaap J., Bos N. P., de Jeu M. T., Geurtsen A. M., Meijer J. H., Pennartz C. M. Neurons of the rat suprachiasmatic nucleus show a circadian rhythm in membrane properties that is lost during prolonged whole-cell recording. Brain Res. 1999; 815: 154–166
  • Schaap J., Albus H., Eilers P. H., Detari L., Meijer J. H. Phase differences in electrical discharge rhythms between neuronal populations of the left and right suprachiasmatic nuclei. Neuroscience 2001; 108: 359–363
  • Schwartz W. J., Davidsen L. C., Smith C. B. In vivo metabolic activity of a putative circadian oscillator, the rat suprachiasmatic nucleus. J. Comp. Neurol. 1980; 189: 157–167
  • Schwartz W. J., Gross R. A., Morton M. T. The suprachiasmatic nuclei contain a tetrodotoxin-resistant circadian pacemaker. Proc. Natl. Acad. Sci. USA 1987; 84: 1694–1698
  • Senseman D. M., Rea M. A. Fast multisite optical recording of mono- and polysynaptic activity in the hamster suprachiasmatic nucleus evoked by retinohypothalamic tract stimulation. Neuroimage 1994; 1: 247–263
  • Shearman L. P., Sriram S., Weaver D. R., Maywood E. S., Chaves I., Zheng B., Kume K., Lee C. C., van der Horst G. T., Hastings M. H., Reppert S. M. Interacting molecular loops in the mammalian circadian clock. Science 2000; 288: 1013–1019
  • Shibata S., Moore R. Y. Neuropeptide Y and optic chiasm stimulation affect suprachiasmatic nucleus circadian function in vitro. Brain Res. 1993a; 615: 95–100
  • Shibata S., Moore R. Y. Tetrodotoxin does not affect circadian rhythms in neuronal activity and metabolism in rodent suprachiasmatic nucleus in vitro. Brain Res. 1993b; 606: 259–266
  • Shibata S., Oomura Y., Kita H., Hattori K. Circadian rhythmic changes of neuronal activity in the suprachiasmatic nucleus of the rat hypothalamic slice. Brain Res. 1982; 247: 154–158
  • Shibata S., Oomura Y., Hattori K., Kita H. Responses of suprachiasmatic nucleus neurons to optic nerve stimulation in rat hypothalamic slice preparation. Brain Res. 1984; 302: 83–89
  • 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 1995; 92: 7396–7400
  • Shinohara K., Hiruma H., Funabashi T., Kimura F. GABAergic modulation of gap junction communication in slice cultures of the rat suprachiasmatic nucleus. Neuroscience 2000; 96: 591–596
  • Shirakawa T., Honma S., Honma K. Multiple oscillators in the suprachiasmatic nucleus. Chronobiol. Int. 2001; 18: 371–387
  • Strecker G. J., Wuarin J. P., Dudek F. E. GABAA-mediated local synaptic pathways connect neurons in the rat suprachiasmatic nucleus. J. Neurophysiol. 1997; 78: 2217–2220
  • Tamada Y., Tanaka M., Munekawa K., Hayashi S., Okamura H., Kubo T., Hisa Y., Ibata Y. Neuron-glia interaction in the suprachiasmatic nucleus: a double labeling light and electron microscopic immunocytochemical study in the rat. Brain Res. Bull. 1998; 45: 281–287
  • Thomson A. M., West D. C. Factors affecting slow regular firing in the suprachiasmatic nucleus in vitro. J. Biol. Rhythms 1990; 5: 59–75
  • Tischkau S. A., Gallman E. A., Buchanan G. F., Gillette M. U. Differential cAMP gating of glutamatergic signaling regulates long-term state changes in the suprachiasmatic circadian clock. J. Neurosci. 2000; 20: 7830–7837
  • van den Top M., Buijs R., Ruijter J., Delagrange P., Spanswick D., Hermes M. L. Melatonin generates an outward potassium current in rat suprachiasmatic nucleus neurones in vitro independent of their circadian rhythm. Neuroscience 2002; 107: 99–108
  • de Vries M. J., Treep J. A., de Pauw E. S., Meijer J. H. The effects of electrical stimulation of the optic nerves and anterior optic chiasm on the circadian activity rhythm of the Syrian hamster: involvement of excitatory amino acids. Brain Res. 1994; 642: 206–212
  • Wagner S., Castel M., Gainer H., Yarom Y. GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature 1997; 387: 598–603
  • 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 1995; 14: 697–706
  • Wheal H. V., Thomson A. M. The electrical properties of neurones of the rat suprachiasmatic nucleus recorded intracellularly in vitro. Neuroscience 1984; 13: 97–104
  • Yamazaki S., Kerbeshian M. C., Hocker C. G., Block G. D., Menaker M. Rhythmic properties of the hamster suprachiasmatic nucleus in vivo. J. Neurosci. 1998; 18: 10709–10723
  • Yamazaki S., Numano R., Abe M., Hida A., Takahashi R., Ueda M., Block G. D., Sakaki Y., Menaker M., Tei H. Resetting central and peripheral circadian oscillators in transgenic rats. Science 2000; 288: 682–685

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