Developmental and circadian changes in Ca2+ mobilization mediated by GABAA and NMDA receptors in the suprachiasmatic nucleus

European Journal of Neuroscience

Volumn 17, Issue 1, 2003, Pages 58-70

  Ikeda, Masayuki ^a,b,c   Yoshioka, Tohru ^c   Allen, Charles N ^b  

^a OSAKA BIOSCIENCE INSTITUTE   (Japan)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c WASEDA UNIVERSITY   (Japan)

Author keywords

Ca2+ imaging; Circadian rhythm; Fura 2; Mouse; Muscimol

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM ION; MAGNESIUM ION; MUSCIMOL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC RECEPTOR; TETRODOTOXIN;

AGE; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; BRAIN SLICE; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CELL POPULATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DEPOLARIZATION; DEVELOPMENTAL STAGE; ELECTRIC POTENTIAL; HYPOTHALAMUS; IMAGE ANALYSIS; LIGHT DARK CYCLE; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SUPRACHIASMATIC NUCLEUS;

ANIMALS; ANIMALS, NEWBORN; CALCIUM; CALCIUM CHANNEL BLOCKERS; CIRCADIAN RHYTHM; GABA AGONISTS; MAGNESIUM; MICE; MICE, INBRED C57BL; MUSCIMOL; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SODIUM CHANNEL BLOCKERS; SUPRACHIASMATIC NUCLEUS; TETRODOTOXIN;

EID: 0037234760     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02427.x     Document Type: Article

References (59)

1. Allen, C.N., Jiang, Z.G., Teshima, K., Darland, T., Ikeda, M., Nelson, C.S., Quigley, D.I., Yoshioka, T., Allen, R.G., Rea, M.A. & Grandy, D.K. (1999) Orphanin-FQ/nociceptin (OFQ/N) modulates the activity of suprachiasmatic nucleus neurons. J. Neurosci., 19, 2152-2160.
2. Bergeron, H.E., Danielson, B., Biggs, K.R. & Prosser, R.A. (1999) TTX blocks baclofen-induced phase shifts of the mammalian circadian pacemaker in vitro. Brain Res., 841, 193-196.
3. Buijs, R.M., Hou, Y.X., Shin, S. & Renaud, L.P. (1994) Ultrastructural evidence from intra- and extranuclear projections of GABAergic neurons of the suprachiasmatic nucleus. J. Comp. Neurol., 340, 381-391.
4. Chen, G., Trombely, P.Q. & van den Pol, A.N. (1996) Excitatory actions of GABA in developing rat hypothalamic neurons. J. Physiol. (Lond.), 494, 451-464.
5. Cherubini, E., Gaiarsa, J.L. & Ben-Ari, Y. (1991) GABA: an excitatory neurotransmitter in early postnatal life. Trends Neurosci., 14, 515-519.
6. Colwell, C.S. (2000a) Circadian modulation of calcium levels in cells in the suprachiasmatic nucleus. Eur. J. Neurosci., 12, 571-576.
7. Colwell, C.S. (2000b) Rhythmic coupling among cells in the suprachiasmatic nucleus. J. Neurobiol., 43, 379-388.
8. Decavel, C. & van den Pol, A.N. (1990) GABA: a dominant neurotransmitter in the hypothalamus. J. Comp. Neurol., 302, 1019-1037.
9. Ding, D.M., Chen, D., Weber, E.T., Faiman, L.E., Rea, M.A. & Gillette, M.U. (1994) Resetting the biological clock: mediation of nocturnal circadian shifts by glutamate and NO. Science, 266, 1713-1717.
10. Edelstein, K. & Amir, S. (1999) The role of the intergeniculate leaflet in entrainment of circadian rhythms to skeleton photoperiod. J. Neurosci., 19, 372-380.
11. Gao, X.B., Chen, G. & van den Pol, A. (1998) GABA-dependent firing of glutamate-evoked action potentials at AMPA/kainate receptors in developing hypothalamic neurons. J. Neurophysiol., 79, 716-726.
12. Gillette, M.U. (1986) The suprachiasmatic nuclei: circadian phase-shifts induced at the time of hypothalamic slice preparation are preserved in vitro. Brain Res., 379, 176-181.
13. Gribkoff, V.K., Pieschl, R.L., Wisialowski, T.A., Park, W.K., Strecker, G.J., de Jeu, M.T.G., Pennartz, C.M.A. & Dudek, F.E. (1999) A reexamination of the role of GABA in the mammalian suprachiasmatic nucleus. J. Biol. Rhythms, 14, 126-130.
14. Harrington, M.E., Nance, D.M. & Rusak, B. (1987) Double-labeling of neuropeptide Y-immunoreactive neurons which project from the geniculate to the suprachiasmatic nuclei. Brain Res., 410, 275-282.
15. Harrington, M.E. & Rusak, B. (1989) Photic response of geniculo-hypothalamic tract neurons in the Syrian hamster. Vis. Neurosci., 2, 367-375.
16. Huhman, K.L., Marvel, C.L., Gillespie, C.F., Mintz, E.M. & Albers, H.E. (1997) Tetrodotoxin blocks NPY-induced but not muscimol-induced phase advances of wheel-running activity in Syrian hamsters. Brain Res., 772, 176-180.
17. - in the suprachiasmatic nucleus. In Kuba, K., Higashida, H., Brown, D.A. & Yoshioka, T. (Eds), Slow Synaptic Responses and Modulation. Springer Verlag, Tokyo, pp. 200-205.
18. A and NMDA receptors in the suprachiasmatic nucleus. Soc. Neurosci. Abstr., 24, 1184.
19. Inouye, S.I.T. & Kawamura, H. (1979) Persistence of circadian rhythmicity in mammalian hypothalamic 'island' containing the suprachiasmatic nucleus. Proc. Natl Acad. Sci. USA, 76, 5962-5966.
20. de Jeu, M. & Pennartz, C.M.A. (2002) Circadian modulation of GABA function in the rat suprachiasmatic nucleus: excitatory effects during the night phase. J. Neurophysiol., 87, 834-844.
21. Jiang, Z.-G., Yang, Y.-Q. & Allen, C.N. (1997) Tracer and electrical coupling of rat suprachiasmatic nucleus neurons. Neuroscience, 77, 1059-1066.
22. + transient. J. Neurosci., 17, 7662-7672.
23. Lambert, N. & Grover, L. (1995) The mechanism of biphasic GABA response. Science, 269, 928-929.
24. Lavialle, M. & Servière, J. (1995) Developmental study in the circadian clock of the golden hamster: a putative role of astrocytes. Dev. Brain Res., 86, 275-282.
25. A and NMDA receptors in the neonatal hippocampus. Neuron, 18, 243-255.
26. 2+ rise in pyramidal cells and interneurons from rat neonatal hippocampal slices. J. Physiol. (Lond.), 487, 319-329.
27. Li, Y.-X., Schaffner, A.E., Walton, M.K. & Barker, J.L. (1998) Astrocytes regulate developmental changes in the chloride ion gradient of embryonic rat ventral spinal cord neurons in culture. J. Physiol. (Lond.), 509, 847-858.
28. Liu, C. & Reppert, S.M. (2000) GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron, 25, 123-128.
29. Moore, R.Y. & Eichler, V.B. (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res., 42, 201-206.
30. Moore, R.Y. & Speh, J.C. (1993) GABA is the principal neurotransmitter of the circadian system. Neurosci. Lett., 150, 112-116.
31. Müller, C. & Torrealba, F. (1998) Postnatal development of neuron number and connections in the suprachiasmatic nucleus of the hamster. Dev. Brain Res., 110, 203-213.
32. Munekawa, K., Tamada, Y., Iijima, N., Hayashi, S., Ishihara, A., Inoue, K., Tanaka, M. & Ibata, Y. (2000) Development of astroglial elements in the suprachiasmatic nucleus of the rat: with special reference to the involvement of the optic nerve. Exp. Neurol., 166, 44-51.
33. Munoz-Llamosas, M., Huerta, J.J., Cernuda-Cernuda, R. & Garcia-Fernandez, J.M. (2000) Ontogeny of a photic response in the retina and suprachiasmatic nucleus in the mouse. Dev. Brain Res., 120, 1-6.
34. Nakamura, W., Honma, S., Shirakawa, T. & Honma, K. (2001) Regional pacemakers composed of multiple oscillator neurons in the rat suprachiasmatic nucleus. Eur. J. Neurosci., 14, 666-674.
35. 2+ elevating to depressing. J. Neurosci., 15, 5065-5077.
36. Okamura, H., Berod, A., Julien, J.F., Geffard, M., Kitahama, K., Mallet, J. & Bobliller, P. (1986) Demonstration of GABAergic cell bodies in the suprachiasmatic nucleus: in situ hybridization of glutamic acid decarboxylase (GAD) mRNA and immunocytochemistry of GAD and GABA. Neurosci. Lett., 102, 131-136.
37. Pennartz, C.M., de Jeu, M.T., Bos, N.P., Schaap, J. & Geurtsen, A.M. (2002) Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock. Nature, 416, 286-290.
38. Pennartz, C.M.A., Hamstra, R. & Geurtsen, A.M.S. (2001) Enhanced NMDA receptor activity in retinal inputs to the rat suprachiasmatic nucleus during the subjective night. J. Physiol. (Lond.), 532, 181-194.
39. Perez de la Mora, M., Possani, L.D., Tapia, R., Teran, L., Palacios, R., Fuxe, K., Hokfelt, T. & Ljungdhal, A. (1981) Demonstration of gamma-aminobutyrate-containing nerve terminals by means of antibodies against glutamate decarboxylase. Neuroscience, 6, 875-895.
40. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature, 397, 251-255.
41. Rusak, B., Meijer, J.H. & Harrington, M.E. (1989) Hamster circadian rhythms are phase-shifted by electrical stimulation of the geniculo-hypothalamic tract. Brain Res., 493, 283-291.
42. Rusak, B. & Zucker, I. (1979) Neuronal regulation of circadian rhythms. Physiol. Rev., 59, 449-526.
43. Shibata, S., Liou, S.Y. & Ueki, S. (1983) Development of the circadian rhythm of neuronal activity in suprachiasmatic nucleus of rat hypothalamic slices. Neurosci. Lett., 43, 231-234.
44. Shibata, S. & Moore, R.Y. (1987) Development of neuronal activity in the rat suprachiasmatic nucleus. Dev. Brain Res., 34, 311-315.
45. Shibata, S., Oomura, Y., Liou, S.Y. & Ueki, S. (1984) Electrophysiological studies of the development of suprachiasmatic neuronal activity in hypothalamic slice preparations. Brain Res., 315, 29-35.
46. Shirakawa, T., Honma, S., Katsuno, Y., Oguchi, H. & Honma, K. (2000) Synchronization of circadian firing rhythms in cultured rat suprachiasmatic neurons. Eur. J. Neurosci., 12, 2833-2838.
47. Smith, R.D., Inouye, S.I.T. & Turek, F.W. (1989) Central administration of muscimol phase-shifts the mammalian circadian clock. J. Comp. Physiol. A., 164, 805-814.
48. 2+ concentrations in chick embryo ciliary ganglion cells. J. Neurochem., 69, 797-805.
49. Speh, J.C. & Moore, R.Y. (1993) Retinohypothalamic tract development in the hamster and rat. Dev. Brain Res., 76, 171-181.
50. A receptors. Science, 269, 977-981.
51. Stephan, F.K. & Zucker, I. (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc. Natl Acad. Sci. USA, 69, 1583-1586.
52. A receptor agonist muscimol can reset the phase of neural activity rhythm in the rat suprachiasmatic nucleus in vitro. Neurosci. Lett., 166, 81-84.
53. Torrealba, F., Parraguez, V.H., Reyes, G., Valenzuela, G. & Serón-Ferré, M. (1993) Prenatal development of the retinohypothalamic pathway and the suprachiasmatic nucleus in the sheep. J. Comp. Neurol., 338, 304-316.
54. Viswanathan, N., Weaver, D.R., Reppert, S.M. & Davis, F.C. (1994) Entrainment of the fetal hamster circadian pacemaker by prenatal injection of the dopamine agonist SFK 38393. J. Neurosci., 14, 5393-5398.
55. de Vries, M.J., Cardozo, B.N., van der Want, J., de Wolf, A. & Meijer, J.H. (1993) Glutamate immunoreactivity in terminals of the retinohypothalamic tract of the brown Norwegian rat. Brain Res., 612, 231-237.
56. Wagner, S., Castel, M., Gainer, H. & Yarom, Y. (1997) GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature, 387, 598-603.
57. Wagner, S., Sagiv, N. & Yarom, Y. (2001) GABA-induced current and circadian regulation of chloride in neurones of the rat suprachiasmatic nucleus. J. Physiol. (Lond.), 537, 853-869.
58. Welsh, D.K. & Reppert, S.M. (1996) Gap junctions couple astrocytes but not neurons in dissociated cultures of rat suprachiasmatic nucleus. Brain Res., 706, 30-36.
59. Zhang, D.X. & Rusak, B. (1989) Photic sensitivity of geniculate neurons that project to the suprachiasmatic nuclei or contralateral geniculate. Brain Res., 504, 161-164.