Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1996 Dec 1;497(Pt 2):483–493. doi: 10.1113/jphysiol.1996.sp021782

Synaptic input from the retina to the suprachiasmatic nucleus changes with the light-dark cycle in the Syrian hamster.

L N Cui 1, R E Dyball 1
PMCID: PMC1160998  PMID: 8961189

Abstract

1. Single cell extracellular recordings were made from the suprachiasmatic nucleus (SCN) in urethane-anaesthetized Syrian hamsters at different times of the light-dark cycle. Peristimulus time histograms (PSTHs) were created following stimulation of the optic nerve. 2. Both short-latency (< 50 ms) and long-latency (> 50 ms) excitatory responses were seen. Almost all inhibitory responses had a short latency. 3. A total of 288 SCN neurones were recorded. Taking all types of response together, 55 (36.9%) of the 149 neurones tested in the dark period responded to optic nerve stimulation while only 23 (16.6%) of the 139 neurones tested in the light period responded. The difference between the proportion of all responsive and non-responsive neurones in the dark and light periods was highly significant (P < 0.01, Fisher's exact probability test). The difference in the proportion of excitatory responses was also significant (P < 0.01). 4. During the dark period, the mean spontaneous firing rate (5.00 +/- 0.88 spikes s-1; mean +/- S.E.M., n = 55) of the responsive cells was significantly higher than that of the non-responsive cells (2.65 +/- 0.33 spikes s-1; mean +/- S.E.M., n = 74; P < 0.01; Student's unpaired t test). 5. Injection of APV (20 mM, 2 microliters, I.C.V.; n = 6), an antagonist for the NMDA receptor, or CNQX (10 mM, 2 microliters, I.C.V.; n = 5), an antagonist of the non-NMDA receptor, significantly reduced the responses of all the neurones tested. 6. We conclude that there is daily variation in the firing of SCN neurones in vivo and the variation is restricted to those cells receiving optic nerve inputs. The change in the responsiveness of the SCN to optic nerve stimulation at different times of day suggests that there is a rapidly changing cycle of synaptic function in the SCN. The action of the antagonists suggests that the excitatory retinal projections to the SCN which show this variation are mediated by glutamate and that both NMDA and non-NMDA receptors are involved.

Full text

PDF
483

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abe H., Rusak B., Robertson H. A. NMDA and non-NMDA receptor antagonists inhibit photic induction of Fos protein in the hamster suprachiasmatic nucleus. Brain Res Bull. 1992 May;28(5):831–835. doi: 10.1016/0361-9230(92)90269-4. [DOI] [PubMed] [Google Scholar]
  2. Bouskila Y., Dudek F. E. Neuronal synchronization without calcium-dependent synaptic transmission in the hypothalamus. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3207–3210. doi: 10.1073/pnas.90.8.3207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cahill G. M., Menaker M. Effects of excitatory amino acid receptor antagonists and agonists on suprachiasmatic nucleus responses to retinohypothalamic tract volleys. Brain Res. 1989 Feb 6;479(1):76–82. doi: 10.1016/0006-8993(89)91337-1. [DOI] [PubMed] [Google Scholar]
  4. Card J. P., Moore R. Y. Organization of lateral geniculate-hypothalamic connections in the rat. J Comp Neurol. 1989 Jun 1;284(1):135–147. doi: 10.1002/cne.902840110. [DOI] [PubMed] [Google Scholar]
  5. Colwell C. S., Menaker M. NMDA as well as non-NMDA receptor antagonists can prevent the phase-shifting effects of light on the circadian system of the golden hamster. J Biol Rhythms. 1992 Summer;7(2):125–136. doi: 10.1177/074873049200700204. [DOI] [PubMed] [Google Scholar]
  6. Colwell C. S., Ralph M. R., Menaker M. Do NMDA receptors mediate the effects of light on circadian behavior? Brain Res. 1990 Jul 16;523(1):117–120. doi: 10.1016/0006-8993(90)91643-u. [DOI] [PubMed] [Google Scholar]
  7. Ellaway P. H. Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroencephalogr Clin Neurophysiol. 1978 Aug;45(2):302–304. doi: 10.1016/0013-4694(78)90017-2. [DOI] [PubMed] [Google Scholar]
  8. Gannon R. L., Rea M. A. In situ hybridization of antisense mRNA oligonucleotides for AMPA, NMDA and metabotropic glutamate receptor subtypes in the rat suprachiasmatic nucleus at different phases of the circadian cycle. Brain Res Mol Brain Res. 1994 Jun;23(4):338–344. doi: 10.1016/0169-328x(94)90244-5. [DOI] [PubMed] [Google Scholar]
  9. Glotzbach S. F., Cornett C. M., Heller H. C. Activity of suprachiasmatic and hypothalamic neurons during sleep and wakefulness in the rat. Brain Res. 1987 Sep 1;419(1-2):279–286. doi: 10.1016/0006-8993(87)90594-4. [DOI] [PubMed] [Google Scholar]
  10. Green D. J., Gillette R. Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res. 1982 Aug 5;245(1):198–200. doi: 10.1016/0006-8993(82)90361-4. [DOI] [PubMed] [Google Scholar]
  11. Groos G. A., Hendriks J. Regularly firing neurones in the rat suprachiasmatic nucleus. Experientia. 1979 Dec 15;35(12):1597–1598. doi: 10.1007/BF01953215. [DOI] [PubMed] [Google Scholar]
  12. Harrington M. E., Nance D. M., Rusak B. Double-labeling of neuropeptide Y-immunoreactive neurons which project from the geniculate to the suprachiasmatic nuclei. Brain Res. 1987 May 5;410(2):275–282. doi: 10.1016/0006-8993(87)90325-8. [DOI] [PubMed] [Google Scholar]
  13. Inouye S. T., Kawamura H. Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5962–5966. doi: 10.1073/pnas.76.11.5962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ishida N., Matsui M., Mitsui Y., Mishina M. Circadian expression of NMDA receptor mRNAs, epsilon 3 and zeta 1, in the suprachiasmatic nucleus of rat brain. Neurosci Lett. 1994 Jan 31;166(2):211–215. doi: 10.1016/0304-3940(94)90488-x. [DOI] [PubMed] [Google Scholar]
  15. Kim Y. I., Dudek F. E. Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: excitatory synaptic mechanisms. J Physiol. 1991 Dec;444:269–287. doi: 10.1113/jphysiol.1991.sp018877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kim Y. I., Dudek F. E. Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: inhibitory synaptic mechanisms. J Physiol. 1992 Dec;458:247–260. doi: 10.1113/jphysiol.1992.sp019416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kornhauser J. M., Nelson D. E., Mayo K. E., Takahashi J. S. Photic and circadian regulation of c-fos gene expression in the hamster suprachiasmatic nucleus. Neuron. 1990 Aug;5(2):127–134. doi: 10.1016/0896-6273(90)90303-w. [DOI] [PubMed] [Google Scholar]
  18. Meijer J. H., Groos G. A., Rusak B. Luminance coding in a circadian pacemaker: the suprachiasmatic nucleus of the rat and the hamster. Brain Res. 1986 Sep 10;382(1):109–118. doi: 10.1016/0006-8993(86)90117-4. [DOI] [PubMed] [Google Scholar]
  19. Meijer J. H., van der Zee E. A., Dietz M. Glutamate phase shifts circadian activity rhythms in hamsters. Neurosci Lett. 1988 Mar 31;86(2):177–183. doi: 10.1016/0304-3940(88)90567-8. [DOI] [PubMed] [Google Scholar]
  20. Moore R. Y., Eichler V. B. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res. 1972 Jul 13;42(1):201–206. doi: 10.1016/0006-8993(72)90054-6. [DOI] [PubMed] [Google Scholar]
  21. Moore R. Y., Halaris A. E., Jones B. E. Serotonin neurons of the midbrain raphe: ascending projections. J Comp Neurol. 1978 Aug 1;180(3):417–438. doi: 10.1002/cne.901800302. [DOI] [PubMed] [Google Scholar]
  22. Moore R. Y., Lenn N. J. A retinohypothalamic projection in the rat. J Comp Neurol. 1972 Sep;146(1):1–14. doi: 10.1002/cne.901460102. [DOI] [PubMed] [Google Scholar]
  23. Nishino H., Kiyomi K., Brooks C. M. The role of suprachiasmatic nuclei of the hypothalamus in the production of circadian rhythm. Brain Res. 1976 Aug 6;112(1):45–59. doi: 10.1016/0006-8993(76)90333-4. [DOI] [PubMed] [Google Scholar]
  24. Ohi K., Takashima M., Nishikawa T., Takahashi K. N-methyl-D-aspartate receptor participates in neuronal transmission of photic information through the retinohypothalamic tract. Neuroendocrinology. 1991 Apr;53(4):344–348. doi: 10.1159/000125740. [DOI] [PubMed] [Google Scholar]
  25. Ralph M. R., Foster R. G., Davis F. C., Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science. 1990 Feb 23;247(4945):975–978. doi: 10.1126/science.2305266. [DOI] [PubMed] [Google Scholar]
  26. Sawaki Y. Suprachiasmatic nucleus neurones: excitation and inhibition mediated by the direct retino-hypothalamic projection in female rats. Exp Brain Res. 1979 Sep;37(1):127–138. doi: 10.1007/BF01474259. [DOI] [PubMed] [Google Scholar]
  27. Schwartz W. J., Gainer H. Suprachiasmatic nucleus: use of 14C-labeled deoxyglucose uptake as a functional marker. Science. 1977 Sep 9;197(4308):1089–1091. doi: 10.1126/science.887940. [DOI] [PubMed] [Google Scholar]
  28. Shibata S., Liou S. Y., Ueki S. Influence of excitatory amino acid receptor antagonists and of baclofen on synaptic transmission in the optic nerve to the suprachiasmatic nucleus in slices of rat hypothalamus. Neuropharmacology. 1986 Apr;25(4):403–409. doi: 10.1016/0028-3908(86)90235-2. [DOI] [PubMed] [Google Scholar]
  29. Shibata S., Moore R. Y. Electrical and metabolic activity of suprachiasmatic nucleus neurons in hamster hypothalamic slices. Brain Res. 1988 Jan 12;438(1-2):374–378. doi: 10.1016/0006-8993(88)91367-4. [DOI] [PubMed] [Google Scholar]
  30. Shibata S., Newman G. C., Moore R. Y. Effects of calcium ions on glucose utilization in the rat suprachiasmatic nucleus in vitro. Brain Res. 1987 Nov 24;426(2):332–338. doi: 10.1016/0006-8993(87)90886-9. [DOI] [PubMed] [Google Scholar]
  31. Shibata S., Oomura Y., Liou S. Y., Ueki S. Electrophysiological studies of the development of suprachiasmatic neuronal activity in hypothalamic slice preparations. Brain Res. 1984 Mar;315(1):29–35. doi: 10.1016/0165-3806(84)90074-9. [DOI] [PubMed] [Google Scholar]
  32. Stephan F. K., Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1583–1586. doi: 10.1073/pnas.69.6.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Thomson A. M., West D. C., Vlachonikolis I. G. Regular firing patterns of suprachiasmatic neurons maintained in vitro. Neurosci Lett. 1984 Dec 21;52(3):329–334. doi: 10.1016/0304-3940(84)90183-6. [DOI] [PubMed] [Google Scholar]
  34. Walsh I. B., van den Berg R. J., Marani E., Rietveld W. J. Spontaneous and stimulated firing in cultured rat suprachiasmatic neurons. Brain Res. 1992 Aug 14;588(1):120–131. doi: 10.1016/0006-8993(92)91351-e. [DOI] [PubMed] [Google Scholar]
  35. 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 Apr;14(4):697–706. doi: 10.1016/0896-6273(95)90214-7. [DOI] [PubMed] [Google Scholar]
  36. 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 Apr 11;642(1-2):206–212. doi: 10.1016/0006-8993(94)90923-7. [DOI] [PubMed] [Google Scholar]
  37. van de Kar L. D., Lorens S. A. Differential serotonergic innervation of individual hypothalamic nuclei and other forebrain regions by the dorsal and median midbrain raphe nuclei. Brain Res. 1979 Feb 16;162(1):45–54. doi: 10.1016/0006-8993(79)90754-6. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES