Reviews in Endocrine and Metabolic Disorders

, Volume 10, Issue 4, pp 279–291

Physiological responses of the circadian clock to acute light exposure at night

  • Michael C. Antle
  • Victoria M. Smith
  • Roxanne Sterniczuk
  • Glenn R. Yamakawa
  • Brooke D. Rakai
Article

Abstract

Circadian rhythms in physiological, endocrine and metabolic functioning are controlled by a neural clock located in the suprachiasmatic nucleus (SCN). This structure is endogenously rhythmic and the phase of this rhythm can be reset by light information from the eye. A key feature of the SCN is that while it is a small structure containing on the order of about 20,000 cells, it is amazingly heterogeneous. It is likely that anatomical heterogeneity reflects an underlying functional heterogeneity. In this review, we examine the physiological responses of cells in the SCN to light stimuli that reset the phase of the circadian clock, highlighting where possible the spatial pattern of such responses. Increases in intracellular calcium are an important signal in response to light, and this increase triggers many biochemical cascades that mediate responses to light. Furthermore, only some cells in the SCN are actually endogenously rhythmic, and these cells likely do not receive strong direct input from the retina. Therefore, this review also considers how light information is conveyed from the retinorecipient cells to the endogenously rhythmic cells that track circadian phase. A number of neuropeptides, including vasoactive intestinal polypeptide, gastrin-releasing peptide and substance P, may be particularly important in relaying such signals, but other neurochemicals such as GABA and nitric oxide may participate as well. A thorough understanding of the intracellular and intercellular responses to light, as well as the spatial arrangements of such responses may help identify important pharmacological targets for therapeutic interventions to treat sleep and circadian disorders.

Keywords

VIP GRP SP PKC PKG PKA MAPK CamKII Kinase 

References

  1. 1.
    Moore RY, Eichler VB. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res. 1972;42:201–6.PubMedGoogle Scholar
  2. 2.
    Stephan FK, Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA. 1972;69:1583–6.PubMedGoogle Scholar
  3. 3.
    Knutsson A. Health disorders of shift workers. Occup Med (Lond). 2003;53:103–8.Google Scholar
  4. 4.
    Hoogerwerf WA. Role of biological rhythms in gastrointestinal health and disease. Rev Endoc Metab Dis. 2009. doi:10.1007/s11154-009-9119-3.
  5. 5.
    van Mark A, Spallek M, Kessel R, Brinkmann E. Shift work and pathological conditions. J Occup Med Toxicol. 2006;1:25.PubMedGoogle Scholar
  6. 6.
    Antle MC, Silver R. Orchestrating time: arrangements of the brain circadian clock. Trends Neurosci. 2005;28:145–51.PubMedGoogle Scholar
  7. 7.
    Yan L. Expression of clock genes in the suprachiasmatic nucleus: effect of environmental lighting conditions. Rev Endoc Metab Dis. 2009. doi:10.1007/s11154-009-9121-9.
  8. 8.
    Reppert SM, Weaver DR. Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol. 2001;63:647–76.PubMedGoogle Scholar
  9. 9.
    Tosini G. Role of the retina in regulation of circadian rhythms. Rev Endoc Metab Dis. 2009. doi:10.1007/s11154-009-9120-x.
  10. 10.
    Moore RY. Entrainment pathways and the functional organization of the circadian system. Prog Brain Res. 1996;111:103–19.PubMedGoogle Scholar
  11. 11.
    Morin LP. SCN organization reconsidered. J Biol Rhythms. 2007;22:3–13.PubMedGoogle Scholar
  12. 12.
    Morin LP, Shivers KY, Blanchard JH, Muscat L. Complex organization of mouse and rat suprachiasmatic nucleus. Neuroscience 2006;137:1285–97.PubMedGoogle Scholar
  13. 13.
    Hamada T, LeSauter J, Venuti JM, Silver R. Expression of Period genes: rhythmic and nonrhythmic compartments of the suprachiasmatic nucleus pacemaker. J Neurosci. 2001;21:7742–50.PubMedGoogle Scholar
  14. 14.
    Karatsoreos IN, Yan L, LeSauter J, Silver R. Phenotype matters: identification of light-responsive cells in the mouse suprachiasmatic nucleus. J Neurosci. 2004;24:68–75.PubMedGoogle Scholar
  15. 15.
    Hamada T, Antle MC, Silver R. Temporal and spatial expression patterns of canonical clock genes and clock-controlled genes in the suprachiasmatic nucleus. Eur J NeuroSci. 2004;19:1741–8.PubMedGoogle Scholar
  16. 16.
    Yan L, Silver R. Differential induction and localization of mPer1 and mPer2 during advancing and delaying phase shifts. Eur J NeuroSci. 2002;16:1531–40.PubMedGoogle Scholar
  17. 17.
    Ebling FJ. The role of glutamate in the photic regulation of the suprachiasmatic nucleus. Prog Neurobiol. 1996;50:109–32.PubMedGoogle Scholar
  18. 18.
    Mikkelsen JD, Larsen PJ, Mick G, Vrang N, Ebling FJ, Maywood ES, et al. Gating of retinal inputs through the suprachiasmatic nucleus: role of excitatory neurotransmission. Neurochem Int. 1995;27:263–72.PubMedGoogle Scholar
  19. 19.
    Gannon RL, Rea MA. 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;23:338–44.PubMedGoogle Scholar
  20. 20.
    Mick G, Yoshimura R, Ohno K, Kiyama H, Tohyama M. The messenger RNAs encoding metabotropic glutamate receptor subtypes are expressed in different neuronal subpopulations of the rat suprachiasmatic nucleus. Neuroscience 1995;66:161–73.PubMedGoogle Scholar
  21. 21.
    Hannibal J. Neurotransmitters of the retino-hypothalamic tract. Cell Tissue Res. 2002;309:73–88.PubMedGoogle Scholar
  22. 22.
    Rea MA, Buckley B, Lutton LM. Local administration of EAA antagonists blocks light-induced phase shifts and c-fos expression in hamster SCN. Am J Physiol. 1993;265:R1191–8.PubMedGoogle Scholar
  23. 23.
    Haak LL. Metabotropic glutamate receptor modulation of glutamate responses in the suprachiasmatic nucleus. J Neurophysiol. 1999;81:1308–17.PubMedGoogle Scholar
  24. 24.
    Scott G, Rusak B. Activation of hamster suprachiasmatic neurons in vitro via metabotropic glutamate receptors. Neuroscience 1996;71:533–41.PubMedGoogle Scholar
  25. 25.
    Mintz EM, Marvel CL, Gillespie CF, Price KM, Albers HE. Activation of NMDA receptors in the suprachiasmatic nucleus produces light-like phase shifts of the circadian clock in vivo. J Neurosci. 1999;19:5124–30.PubMedGoogle Scholar
  26. 26.
    Meijer JH, Groos GA, Rusak B. Luminance coding in a circadian pacemaker: the suprachiasmatic nucleus of the rat and the hamster. Brain Res. 1986;382:109–18.PubMedGoogle Scholar
  27. 27.
    Meijer JH, Watanabe K, Detari L, Schaap J. Circadian rhythm in light response in suprachiasmatic nucleus neurons of freely moving rats. Brain Res. 1996;741:352–5.PubMedGoogle Scholar
  28. 28.
    Meijer JH, 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;18:9078–87.PubMedGoogle Scholar
  29. 29.
    Cahill GM, 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.PubMedGoogle Scholar
  30. 30.
    Schmahl C, Bohmer G. Effects of excitatory amino acids and neuropeptide Y on the discharge activity of suprachiasmatic neurons in rat brain slices. Brain Res. 1997;746:151–63.PubMedGoogle Scholar
  31. 31.
    Meijer JH, Schwartz WJ. In search of the pathways for light-induced pacemaker resetting in the suprachiasmatic nucleus. J Biol Rhythms. 2003;18:235–49.PubMedGoogle Scholar
  32. 32.
    Nakamura TJ, Fujimura K, Ebihara S, Shinohara K. Light response of the neuronal firing activity in the suprachiasmatic nucleus of mice. Neurosci Lett. 2004;371:244–8.PubMedGoogle Scholar
  33. 33.
    Borjigin J. Intrinsic and extrinsic control of melatonin production. Rev Endoc Metab Dis. 2009.Google Scholar
  34. 34.
    Colwell CS. NMDA-evoked calcium transients and currents in the suprachiasmatic nucleus: gating by the circadian system. Eur J NeuroSci. 2001;13:1420–8.PubMedGoogle Scholar
  35. 35.
    Irwin RP, Allen CN. Calcium response to retinohypothalamic tract synaptic transmission in suprachiasmatic nucleus neurons. J Neurosci. 2007;27:11748–57.PubMedGoogle Scholar
  36. 36.
    Ding JM, Buchanan GF, Tischkau SA, Chen D, Kuriashkina L, Faiman LE, et al. A neuronal ryanodine receptor mediates light-induced phase delays of the circadian clock. Nature 1998;394:381–4.PubMedGoogle Scholar
  37. 37.
    Gillette MU. Cellular and biochemical mechanisms underlying circadian rhythms in vertebrates. Curr Opin Neurobiol. 1997;7:797–804.PubMedGoogle Scholar
  38. 38.
    Gillette MU, Mitchell JW. Signaling in the suprachiasmatic nucleus: selectively responsive and integrative. Cell Tissue Res. 2002;309:99–107.PubMedGoogle Scholar
  39. 39.
    Golombek DA, Ralph MR. KN-62, an inhibitor of Ca2+/calmodulin kinase II, attenuates circadian responses to light. NeuroReport 1994;5:1638–40.PubMedGoogle Scholar
  40. 40.
    Golombek DA, Ralph MR. Circadian responses to light: the calmodulin connection. Neurosci Lett. 1995;192:101–4.PubMedGoogle Scholar
  41. 41.
    Yokota S, Yamamoto M, Moriya T, Akiyama M, Fukunaga K, Miyamoto E, et al. Involvement of calcium-calmodulin protein kinase but not mitogen-activated protein kinase in light-induced phase delays and Per gene expression in the suprachiasmatic nucleus of the hamster. J Neurochem. 2001;77:618–27.PubMedGoogle Scholar
  42. 42.
    Butcher GQ, Dziema H, Collamore M, Burgoon PW, Obrietan K. The p42/44 mitogen-activated protein kinase pathway couples photic input to circadian clock entrainment. J Biol Chem. 2002;277:29519–25.PubMedGoogle Scholar
  43. 43.
    Gau D, Lemberger T, von Gall C, Kretz O, Le Minh N, Gass P, et al. Phosphorylation of CREB Ser142 regulates light-induced phase shifts of the circadian clock. Neuron 2002;34:245–53.PubMedGoogle Scholar
  44. 44.
    Kornhauser JM, Cowan CW, Shaywitz AJ, Dolmetsch RE, Griffith EC, Hu LS, et al. CREB transcriptional activity in neurons is regulated by multiple, calcium-specific phosphorylation events. Neuron 2002;34:221–33.PubMedGoogle Scholar
  45. 45.
    Lee B, Almad A, Butcher G, Obrietan K. Protein kinase C modulates the phase-delaying effects of light in the mammalian circadian clock. Eur J NeuroSci. 2007;26:451–62.PubMedGoogle Scholar
  46. 46.
    Van der Zee EA, Bult A. Distribution of AVP and Ca2+-dependent PKC-isozymes in the suprachiasmatic nucleus of the mouse and rabbit. Brain Res. 1995;701:99–107.PubMedGoogle Scholar
  47. 47.
    Ding JM, Chen D, Weber ET, Faiman LE, Rea MA, Gillette MU. Resetting the biological clock: mediation of nocturnal circadian shifts by glutamate and NO. Science 1994;266:1713–7.PubMedGoogle Scholar
  48. 48.
    Weber ET, Gannon RL, Michel AM, Gillette MU, Rea MA. Nitric oxide synthase inhibitor blocks light-induced phase shifts of the circadian activity rhythm, but not c-fos expression in the suprachiasmatic nucleus of the Syrian hamster. Brain Res. 1995;692:137–42.PubMedGoogle Scholar
  49. 49.
    Golombek DA, Agostino PV, Plano SA, Ferreyra GA. Signaling in the mammalian circadian clock: The NO/cGMP pathway. Neurochem Int. 2004;45:929–36.PubMedGoogle Scholar
  50. 50.
    Ding JM, Faiman LE, Hurst WJ, Kuriashkina LR, Gillette MU. Resetting the biological clock: mediation of nocturnal CREB phosphorylation via light, glutamate, and nitric oxide. J Neurosci. 1997;17:667–75.PubMedGoogle Scholar
  51. 51.
    Prosser RA, McArthur AJ, Gillette MU. cGMP induces phase shifts of a mammalian circadian pacemaker at night, in antiphase to cAMP effects. Proc Natl Acad Sci USA. 1989;86:6812–5.PubMedGoogle Scholar
  52. 52.
    Revermann M, Maronde E, Ruth P, Korf HW. Protein kinase G I immunoreaction is colocalized with arginine-vasopressin immunoreaction in the rat suprachiasmatic nucleus. Neurosci Lett. 2002;334:119–22.PubMedGoogle Scholar
  53. 53.
    Weber ET, Gannon RL, Rea MA. cGMP-dependent protein kinase inhibitor blocks light-induced phase advances of circadian rhythms in vivo. Neurosci Lett. 1995;197:227–30.PubMedGoogle Scholar
  54. 54.
    Hamada T, Liou SY, Fukushima T, Maruyama T, Watanabe S, Mikoshiba K, et al. The role of inositol trisphosphate-induced Ca2+ release from IP3-receptor in the rat suprachiasmatic nucleus on circadian entrainment mechanism. Neurosci Lett. 1999;263:125–8.PubMedGoogle Scholar
  55. 55.
    Obrietan K, Impey S, Storm DR. Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat Neurosci. 1998;1:693–700.PubMedGoogle Scholar
  56. 56.
    Lee HS, Nelms JL, Nguyen M, Silver R, Lehman MN. The eye is necessary for a circadian rhythm in the suprachiasmatic nucleus. Nat Neurosci. 2003;6:111–2.PubMedGoogle Scholar
  57. 57.
    Nakaya M, Sanada K, Fukada Y. Spatial and temporal regulation of mitogen-activated protein kinase phosphorylation in the mouse suprachiasmatic nucleus. Biochem Biophys Res Commun. 2003;305:494–501.PubMedGoogle Scholar
  58. 58.
    Butcher GQ, Lee B, Obrietan K. Temporal regulation of light-induced extracellular signal-regulated kinase activation in the suprachiasmatic nucleus. J Neurophysiol. 2003;90:3854–63.PubMedGoogle Scholar
  59. 59.
    Coogan AN, Piggins HD. Circadian and photic regulation of phosphorylation of ERK1/2 and Elk-1 in the suprachiasmatic nuclei of the Syrian hamster. J Neurosci. 2003;23:3085–93.PubMedGoogle Scholar
  60. 60.
    Dziema H, Oatis B, Butcher GQ, Yates R, Hoyt KR, Obrietan K. The ERK/MAP kinase pathway couples light to immediate-early gene expression in the suprachiasmatic nucleus. Eur J NeuroSci. 2003;17:1617–27.PubMedGoogle Scholar
  61. 61.
    Meyer-Spasche A, Piggins HD. Vasoactive intestinal polypeptide phase-advances the rat suprachiasmatic nuclei circadian pacemaker in vitro via protein kinase A and mitogen-activated protein kinase. Neurosci Lett. 2004;358:91–4.PubMedGoogle Scholar
  62. 62.
    Hainich EC, Pizzio GA, Golombek DA. Constitutive activation of the ERK-MAPK pathway in the suprachiasmatic nuclei inhibits circadian resetting. FEBS Lett. 2006;580:6665–8.PubMedGoogle Scholar
  63. 63.
    Chen Z, Gibson TB, Robinson F, Silvestro L, Pearson G, Xu B, et al. MAP kinases. Chem Rev. 2001;101:2449–76.PubMedGoogle Scholar
  64. 64.
    Bina KG, Rusak B. Nerve growth factor phase shifts circadian activity rhythms in Syrian hamsters. Neurosci Lett. 1996;206:97–100.PubMedGoogle Scholar
  65. 65.
    Pizzio GA, Golombek DA. Photic regulation of map kinase phosphatases MKP1/2 and MKP3 in the hamster suprachiasmatic nuclei. J Mol Neurosci. 2008;34:187–92.PubMedGoogle Scholar
  66. 66.
    Doi M, Cho S, Yujnovsky I, Hirayama J, Cermakian N, Cato AC, et al. Light-inducible and clock-controlled expression of MAP kinase phosphatase 1 in mouse central pacemaker neurons. J Biol Rhythms. 2007;22:127–39.PubMedGoogle Scholar
  67. 67.
    Ginty D, Kornhauser J, Thompson M, Bading H, Mayo K, Takahashi J, et al. Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 1993;260:238–41.PubMedGoogle Scholar
  68. 68.
    von Gall C, Duffield GE, Hastings MH, Kopp MD, Dehghani F, Korf HW, et al. CREB in the mouse SCN: a molecular interface coding the phase-adjusting stimuli light, glutamate, PACAP, and melatonin for clockwork access. J Neurosci. 1998;18:10389–97.Google Scholar
  69. 69.
    Tischkau SA, Mitchell JW, Tyan SH, Buchanan GF, Gillette MU. Ca2+/cAMP response element-binding protein (CREB)-dependent activation of Per1 is required for light-induced signaling in the suprachiasmatic nucleus circadian clock. J Biol Chem. 2003;278:718–23.PubMedGoogle Scholar
  70. 70.
    Antle MC, Kriegsfeld LJ, Silver R. Signaling within the master clock of the brain: localized activation of mitogen-activated protein kinase by gastrin-releasing peptide. J Neurosci. 2005;25:2447–54.PubMedGoogle Scholar
  71. 71.
    Piggins HD, Antle MC, Rusak B. Neuropeptides phase shift the mammalian circadian pacemaker. J Neurosci. 1995;15:5612–22.PubMedGoogle Scholar
  72. 72.
    Gamble KL, Allen GC, Zhou T, McMahon DG. Gastrin-releasing peptide mediates light-like resetting of the suprachiasmatic nucleus circadian pacemaker through cAMP response element-binding protein and Per1 activation. J Neurosci. 2007;27:12078–87.PubMedGoogle Scholar
  73. 73.
    Sassone-Corsi P. Coupling gene expression to cAMP signalling: role of CREB and CREM. Int J Biochem Cell Biol. 1998;30:27–38.PubMedGoogle Scholar
  74. 74.
    Schwartz WJ, Aronin N, Sassone-Corsi P. Photoinducible and rhythmic ICER-CREM immunoreactivity in the rat suprachiasmatic nucleus. Neurosci Lett. 2005;385:87–91.PubMedGoogle Scholar
  75. 75.
    Maldonado R, Smadja C, Mazucchelli C, Sassone-Corsi P. Altered emotional and locomotor responses in mice deficient in the transcription factor CREM. Proc Natl Acad Sci USA. 1999;96:14094–9.PubMedGoogle Scholar
  76. 76.
    Quintero JE, Kuhlman SJ, McMahon DG. The biological clock nucleus: a multiphasic oscillator network regulated by light. J Neurosci. 2003;23:8070–6.PubMedGoogle Scholar
  77. 77.
    Jobst EE, Allen CN. Calbindin neurons in the hamster suprachiasmatic nucleus do not exhibit a circadian variation in spontaneous firing rate. Eur J NeuroSci. 2002;16:2469–74.PubMedGoogle Scholar
  78. 78.
    Antle MC. The circadian clock: Physiology, genes, and disease. In: Tombran-Tink J, Barnstable CJ, editors. Visual transduction and non-visual light perception. Totowa: Humana; 2008. p. 481–99.Google Scholar
  79. 79.
    Moore RY, Speh JC, Leak RK. Suprachiasmatic nucleus organization. Cell Tissue Res. 2002;309:89–98.PubMedGoogle Scholar
  80. 80.
    LeSauter J, Kriegsfeld LJ, Hon J, Silver R. Calbindin-D(28K) cells selectively contact intra-SCN neurons. Neuroscience 2002;111:575–85.PubMedGoogle Scholar
  81. 81.
    Bryant DN, LeSauter J, Silver R, Romero MT. Retinal innervation of calbindin-D28K cells in the hamster suprachiasmatic nucleus: ultrastructural characterization. J Biol Rhythms. 2000;15:103–11.PubMedGoogle Scholar
  82. 82.
    Dardente H, Poirel VJ, Klosen P, Pevet P, Masson-Pevet M. Per and neuropeptide expression in the rat suprachiasmatic nuclei: compartmentalization and differential cellular induction by light. Brain Res. 2002;958:261–71.PubMedGoogle Scholar
  83. 83.
    Silver R, Romero MT, Besmer HR, Leak R, Nunez JM, LeSauter J. Calbindin-D28K cells in the hamster SCN express light-induced Fos. NeuroReport 1996;7:1224–8.PubMedGoogle Scholar
  84. 84.
    Kawamoto K, Nagano M, Kanda F, Chihara K, Shigeyoshi Y, Okamura H. Two types of VIP neuronal components in rat suprachiasmatic nucleus. J Neurosci Res. 2003;74:852–7.PubMedGoogle Scholar
  85. 85.
    Romijn HJ, Sluiter AA, Pool CW, Wortel J, Buijs RM. Differences in colocalization between Fos and PHI, GRP, VIP and VP in neurons of the rat suprachiasmatic nucleus after a light stimulus during the phase delay versus the phase advance period of the night. J Comp Neurol. 1996;372:1–8.PubMedGoogle Scholar
  86. 86.
    Romijn HJ, Sluiter AA, Pool CW, Wortel J, Buijs RM. Evidence from confocal fluorescence microscopy for a dense, reciprocal innervation between AVP-, somatostatin-, VIP/PHI-, GRP-, and VIP/PHI/GRP-immunoreactive neurons in the rat suprachiasmatic nucleus. Eur J NeuroSci. 1997;9:2613–23.PubMedGoogle Scholar
  87. 87.
    van den Pol AN, 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;252:507–21.PubMedGoogle Scholar
  88. 88.
    Leak RK, Card JP, Moore RY. Suprachiasmatic pacemaker organization analyzed by viral transynaptic transport. Brain Res. 1999;819:23–32.PubMedGoogle Scholar
  89. 89.
    Leak RK, Moore RY. Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol. 2001;433:312–34.PubMedGoogle Scholar
  90. 90.
    Colwell CS. Rhythmic coupling among cells in the suprachiasmatic nucleus. J Neurobiol. 2000;43:379–88.PubMedGoogle Scholar
  91. 91.
    Shibata S, Tsuneyoshi A, Hamada T, Tominaga K, Watanabe S. Effect of substance P on circadian rhythms of firing activity and the 2-deoxyglucose uptake in the rat suprachiasmatic nucleus in vitro. Brain Res. 1992;597:257–63.PubMedGoogle Scholar
  92. 92.
    Challet E, Dugovic C, Turek FW, Van Olivier R. The selective neurokinin 1 receptor antagonist R116301 modulates photic responses of the hamster circadian system. Neuropharmacology 2001;40:408–15.PubMedGoogle Scholar
  93. 93.
    Challet E, Naylor E, Metzger JM, MacIntyre DE, Turek FW. An NK1 receptor antagonist affects the circadian regulation of locomotor activity in golden hamsters. Brain Res. 1998;800:32–9.PubMedGoogle Scholar
  94. 94.
    Abe H, Honma S, Shinohara K, Honma K. Substance P receptor regulates the photic induction of Fos-like protein in the suprachiasmatic nucleus of Syrian hamsters. Brain Res. 1996;708:135–42.PubMedGoogle Scholar
  95. 95.
    Piggins HD, Rusak B. Effects of microinjections of substance P into the suprachiasmatic nucleus region on hamster wheel-running rhythms. Brain Res Bull. 1997;42:451–5.PubMedGoogle Scholar
  96. 96.
    Sterniczuk R, Colijn MA, Nunez M, Antle MC. Investigating the role of substance P in photic responses of the circadian system: individual and combined actions with gastrin-releasing peptide. Neuropharmacology, doi:10.1016/j.neuropharm.2009.06.011.
  97. 97.
    Tanaka M, Hayashi S, Tamada Y, Ikeda T, Hisa Y, Takamatsu T, et al. Direct retinal projections to GRP neurons in the suprachiasmatic nucleus of the rat. NeuroReport 1997;8:2187–91.PubMedCrossRefGoogle Scholar
  98. 98.
    Aioun J, Chambille I, Peytevin J, Martinet L. Neurons containing gastrin-releasing peptide and vasoactive intestinal polypeptide are involved in the reception of the photic signal in the suprachiasmatic nucleus of the Syrian hamster: an immunocytochemical ultrastructural study. Cell Tissue Res. 1998;291:239–53.PubMedGoogle Scholar
  99. 99.
    McArthur AJ, Coogan AN, Ajpru S, Sugden D, Biello SM, Piggins HD. Gastrin-releasing peptide phase-shifts suprachiasmatic nuclei neuronal rhythms in vitro. J Neurosci. 2000;20:5496–502.PubMedGoogle Scholar
  100. 100.
    Piggins HD, Cutler DJ, Rusak B. Effects of ionophoretically applied bombesin-like peptides on hamster suprachiasmatic nucleus neurons in vitro. Eur J Pharmacol. 1994;271:413–9.PubMedGoogle Scholar
  101. 101.
    Piggins HD, Goguen D, Rusak B. Gastrin-releasing peptide induces c-Fos in the hamster suprachiasmatic nucleus. Neurosci Lett. 2005;384:205–10.PubMedGoogle Scholar
  102. 102.
    Kallingal GJ, Mintz EM. Glutamatergic activity modulates the phase-shifting effects of gastrin-releasing peptide and light. Eur J NeuroSci. 2006;24:2853–8.PubMedGoogle Scholar
  103. 103.
    Karatsoreos IN, Romeo RD, McEwen BS, Silver R. Diurnal regulation of the gastrin-releasing peptide receptor in the mouse circadian clock. Eur J NeuroSci. 2006;23:1047–53.PubMedGoogle Scholar
  104. 104.
    Aida R, Moriya T, Araki M, Akiyama M, Wada K, Wada E, et al. Gastrin-releasing peptide mediates photic entrainable signals to dorsal subsets of suprachiasmatic nucleus via induction of Period gene in mice. Mol Pharmacol. 2002;61:26–34.PubMedGoogle Scholar
  105. 105.
    Tanaka M, Ichitani Y, Okamura H, Tanaka Y, Ibata Y. The direct retinal projection to VIP neuronal elements in the rat SCN. Brain Res Bull. 1993;31:637–40.PubMedGoogle Scholar
  106. 106.
    Kalamatianos T, Kallo I, Piggins HD, Coen CW. Expression of VIP and/or PACAP receptor mRNA in peptide synthesizing cells within the suprachiasmatic nucleus of the rat and in its efferent target sites. J Comp Neurol. 2004;475:19–35.PubMedGoogle Scholar
  107. 107.
    Kallo I, Kalamatianos T, Wiltshire N, Shen S, Sheward WJ, Harmar AJ, et al. Transgenic approach reveals expression of the VPAC2 receptor in phenotypically defined neurons in the mouse suprachiasmatic nucleus and in its efferent target sites. Eur J NeuroSci. 2004;19:2201–11.PubMedGoogle Scholar
  108. 108.
    Reed HE, Meyer-Spasche A, Cutler DJ, Coen CW, Piggins HD. Vasoactive intestinal polypeptide (VIP) phase-shifts the rat suprachiasmatic nucleus clock in vitro. Eur J NeuroSci. 2001;13:839–43.PubMedGoogle Scholar
  109. 109.
    Nielsen HS, Hannibal J, Fahrenkrug J. Vasoactive intestinal polypeptide induces per1 and per2 gene expression in the rat suprachiasmatic nucleus late at night. Eur J NeuroSci. 2002;15:570–4.PubMedGoogle Scholar
  110. 110.
    Watanabe K, Vanecek J, Yamaoka S. In vitro entrainment of the circadian rhythm of vasopressin-releasing cells in suprachiasmatic nucleus by vasoactive intestinal polypeptide. Brain Res. 2000;877:361–6.PubMedGoogle Scholar
  111. 111.
    Reed HE, Cutler DJ, Brown TM, Brown J, Coen CW, Piggins HD. Effects of vasoactive intestinal polypeptide on neurones of the rat suprachiasmatic nuclei in vitro. J Neuroendocrinol. 2002;14:639–46.PubMedGoogle Scholar
  112. 112.
    Colwell CS, Michel S, Itri J, Rodriguez W, Tam J, Lelievre V, et al. Disrupted circadian rhythms in VIP- and PHI-deficient mice. Am J Physiol Regul Integr Comp Physiol. 2003;285:R939–49.PubMedGoogle Scholar
  113. 113.
    Aton SJ, Colwell CS, Harmar AJ, Waschek J, Herzog ED. Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat Neurosci. 2005;8:476–83.PubMedGoogle Scholar
  114. 114.
    Harmar AJ, Marston HM, Shen S, Spratt C, West KM, Sheward WJ, et al. The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 2002;109:497–508.PubMedGoogle Scholar
  115. 115.
    Hughes AT, Fahey B, Cutler DJ, Coogan AN, Piggins HD. Aberrant gating of photic input to the suprachiasmatic circadian pacemaker of mice lacking the VPAC2 receptor. J Neurosci. 2004;24:3522–6.PubMedGoogle Scholar
  116. 116.
    Ciarleglio CM, Gamble KL, Axley JC, Strauss BR, Cohen JY, Colwell CS, et al. Population encoding by circadian clock neurons organizes circadian behavior. J Neurosci. 2009;29:1670–6.PubMedGoogle Scholar
  117. 117.
    Maywood ES, Reddy AB, Wong GK, O’Neill JS, O’Brien JA, McMahon DG, et al. Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Curr Biol. 2006;16:599–605.PubMedGoogle Scholar
  118. 118.
    Brown TM, Hughes AT, Piggins HD. Gastrin-releasing peptide promotes suprachiasmatic nuclei cellular rhythmicity in the absence of vasoactive intestinal polypeptide-VPAC2 receptor signaling. J Neurosci. 2005;25:11155–64.PubMedGoogle Scholar
  119. 119.
    Castel M, Morris JF. Morphological heterogeneity of the GABAergic network in the suprachiasmatic nucleus, the brain’s circadian pacemaker. J Anat. 2000;196(Pt 1):1–13.PubMedGoogle Scholar
  120. 120.
    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.PubMedGoogle Scholar
  121. 121.
    Choi HJ, Lee CJ, Schroeder A, Kim YS, Jung SH, Kim JS, et al. Excitatory actions of GABA in the suprachiasmatic nucleus. J Neurosci. 2008;28:5450–9.PubMedGoogle Scholar
  122. 122.
    Albus H, Vansteensel MJ, Michel S, Block GD, Meijer JH. A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol. 2005;15:886–93.PubMedGoogle Scholar
  123. 123.
    Colwell CS. Circadian modulation of calcium levels in cells in the suprachiasmatic nucleus. Eur J NeuroSci. 2000;12:571–6.PubMedGoogle Scholar
  124. 124.
    Liu C, Reppert SM. GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 2000;25:123–8.PubMedGoogle Scholar
  125. 125.
    Ehlen JC, Novak CM, Karom MC, Gamble KL, Albers HE. Interactions of GABA A receptor activation and light on period mRNA expression in the suprachiasmatic nucleus. J Biol Rhythms. 2008;23:16–25.PubMedGoogle Scholar
  126. 126.
    Novak CM, Ehlen JC, Huhman KL, Albers HE. GABA(B) receptor activation in the suprachiasmatic nucleus of diurnal and nocturnal rodents. Brain Res Bull. 2004;63:531–5.PubMedGoogle Scholar
  127. 127.
    Ehlen JC, Paul KN. Regulation of light’s action in the mammalian circadian clock: role of the extrasynaptic GABAA receptor. Am J Physiol Regul Integr Comp Physiol. 2009;296:R1606–12.PubMedGoogle Scholar
  128. 128.
    Mintz EM, Jasnow AM, Gillespie CF, Huhman KL, Albers HE. GABA interacts with photic signaling in the suprachiasmatic nucleus to regulate circadian phase shifts. Neuroscience 2002;109:773–8.PubMedGoogle Scholar
  129. 129.
    Gillespie CF, Huhman KL, Babagbemi TO, Albers HE. Bicuculline increases and muscimol reduces the phase-delaying effects of light and VIP/PHI/GRP in the suprachiasmatic region. J Biol Rhythms. 1996;11:137–44.PubMedGoogle Scholar
  130. 130.
    Gillespie CF, Mintz EM, Marvel CL, Huhman KL, Albers HE. GABA(A) and GABA(B) agonists and antagonists alter the phase-shifting effects of light when microinjected into the suprachiasmatic region. Brain Res. 1997;759:181–9.PubMedGoogle Scholar
  131. 131.
    Gillespie CF, Van Der Beek EM, Mintz EM, Mickley NC, Jasnow AM, Huhman KL, et al. GABAergic regulation of light-induced c-Fos immunoreactivity within the suprachiasmatic nucleus. J Comp Neurol. 1999;411:683–92.PubMedGoogle Scholar
  132. 132.
    Reuss S, Decker K, Rosseler L, Layes E, Schollmayer A, Spessert R. Nitric oxide synthase in the hypothalamic suprachiasmatic nucleus of rat: evidence from histochemistry, immunohistochemistry and western blot; and colocalization with VIP. Brain Res. 1995;695:257–62.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Michael C. Antle
    • 1
    • 2
    • 3
  • Victoria M. Smith
    • 1
    • 2
  • Roxanne Sterniczuk
    • 1
    • 2
  • Glenn R. Yamakawa
    • 1
    • 2
  • Brooke D. Rakai
    • 1
    • 2
  1. 1.Department of PsychologyUniversity of CalgaryCalgaryCanada
  2. 2.Hotchkiss Brain InstituteUniversity of CalgaryCalgaryCanada
  3. 3.Physiology & PharmacologyUniversity of CalgaryCalgaryCanada

Personalised recommendations