Circadian Organization of the Vertebrate Retina

Chapter
Part of the Springer Series in Vision Research book series (SSVR, volume 1)

Abstract

Our vision is different at different times of the day because our retina works differently at different times of day. These rhythms in the visual function are not just simple responses to the daily light–dark cycle but are in fact the overt expression of an endogenous, self-sustained circadian clock in the retina that drives many rhythms in retinal physiology and metabolism. Thus, the vertebrate retina is both a sensory organ and a 24-h biological clock. Here, we will explore the molecular, cellular, and neurochemical organization of the retinal circadian clock.

Keywords

Circadian Retina Dopamine Melatonin Clock gene Gene expression Photoreceptor Ganglion cell Vision 

References

  1. 1.
    Bassi CJ, Powers MK. Daily fluctuations in the detectability of dim lights by humans. Physiol Behav. 1986;38(6):871–7.PubMedGoogle Scholar
  2. 2.
    Lotze M, Treutwein B, Roenneberg T. Daily rhythm of vigilance assessed by temporal resolution of the visual system. Vision Res. 2000;40(25):3467–73.PubMedGoogle Scholar
  3. 3.
    Nozaki S, Wakakura M, Ishikawa S. Circadian rhythm of human electroretinogram. Jpn J Ophthalmol. 1983;27(2):346–52.PubMedGoogle Scholar
  4. 4.
    Hankins MW, Jones RJ, Ruddock KH. Diurnal variation in the b-wave implicit time of the human electroretinogram. Vis Neurosci. 1998;15(1):55–67.PubMedGoogle Scholar
  5. 5.
    Nordin S, Lötsch J, Murphy C, Hummel T, Kobal G. Circadian rhythm and desensitization in chemosensory event-related potentials in response to odorous and painful stimuli. Psychophysiology. 2003;40(4):612–9.PubMedGoogle Scholar
  6. 6.
    Lotze M, Wittmann M, von Steinbüchel N, Pöppel E, Roenneberg T. Daily rhythm of temporal resolution in the auditory system. Cortex. 1999;35(1):89–100.PubMedGoogle Scholar
  7. 7.
    Storch K-F, Paz C, Signorovitch J, Raviola E, Pawlyk B, Li T, et al. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell. 2007; 130(4):730–41.PubMedCentralPubMedGoogle Scholar
  8. 8.
    Cameron MA, Barnard AR, Hut RA, Bonnefont X, van der Horst GT, Hankins MW, et al. Electroretinography of wild-type and Cry mutant mice reveals circadian tuning of photopic and mesopic retinal responses. J Biol Rhythms. 2008;23(6):489–501.PubMedGoogle Scholar
  9. 9.
    Granados-Fuentes D, Tseng A, Herzog ED. A circadian clock in the olfactory bulb controls olfactory responsivity. J Neurosci. 2006;26(47):12219–25.PubMedGoogle Scholar
  10. 10.
    Krishnan B, Dryer SE, Hardin PE. Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature. 1999;400(6742):375–8.PubMedGoogle Scholar
  11. 11.
    Barlow Jr RB. Circadian rhythms in the Limulus visual system. J Neurosci. 1983;3(4): 856–70.PubMedGoogle Scholar
  12. 12.
    Page TL, Koelling E. Circadian rhythm in olfactory response in the antennae controlled by the optic lobe in the cockroach. J Insect Physiol. 2003;49(7):697–707.PubMedGoogle Scholar
  13. 13.
    Tanoue S, Krishnan P, Krishnan B, Dryer SE, Hardin PE. Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr Biol. 2004; 14(8):638–49.PubMedGoogle Scholar
  14. 14.
    Besharse JC, Iuvone PM. Circadian clock in Xenopus eye controlling retinal serotonin N-acetyltransferase. Nature. 1983;305(5930):133–5.PubMedGoogle Scholar
  15. 15.
    Tosini G, Menaker M. Circadian rhythms in cultured mammalian retina. Science. 1996; 272(5260):419–21.PubMedGoogle Scholar
  16. 16.
    Tosini G, Menaker M. The clock in the mouse retina: melatonin synthesis and photoreceptor degeneration. Brain Res. 1998;789(2):221–8.PubMedGoogle Scholar
  17. 17.
    Sakamoto K, Liu C, Tosini G. Circadian rhythms in the retina of rats with photoreceptor degeneration. J Neurochem. 2004;90(4):1019–24.PubMedGoogle Scholar
  18. 18.
    Kaneko M, Hernandez-Borsetti N, Cahill GM. Diversity of zebrafish peripheral oscillators revealed by luciferase reporting. Proc Natl Acad Sci U S A. 2006;103(39):14614–9.PubMedCentralPubMedGoogle Scholar
  19. 19.
    Tosini G, Menaker M. Multioscillatory circadian organization in a vertebrate, Iguana iguana. J Neurosci. 1998;18(3):1105–14.PubMedGoogle Scholar
  20. 20.
    Steele CT, Tosini G, Siopes T, Underwood H. Time keeping by the quail’s eye: circadian regulation of melatonin production. Gen Comp Endocrinol. 2006;145(3):232–6.PubMedGoogle Scholar
  21. 21.
    Doyle SE, Grace MS, McIvor W, Menaker M. Circadian rhythms of dopamine in mouse retina: the role of melatonin. Vis Neurosci. 2002;19(5):593–601.PubMedGoogle Scholar
  22. 22.
    Nir I, Haque R, Iuvone PM. Diurnal metabolism of dopamine in the mouse retina. Brain Res. 2000;870(1–2):118–25.PubMedGoogle Scholar
  23. 23.
    Jaliffa CO, Saenz D, Resnik E, Keller Sarmiento MI, Rosenstein RE. Circadian activity of the GABAergic system in the golden hamster retina. Brain Res. 2001;912(2):195–202.PubMedGoogle Scholar
  24. 24.
    Dmitriev AV, Mangel SC. Circadian clock regulation of pH in the rabbit retina. J Neurosci. 2001;21(8):2897–902.PubMedGoogle Scholar
  25. 25.
    Teirstein PS, Goldman AI, O’Brien PJ. Evidence for both local and central regulation of rat rod outer segment disc shedding. Invest Ophthalmol Vis Sci. 1980;19(11):1268–73.PubMedGoogle Scholar
  26. 26.
    Tosini G, Kasamatsu M, Sakamoto K. Clock gene expression in the rat retina: effects of lighting conditions and photoreceptor degeneration. Brain Res. 2007;1159:134–40.PubMedCentralPubMedGoogle Scholar
  27. 27.
    Ruan G-X, Allen GC, Yamazaki S, McMahon DG. An autonomous circadian clock in the inner mouse retina regulated by dopamine and GABA. PLoS Biol. 2008;6(10):e249.PubMedGoogle Scholar
  28. 28.
    Ruan G-X, Zhang D-Q, Zhou T, Yamazaki S, McMahon DG. Circadian organization of the mammalian retina. Proc Natl Acad Sci U S A. 2006;103(25):9703–8.PubMedCentralPubMedGoogle Scholar
  29. 29.
    Organisciak DT, Darrow RM, Barsalou L, Kutty RK, Wiggert B. Circadian-dependent retinal light damage in rats. Invest Ophthalmol Vis Sci. 2000;41(12):3694–701.PubMedGoogle Scholar
  30. 30.
    Grewal R, Organisciak D, Wong P. Factors underlying circadian dependent susceptibility to light induced retinal damage. Adv Exp Med Biol. 2006;572(3):411–6.Google Scholar
  31. 31.
    Ogilvie JM, Speck JD. Dopamine has a critical role in photoreceptor degeneration in the rd mouse. Neurobiol Dis. 2002;10(1):33–40.PubMedGoogle Scholar
  32. 32.
    Baba K, Pozdeyev N, Mazzoni F, Contreras-Alcantara S, Liu C, Kasamatsu M, et al. Melatonin modulates visual function and cell viability in the mouse retina via the MT1 melatonin receptor. Proc Natl Acad Sci U S A. 2009;106(35):15043–8.PubMedCentralPubMedGoogle Scholar
  33. 33.
    Iuvone PM, Tigges M, Stone RA, Lambert S, Laties AM. Effects of apomorphine, a dopamine receptor agonist, on ocular refraction and axial elongation in a primate model of myopia. Invest Ophthalmol Vis Sci. 1991;32(5):1674–7.PubMedGoogle Scholar
  34. 34.
    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(2):111–2.PubMedGoogle Scholar
  35. 35.
    Takahashi JS, Hong HK, Ko CH, McDearmon EL. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet. 2008; 9(10):764–75.PubMedCentralPubMedGoogle Scholar
  36. 36.
    Bae K, Jin X, Maywood ES, Hastings MH, Reppert SM, Weaver DR. Differential functions of mPer1, mPer2, and mPer3 in the SCN circadian clock. Neuron. 2001;30(2):525–36.PubMedGoogle Scholar
  37. 37.
    Vitaterna MH, Selby CP, Todo T, Niwa H, Thompson C, Fruechte EM, et al. Differential regulation of mammalian period genes and circadian rhythmicity by cryptochromes 1 and 2. Proc Natl Acad Sci U S A. 1999;96(21):12114–9.PubMedCentralPubMedGoogle Scholar
  38. 38.
    van der Horst GT, Muijtjens M, Kobayashi K, Takano R, Kanno S, Takao M, et al. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature. 1999; 398(6728):627–30.PubMedGoogle Scholar
  39. 39.
    Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, et al. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell. 2000; 103(7):1009–17.PubMedCentralPubMedGoogle Scholar
  40. 40.
    Zhu H, LaRue S, Whiteley A, Steeves TD, Takahashi JS, Green CB. The Xenopus clock gene is constitutively expressed in retinal photoreceptors. Brain Res Mol Brain Res. 2000; 75(2):303–8.PubMedGoogle Scholar
  41. 41.
    Besharse JC, Zhuang M, Freeman K, Fogerty J. Regulation of photoreceptor Per1 and Per2 by light, dopamine and a circadian clock. Eur J Neurosci. 2004;20(1):167–74.PubMedGoogle Scholar
  42. 42.
    Zhuang M, Wang Y, Steenhard BM, Besharse JC. Differential regulation of two period genes in the Xenopus eye. Brain Res Mol Brain Res. 2000;82(1–2):52–64.PubMedGoogle Scholar
  43. 43.
    Zhu H, Green CB. Three cryptochromes are rhythmically expressed in Xenopus laevis retinal photoreceptors. Mol Vis. 2001;7:210–5.PubMedGoogle Scholar
  44. 44.
    Bailey MJ, Chong NW, Xiong J, Cassone VM. Chickens’ Cry2: molecular analysis of an avian cryptochrome in retinal and pineal photoreceptors. FEBS Lett. 2002;513(2–3):169–74.PubMedGoogle Scholar
  45. 45.
    Haque R, Chaurasia SS, Wessel 3rd JH, Iuvone PM. Dual regulation of cryptochrome 1 mRNA expression in chicken retina by light and circadian oscillators. Neuroreport. 2002; 13(17):2247–51.PubMedGoogle Scholar
  46. 46.
    Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, et al. Role of the CLOCK protein in the mammalian circadian mechanism. Science. 1998;280(5369):1564–9.PubMedGoogle Scholar
  47. 47.
    Miyamoto Y, Sancar A. Vitamin B2-based blue-light photoreceptors in the retinohypothalamic tract as the photoactive pigments for setting the circadian clock in mammals. Proc Natl Acad Sci U S A. 1998;95(11):6097–102.PubMedCentralPubMedGoogle Scholar
  48. 48.
    Namihira M, Honma S, Abe H, Masubuchi S, Ikeda M, Honmaca K. Circadian pattern, light responsiveness and localization of rPer1 and rPer2 gene expression in the rat retina. Neuroreport. 2001;12(3):471–5.PubMedGoogle Scholar
  49. 49.
    Witkovsky P, Veisenberger E, LeSauter J, Yan L, Johnson M, Zhang D-Q, et al. Cellular location and circadian rhythm of expression of the biological clock gene Period 1 in the mouse retina. J Neurosci. 2003;23(20):7670–6.PubMedCentralPubMedGoogle Scholar
  50. 50.
    Thompson CL, Rickman CB, Shaw SJ, Ebright JN, Kelly U, Sancar A, et al. Expression of the blue-light receptor cryptochrome in the human retina. Invest Ophthalmol Vis Sci. 2003;44(10):4515–21.PubMedGoogle Scholar
  51. 51.
    Namihira M, Honma S, Abe H, Tanahashi Y, Ikeda M, Honma K. Circadian rhythms and light responsiveness of mammalian clock gene, Clock and BMAL1, transcripts in the rat retina. Neurosci Lett. 1999;271(1):1–4.PubMedGoogle Scholar
  52. 52.
    Baba K, Sengupta A, Tosini M, Contreras-Alcantara S, Tosini G. Circadian regulation of the PERIOD 2::LUCIFERASE bioluminescence rhythm in the mouse retinal pigment epithelium-choroid. Mol Vis. 2010;16:2605–11.PubMedGoogle Scholar
  53. 53.
    Hastings MH, Reddy AB, McMahon DG, Maywood ES. Analysis of circadian mechanisms in the suprachiasmatic nucleus by transgenesis and biolistic transfection. Methods Enzymol. 2005;393:579–92.PubMedGoogle Scholar
  54. 54.
    Ruan G-X, Gamble KL, Risner ML, Young LA, McMahon DG. Divergent roles of clock genes in retinal and suprachiasmatic nucleus circadian oscillators. PLoS One. 2012; 7(6):e38985.PubMedCentralPubMedGoogle Scholar
  55. 55.
    Liu AC, Welsh DK, Ko CH, Tran HG, Zhang EE, Priest AA, et al. Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell. 2007;129(3): 605–16.PubMedCentralPubMedGoogle Scholar
  56. 56.
    Pendergast JS, Friday RC, Yamazaki S. Distinct functions of Period2 and Period3 in the mouse circadian system revealed by in vitro analysis. PLoS One. 2010;5(1):e8552.PubMedCentralPubMedGoogle Scholar
  57. 57.
    Cahill GM, Besharse JC. Circadian clock functions localized in Xenopus retinal photoreceptors. Neuron. 1993;10(4):573–7.PubMedGoogle Scholar
  58. 58.
    Pierce ME, Sheshberadaran H, Zhang Z, Fox LE, Applebury ML, Takahashi JS. Circadian regulation of iodopsin gene expression in embryonic photoreceptors in retinal cell culture. Neuron. 1993;10(4):579–84.PubMedGoogle Scholar
  59. 59.
    Ko GY, Ko ML, Dryer SE. Circadian regulation of cGMP-gated channels of vertebrate cone photoreceptors: role of cAMP and Ras. J Neurosci. 2004;24(6):1296–304.PubMedCentralPubMedGoogle Scholar
  60. 60.
    Hayasaka N, LaRue SI, Green CB. In vivo disruption of Xenopus CLOCK in the retinal photoreceptor cells abolishes circadian melatonin rhythmicity without affecting its production levels. J Neurosci. 2002;22(5):1600–7.PubMedGoogle Scholar
  61. 61.
    Hayasaka N, LaRue SI, Green CB. Differential contribution of rod and cone circadian clocks in driving retinal melatonin rhythms in Xenopus. PLoS One. 2010;5(12):e15599.PubMedCentralPubMedGoogle Scholar
  62. 62.
    Tosini G. Melatonin circadian rhythm in the retina of mammals. Chronobiol Int. 2000; 17(5):599–612.PubMedGoogle Scholar
  63. 63.
    Liu X, Zhang Z, Ribelayga CP. Heterogeneous expression of the core circadian clock proteins among neuronal cell types in mouse retina. PLoS One. 2012;7(11):e50602.PubMedCentralPubMedGoogle Scholar
  64. 64.
    Dorenbos R, Contini M, Hirasawa H, Gustincich S, Raviola E. Expression of circadian clock genes in retinal dopaminergic cells. Vis Neurosci. 2007;24(4):573–80.PubMedGoogle Scholar
  65. 65.
    Tosini G, Davidson AJ, Fukuhara C, Kasamatsu M, Castanon-Cervantes O. Localization of a circadian clock in mammalian photoreceptors. FASEB J. 2007;21(14):3866–71.PubMedCentralPubMedGoogle Scholar
  66. 66.
    Sandu C, Hicks D, Felder-Schmittbuhl M-P. Rat photoreceptor circadian oscillator strongly relies on lighting conditions. Eur J Neurosci. 2011;34(3):507–16.PubMedGoogle Scholar
  67. 67.
    Gustincich S, Contini M, Gariboldi M, Puopolo M, Kadota K, Bono H, et al. Gene discovery in genetically labeled single dopaminergic neurons of the retina. Proc Natl Acad Sci U S A. 2004;101(14):5069–74.PubMedCentralPubMedGoogle Scholar
  68. 68.
    Sengupta A, Baba K, Mazzoni F, Pozdeyev NV, Strettoi E, Iuvone PM, et al. Localization of melatonin receptor 1 in mouse retina and its role in the circadian regulation of the electroretinogram and dopamine levels. PLoS One. 2011;6(9):e24483.PubMedCentralPubMedGoogle Scholar
  69. 69.
    Jackson CR, Ruan G-X, Aseem F, Abey J, Gamble K, Stanwood G, et al. Retinal dopamine mediates multiple dimensions of light-adapted vision. J Neurosci. 2012;32(27):9359–68.PubMedCentralPubMedGoogle Scholar
  70. 70.
    Zhang D-Q, Zhou T, Ruan G-X, McMahon DG. Circadian rhythm of Period1 clock gene expression in NOS amacrine cells of the mouse retina. Brain Res. 2005;1050(1–2):101–9.PubMedGoogle Scholar
  71. 71.
    Sakamoto K, Liu C, Kasamatsu M, Pozdeyev NV, Iuvone PM, Tosini G. Dopamine regulates melanopsin mRNA expression in intrinsically photosensitive retinal ganglion cells. Eur J Neurosci. 2005;22(12):3129–36.PubMedGoogle Scholar
  72. 72.
    Sakamoto K, Liu C, Tosini G. Classical photoreceptors regulate melanopsin mRNA levels in the rat retina. J Neurosci. 2004;24(43):9693–7.PubMedGoogle Scholar
  73. 73.
    Mathes A, Engel L, Holthues H, Wolloscheck T, Spessert R. Daily profile in melanopsin transcripts depends on seasonal lighting conditions in the rat retina. J Neuroendocrinol. 2007;19(12):952–7.PubMedGoogle Scholar
  74. 74.
    Weng S, Wong KY, Berson DM. Circadian modulation of melanopsin-driven light response in rat ganglion-cell photoreceptors. J Biol Rhythms. 2009;24(5):391–402.PubMedCentralPubMedGoogle Scholar
  75. 75.
    Zele AJ, Feigl B, Smith SS, Markwell EL. The circadian response of intrinsically photosensitive retinal ganglion cells. PLoS One. 2011;6(3):e17860.PubMedCentralPubMedGoogle Scholar
  76. 76.
    Doyle SE, McIvor WE, Menaker M. Circadian rhythmicity in dopamine content of mammalian retina: role of the photoreceptors. J Neurochem. 2002;83(1):211–9.PubMedGoogle Scholar
  77. 77.
    Block GD, McMahon DG. Cellular analysis of the Bulla ocular circadian pacemaker system III. Localization of the circadian pacemaker. J Comp Physiol A. 1984;155:387–95.Google Scholar
  78. 78.
    Yamaguchi S, Isejima H, Matsuo T, Okura R, Yagita K, Kobayashi M, et al. Synchronization of cellular clocks in the suprachiasmatic nucleus. Science. 2003;302(5649):1408–12.PubMedGoogle Scholar
  79. 79.
    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(4):476–83.PubMedCentralPubMedGoogle Scholar
  80. 80.
    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(6):599–605.PubMedGoogle Scholar
  81. 81.
    Zhang D-Q, Belenky MA, Sollars PJ, Pickard GE, McMahon DG. Melanopsin mediates retrograde visual signaling in the retina. PLoS One. 2012;7(8):e42647.PubMedCentralPubMedGoogle Scholar
  82. 82.
    Zhang D-Q, Wong KY, Sollars PJ, Berson DM, Pickard GE, McMahon DG. Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. Proc Natl Acad Sci U S A. 2008;105(37):14181–6.PubMedCentralPubMedGoogle Scholar
  83. 83.
    Witkovsky P. Dopamine and retinal function. Doc Ophthalmol. 2004;108(1):17–40.PubMedGoogle Scholar
  84. 84.
    Cohen AI, Todd RD, Harmon S, O’Malley KL. Photoreceptors of mouse retinas possess D4 receptors coupled to adenylate cyclase. Proc Natl Acad Sci U S A. 1992;89(24):12093–7.PubMedCentralPubMedGoogle Scholar
  85. 85.
    Cahill GM, Besharse JC. Resetting the circadian clock in cultured Xenopus eyecups: regulation of retinal melatonin rhythms by light and D2 dopamine receptors. J Neurosci. 1991; 11(10):2959–71.PubMedGoogle Scholar
  86. 86.
    Yujnovsky I, Hirayama J, Doi M, Borrelli E, Sassone-Corsi P. Signaling mediated by the dopamine D2 receptor potentiates circadian regulation by CLOCK:BMAL1. Proc Natl Acad Sci U S A. 2006;103(16):6386–91.PubMedCentralPubMedGoogle Scholar
  87. 87.
    Morgan WW, Kamp CW. Dopaminergic amacrine neurons of rat retinas with photoreceptor degeneration continue to respond to light. Life Sci. 1980;26(19):1619–26.PubMedGoogle Scholar
  88. 88.
    Vugler AA, Redgrave P, Hewson-Stoate NJ, Greenwood J, Coffey PJ. Constant illumination causes spatially discrete dopamine depletion in the normal and degenerate retina. J Chem Neuroanat. 2007;33(1):9–22.PubMedGoogle Scholar
  89. 89.
    Cameron MA, Pozdeyev N, Vugler AA, Cooper H, Iuvone PM, Lucas RJ. Light regulation of retinal dopamine that is independent of melanopsin phototransduction. Eur J Neurosci. 2009;29(4):761–7.PubMedCentralPubMedGoogle Scholar
  90. 90.
    Qian H, Dowling JE. Novel GABA responses from rod-driven retinal horizontal cells. Nature. 1993;361(6408):162–4.PubMedGoogle Scholar
  91. 91.
    Ning K, Li L, Liao M, Liu B, Mielke JG, Chen Y, et al. Circadian regulation of GABAA receptor function by CKI epsilon-CKI delta in the rat suprachiasmatic nuclei. Nat Neurosci. 2004;7(5):489–90.PubMedGoogle Scholar
  92. 92.
    Dubocovich ML. Melatonin is a potent modulator of dopamine release in the retina. Nature. 1983;306(5945):782–4.PubMedGoogle Scholar
  93. 93.
    Klitten LL, Rath MF, Coon SL, Kim J-S, Klein DC, Møller M. Localization and regulation of dopamine receptor D4 expression in the adult and developing rat retina. Exp Eye Res. 2008;87(5):471–7.PubMedCentralPubMedGoogle Scholar
  94. 94.
    Nir I, Harrison JM, Haque R, Low MJ, Grandy DK, Rubinstein M, et al. Dysfunctional light-evoked regulation of cAMP in photoreceptors and abnormal retinal adaptation in mice lacking dopamine D4 receptors. J Neurosci. 2002;22(6):2063–73.PubMedGoogle Scholar
  95. 95.
    Pozdeyev N, Tosini G, Li L, Ali F, Rozov S, Lee RH, et al. Dopamine modulates diurnal and circadian rhythms of protein phosphorylation in photoreceptor cells of mouse retina. Eur J Neurosci. 2008;27(10):2691–700.PubMedCentralPubMedGoogle Scholar
  96. 96.
    Jackson CR, Chaurasia SS, Hwang CK, Iuvone PM. Dopamine D4 receptor activation controls circadian timing of the adenylyl cyclase 1/cyclic AMP signaling system in mouse retina. Eur J Neurosci. 2011;34(1):57–64.PubMedCentralPubMedGoogle Scholar
  97. 97.
    Jackson CR, Chaurasia SS, Zhou H, Haque R, Storm DR, Iuvone PM. Essential roles of dopamine D4 receptors and the type 1 adenylyl cyclase in photic control of cyclic AMP in photoreceptor cells. J Neurochem. 2009;109(1):148–57.PubMedCentralPubMedGoogle Scholar
  98. 98.
    Ribelayga C, Cao Y, Mangel SC. The circadian clock in the retina controls rod-cone coupling. Neuron. 2008;59(5):790–801.PubMedGoogle Scholar
  99. 99.
    Ribelayga C, Mangel SC. Absence of circadian clock regulation of horizontal cell gap junctional coupling reveals two dopamine systems in the goldfish retina. J Comp Neurol. 2003; 467(2):243–53.PubMedGoogle Scholar
  100. 100.
    Ribelayga C, Mangel SC. Tracer coupling between fish rod horizontal cells: modulation by light and dopamine but not the retinal circadian clock. Vis Neurosci. 2007;24(3):333–44.PubMedGoogle Scholar
  101. 101.
    Korenbrot JI, Fernald RD. Circadian rhythm and light regulate opsin mRNA in rod photoreceptors. Nature. 1989;337(6206):454–7.PubMedGoogle Scholar
  102. 102.
    Berson DM. Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci. 2003;26(6):314–20.PubMedGoogle Scholar
  103. 103.
    Yamazaki S, Alones V, Menaker M. Interaction of the retina with suprachiasmatic pacemakers in the control of circadian behavior. J Biol Rhythms. 2002;17(4):315–29.PubMedGoogle Scholar
  104. 104.
    Van Hook MJ, Wong KY, Berson DM. Dopaminergic modulation of ganglion-cell photoreceptors in rat. Eur J Neurosci. 2012;35(4):507–18.PubMedCentralPubMedGoogle Scholar
  105. 105.
    Manglapus MK, Iuvone PM, Underwood H, Pierce ME, Barlow RB. Dopamine mediates circadian rhythms of rod-cone dominance in the Japanese quail retina. J Neurosci. 1999; 19(10):4132–41.PubMedGoogle Scholar
  106. 106.
    Emran F, Rihel J, Adolph AR, Dowling JE. Zebrafish larvae lose vision at night. Proc Natl Acad Sci U S A. 2010;107(13):6034–9.PubMedCentralPubMedGoogle Scholar
  107. 107.
    Wang Y, Mangel SC. A circadian clock regulates rod and cone input to fish retinal cone horizontal cells. Proc Natl Acad Sci U S A. 1996;93(10):4655–60.PubMedCentralPubMedGoogle Scholar
  108. 108.
    Krizaj D, Gabriel R, Owen WG, Witkovsky P. Dopamine D2 receptor-mediated modulation of rod-cone coupling in the Xenopus retina. J Comp Neurol. 1998;398(4):529–38.PubMedCentralPubMedGoogle Scholar
  109. 109.
    Hampson EC, Vaney DI, Weiler R. Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J Neurosci. 1992;12(12):4911–22.PubMedGoogle Scholar
  110. 110.
    Ingster-Moati I, Le Coz P, Albuisson E, Fromont G, Pierron C, Grall Y, et al. [Static contrast sensitivity in idiopathic Parkinson disease]. Rev Neurol (Paris). 1996;152(12):738–43.Google Scholar
  111. 111.
    Haug BA, Trenkwalder C, Arden GB, Oertel WH, Paulus W. Visual thresholds to low-contrast pattern displacement, color contrast, and luminance contrast stimuli in Parkinson’s disease. Mov Disord. 1994;9(5):563–70.PubMedGoogle Scholar
  112. 112.
    Ikeda H, Head GM, Ellis CJ. Electrophysiological signs of retinal dopamine deficiency in recently diagnosed Parkinson’s disease and a follow up study. Vision Res. 1994;34(19): 2629–38.PubMedGoogle Scholar
  113. 113.
    Herrmann R, Heflin SJ, Hammond T, Lee B, Wang J, Gainetdinov RR, et al. Rod vision is controlled by dopamine-dependent sensitization of rod bipolar cells by GABA. Neuron. 2011;72(1):101–10.PubMedCentralPubMedGoogle Scholar
  114. 114.
    Hölter P, Kunst S, Wolloscheck T, Kelleher DK, Sticht C, Wolfrum U, et al. The retinal clock drives the expression of Kcnv2, a channel essential for visual function and cone survival. Invest Ophthalmol Vis Sci. 2012;53(11):6947–54.PubMedGoogle Scholar
  115. 115.
    Bartmann M, Schaeffel F, Hagel G, Zrenner E. Constant light affects retinal dopamine levels and blocks deprivation myopia but not lens-induced refractive errors in chickens. Vis Neurosci. 1994;11(2):199–208.PubMedGoogle Scholar
  116. 116.
    Feldkaemper M, Diether S, Kleine G, Schaeffel F. Interactions of spatial and luminance information in the retina of chickens during myopia development. Exp Eye Res. 1999; 68(1):105–15.PubMedGoogle Scholar
  117. 117.
    Guo SS, Sivak JG, Callender MG, Diehl-Jones B. Retinal dopamine and lens-induced refractive errors in chicks. Curr Eye Res. 1995;14(5):385–9.PubMedGoogle Scholar
  118. 118.
    Rohrer B, Spira AW, Stell WK. Apomorphine blocks form-deprivation myopia in chickens by a dopamine D2-receptor mechanism acting in retina or pigmented epithelium. Vis Neurosci. 1993;10(3):447–53.PubMedGoogle Scholar
  119. 119.
    Weiss S, Schaeffel F. Diurnal growth rhythms in the chicken eye: relation to myopia development and retinal dopamine levels. J Comp Physiol A. 1993;172(3):263–70.PubMedGoogle Scholar
  120. 120.
    Stone RA, Pardue MT, Iuvone PM, Khurana TS. Pharmacology of myopia and potential role for intrinsic retinal circadian rhythms. Exp Eye Res. 2013;114:35–47.PubMedGoogle Scholar
  121. 121.
    Koyanagi S, Kuramoto Y, Nakagawa H, Aramaki H, Ohdo S, Soeda S, et al. A molecular mechanism regulating circadian expression of vascular endothelial growth factor in tumor cells. Cancer Res. 2003;63(21):7277–83.PubMedGoogle Scholar
  122. 122.
    Chilov D, Hofer T, Bauer C, Wenger RH, Gassmann M. Hypoxia affects expression of circadian genes PER1 and CLOCK in mouse brain. FASEB J. 2001;15(14):2613–22.PubMedGoogle Scholar
  123. 123.
    Sarkar C, Chakroborty D, Mitra RB, Banerjee S, Dasgupta PS, Basu S. Dopamine in vivo inhibits VEGF-induced phosphorylation of VEGFR-2, MAPK, and focal adhesion kinase in endothelial cells. Am J Physiol Heart Circ Physiol. 2004;287(4):H1554–60.PubMedGoogle Scholar
  124. 124.
    Sinha S, Vohra PK, Bhattacharya R, Dutta S, Sinha S, Mukhopadhyay D. Dopamine regulates phosphorylation of VEGF receptor 2 by engaging Src-homology-2-domain-containing protein tyrosine phosphatase 2. J Cell Sci. 2009;122(Pt 18):3385–92.PubMedGoogle Scholar
  125. 125.
    Bhatwadekar AD, Yan Y, Qi X, Thinschmidt JS, Neu MB, Li Calzi S, et al. Per2 mutation recapitulates the vascular phenotype of diabetes in the retina and bone marrow. Diabetes. 2013;62(1):273–82.PubMedGoogle Scholar
  126. 126.
    Busik JV, Tikhonenko M, Bhatwadekar A, Opreanu M, Yakubova N, Caballero S, et al. Diabetic retinopathy is associated with bone marrow neuropathy and a depressed peripheral clock. J Exp Med. 2009;206(13):2897–906.PubMedCentralPubMedGoogle Scholar
  127. 127.
    Debruyne JP, Noton E, Lambert CM, Maywood ES, Weaver DR, Reppert SM. A clock shock: mouse CLOCK is not required for circadian oscillator function. Neuron. 2006;50(3): 465–77.PubMedGoogle Scholar
  128. 128.
    DeBruyne JP, Weaver DR, Reppert SM. Peripheral circadian oscillators require CLOCK. Curr Biol. 2007;17(14):R538–9.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of Biological SciencesVanderbilt UniversityNashvilleUSA

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