Genetic Advances in Ophthalmology: The Role of Melanopsin-Expressing, Intrinsically Photosensitive Retinal Ganglion Cells in the Circadian Organization of the Visual System

References

• Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science 2002;295:1070–1073
   PubMed Web of Science ®Google Scholar
• Hattar S, Liao HW, Takao M, et al. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 2002;295:1065–1070
   PubMed Web of Science ®Google Scholar
• Provencio I, Jiang G, De Grip WJ, et al. Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci USA 1998;95:340–345
   PubMed Web of Science ®Google Scholar
• Provencio I, Rodriguez IR, Jiang G, et al. A novel human opsin in the inner retina. J Neurosci: Off J Soc Neurosci 2000;20:600–605
   PubMed Web of Science ®Google Scholar
• Provencio I, Rollag MD, Castrucci AM. Photoreceptive net in the mammalian retina: this mesh of cells may explain how some blind mice can still tell day from night. Nature 2002;415:493
   PubMed Web of Science ®Google Scholar
• Sekaran S, Foster RG, Lucas RJ, Hankins MW. Calcium imaging reveals a network of intrinsically light-sensitive inner-retinal neurons. Curr Biol 2003;13:1290–1298
   PubMedGoogle Scholar
• Dacey DM, Liao HW, Peterson BB, et al. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 2005;433:749–754
   PubMed Web of Science ®Google Scholar
• Wong KY, Dunn FA, Graham DM, Berson DM. Synaptic influences on rat ganglion-cell photoreceptors. J Physiol 2007;582:279–296
   PubMed Web of Science ®Google Scholar
• Altimus CM, Güler AD, Alam NM, et al. Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat Neurosci 2010;13:1107–1112
   PubMed Web of Science ®Google Scholar
• Hendrickson AE, Wagoner N, Cowan WM. An autoradiographic and electron microscopic study of retino-hypothalamic connections. Z Zellforsch Mikrosk Anat 1972;135:1–26
   PubMedGoogle Scholar
• Moore RY, Lenn NJ. A retinohypothalamic projection in the rat. J Compar Neurol 1972;146:1–14
   PubMed Web of Science ®Google Scholar
• Gooley JJ, Lu J, Chou TC, et al. Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 2001;4:1165
   PubMed Web of Science ®Google Scholar
• Swanson LW, Cowan WM, Jones EG. An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. J Compar Neurol 1974;156:143–163
   PubMed Web of Science ®Google Scholar
• Pickard GE, Sollars PJ. Intrinsically photosensitive retinal ganglion cells. Rev Physiol Biochem Pharmacol 2012;162:59–90
   PubMed Web of Science ®Google Scholar
• Walker JA, Olton DS. Circadian rhythm of luminance detectability in the rat. Physiol Behav 1979;23:17–21
   PubMedGoogle Scholar
• Brandenburg J, Bobbert AC, Eggelmeyer F. Circadian changes in the response of the rabbits retina to flashes. Behav Brain Res 1983;7:113–123
   PubMed Web of Science ®Google Scholar
• Pierce ME, Sheshberadaran H, Zhang Z, et al. Circadian regulation of iodopsin gene expression in embryonic photoreceptors in retinal cell culture. Neuron 1993;10:579–584
   PubMed Web of Science ®Google Scholar
• LaVail MM. Rod outer segment disc shedding in relation to cyclic lighting. Exp Eye Res 1976;23:277–280
   PubMed Web of Science ®Google Scholar
• 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;19:1268–1273
   PubMed Web of Science ®Google Scholar
• Anderson DH, Fisher SK, Erickson PA, Tabor GA. Rod and cone disc shedding in the rhesus monkey retina: a quantitative study. Exp Eye Res 1980;30:559–574
   PubMedGoogle Scholar
• Reme C, Wirz-Justice A, Rhyner A, Hofmann S. Circadian rhythm in the light response of rat retinal disk-shedding and autophagy. Brain Research 1986;369:356–360
   PubMed Web of Science ®Google Scholar
• Wirz-Justice A, Da Prada M, Reme C. Circadian rhythm in rat retinal dopamine. Neurosci Lett 1984;45:21–25
   PubMed Web of Science ®Google Scholar
• Besharse JC, Iuvone PM. Circadian clock in Xenopus eye controlling retinal serotonin N-acetyltransferase. Nature 1983;305:133–135
   PubMed Web of Science ®Google Scholar
• Jaliffa CO, Saenz D, Resnik E, et al. Circadian activity of the GABAergic system in the golden hamster retina. Brain Research 2001;912:195–202
   PubMedGoogle Scholar
• Gonzalez-Menendez I, Contreras F, Cernuda-Cernuda R, Garcia-Fernandez JM. Daily rhythm of melanopsin-expressing cells in the mouse retina. Frontiers in Cellular Neuroscience 2009;3:3
   PubMedGoogle Scholar
• Gonzalez-Menendez I, Contreras F, Cernuda-Cernuda R, et al. Postnatal development and functional adaptations of the melanopsin photoreceptive system in the albino mouse retina. Invest Ophthalmol Vis Sci 2010;51:4840–4847
   PubMed Web of Science ®Google Scholar
• Hannibal J, Georg B, Hindersson P, Fahrenkrug J. Light and darkness regulate melanopsin in the retinal ganglion cells of the albino Wistar rat. J Mol Neurosci 2005;27:147–155
   PubMed Web of Science ®Google Scholar
• Mathes A, Engel L, Holthues H, et al. Daily profile in melanopsin transcripts depends on seasonal lighting conditions in the rat retina. J Neuroendocrinol 2007;19:952–957
   PubMed Web of Science ®Google Scholar
• Sakamoto K, Liu C, Tosini G. Classical photoreceptors regulate melanopsin mRNA levels in the rat retina. J Neurosci: Off J Soc Neurosci 2004;24:9693–9697
   PubMed Web of Science ®Google Scholar
• Hannibal J, Georg B, Fahrenkrug J. Differential expression of melanopsin mRNA and protein in Brown Norwegian rats. Exp Eye Res 2013;106:55–63
   PubMed Web of Science ®Google Scholar
• Zhang DQ, Wong KY, Sollars PJ, et al. Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. Proc Natl Acad Sci USA 2008;105:14181–14186
   PubMed Web of Science ®Google Scholar
• Zhang R, Hrushesky WJ, Wood PA, et al. Melatonin reprogrammes proteomic profile in light-exposed retina in vivo. Int J Biol Macromol 2010;47:255–260
   PubMed Web of Science ®Google Scholar
• Muller LP, Do MT, Yau KW, et al. Tracer coupling of intrinsically photosensitive retinal ganglion cells to amacrine cells in the mouse retina. J Compar Neurol 2010;518:4813–4824
   PubMedGoogle Scholar
• Roecklein KA, Rohan KJ, Duncan WC, et al. A missense variant (P10L) of the melanopsin (OPN4) gene in seasonal affective disorder. J Affect Disord 2009;114:279–285
   PubMed Web of Science ®Google Scholar
• Buünning E. Die endonome Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber Dtsc Bot Ges 1936;54:590–607
   Google Scholar
• Mackey SR. Biological Rhythms Workshop IA: molecular basis of rhythms generation. Cold Spring Harb Symp Quant Biol 2007;72:7–19
   PubMedGoogle Scholar
• Hastings MH, Maywood ES, Reddy AB. Two decades of circadian time. J Neuroendocrinol 2008;20:812–819
   PubMed Web of Science ®Google Scholar
• Sack RL, Auckley D, Auger RR, et al. Circadian rhythm sleep disorders: part I, basic principles, shift work and jet lag disorders. An American Academy of Sleep Medicine review. Sleep 2007;30:1460–1483
   PubMed Web of Science ®Google Scholar
• Laposky AD, Bass J, Kohsaka A, Turek FW. Sleep and circadian rhythms: key components in the regulation of energy metabolism. FEBS letters 2008;582:142–151
   PubMed Web of Science ®Google Scholar
• Ramsey KM, Marcheva B, Kohsaka A, Bass J. The clockwork of metabolism. Annu Rev Nutr 2007;27:219–240
   PubMed Web of Science ®Google Scholar
• Jean-Louis G, Zizi F, Lazzaro DR, Wolintz AH. Circadian rhythm dysfunction in glaucoma: a hypothesis. Journal of Circadian Rhythms 2008;6:1
   PubMedGoogle Scholar
• Guido ME, Garbarino-Pico E, Contin MA, et al. Inner retinal circadian clocks and non-visual photoreceptors: novel players in the circadian system. Prog Neurobiol 2010;92:484–504
   PubMed Web of Science ®Google Scholar
• La Morgia C, Ross-Cisneros FN, Hannibal J, et al. Melanopsin-expressing retinal ganglion cells: implications for human diseases. Vision Res 2011;51:296–302
   PubMed Web of Science ®Google Scholar
• Ebihara S, Tsuji K, Kondo K. Strain differences of the mouse's free-running circadian rhythm in continuous darkness. Physiol Behav 1978;20:795–799
   PubMed Web of Science ®Google Scholar
• Czeisler CA, Duffy JF, Shanahan TL, et al. Stability, precision, and near-24-hour period of the human circadian pacemaker. Science 1999;284:2177–2181
   PubMed Web of Science ®Google Scholar
• Pittendrigh CS. Circadian rhythms and the circadian organization of living systems. Cold Spring Harb Symp Quant Biol 1960;25:159–184
   PubMedGoogle Scholar
• Honma S, Ono D, Suzuki Y, et al. Suprachiasmatic nucleus: cellular clocks and networks. Prog Brain Res 2012;199:129–141
   PubMed Web of Science ®Google Scholar
• Morin LP, Allen CN. The circadian visual system. Brain Res Brain Res Rev 2005;51:1–60
   Google Scholar
• Hattar S, Kumar M, Park A, et al. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Compar Neurol 2006;497:326–349
   PubMed Web of Science ®Google Scholar
• Gooley JJ, Lu J, Fischer D, Saper CB. A broad role for melanopsin in nonvisual photoreception. J Neurosci: Off J Soc Neurosci 2003;23:7093–7106
   PubMed Web of Science ®Google Scholar
• Morin LP, Blanchard JH, Provencio I. Retinal ganglion cell projections to the hamster suprachiasmatic nucleus, intergeniculate leaflet, and visual midbrain: bifurcation and melanopsin immunoreactivity. J Compar Neurol 2003;465:401–416
   PubMed Web of Science ®Google Scholar
• LeGates TA, Altimus CM, Wang H, et al. Aberrant light directly impairs mood and learning through melanopsin-expressing neurons. Nature 2012;491:594–598
   PubMed Web of Science ®Google Scholar
• Golombek DA Rosenstein RE. Physiology of circadian entrainment. Physiol Rev 2010;90:1063–1102
   PubMed Web of Science ®Google Scholar
• Bonsall DR, Lall GS. Protein kinase C differentially regulates entrainment of the mammalian circadian clock. Chronobiol Int 2013;30:460–469
   PubMed Web of Science ®Google Scholar
• Ibuka N, Inouye SI, Kawamura H. Analysis of sleep-wakefulness rhythms in male rats after suprachiasmatic nucleus lesions and ocular enucleation. Brain Research 1977;122:33–47
   PubMed Web of Science ®Google Scholar
• Skene DJ, Arendt J. Human circadian rhythms: physiological and therapeutic relevance of light and melatonin. Ann Clin Biochem 2006;43:344–353
   PubMed Web of Science ®Google Scholar
• Idda ML, Bertolucci C, Vallone D, et al. Circadian clocks: lessons from fish. Prog Brain Res 2012;199:41–57
   PubMed Web of Science ®Google Scholar
• Kott O, Sumbera R, Nemec P. Light perception in two strictly subterranean rodents: life in the dark or blue? PloS one 2010;5:e11810
   PubMed Web of Science ®Google Scholar
• David-Gray ZK, Janssen JW, DeGrip WJ, et al. Light detection in a “blind” mammal. Nat Neurosci 1998;1:655–656
   PubMed Web of Science ®Google Scholar
• Sack RL, Lewy AJ, Blood ML, et al. Circadian rhythm abnormalities in totally blind people: incidence and clinical significance. J Clin Endocrinol Metab 1992;75:127–134
   PubMed Web of Science ®Google Scholar
• Czeisler CA, Shanahan TL, Klerman EB, et al. Suppression of melatonin secretion in some blind patients by exposure to bright light. N Engl J Med 1995;332:6–11
   PubMed Web of Science ®Google Scholar
• Lockley SW, Skene DJ, Arendt J, et al. Relationship between melatonin rhythms and visual loss in the blind. J Clin Endocrinol Metab 1997;82:3763–3770
   PubMed Web of Science ®Google Scholar
• Campbell SS, Murphy PJ. Extraocular circadian phototransduction in humans. Science 1998;279:396–399
   PubMed Web of Science ®Google Scholar
• Eastman CI, Martin SK, Hebert M. Failure of extraocular light to facilitate circadian rhythm reentrainment in humans. Chronobiol Int 2000;17:807–826
   PubMed Web of Science ®Google Scholar
• Wright KP Jr, Czeisler CA. Absence of circadian phase resetting in response to bright light behind the knees. Science 2002;297:571
   PubMed Web of Science ®Google Scholar
• Skene DJ, Arendt J. Circadian rhythm sleep disorders in the blind and their treatment with melatonin. Sleep Medicine 2007;8:651–655
   PubMed Web of Science ®Google Scholar
• Hätönen T, Laakso ML, Heiskala H, et al. Bright light suppresses melatonin in blind patients with neuronal ceroid-lipofuscinoses. Neurology 1998;50:1445–1450
   PubMed Web of Science ®Google Scholar
• Foster RG, Provencio I, Hudson D, et al. Circadian photoreception in the retinally degenerate mouse (rd/rd). J Comp Physiol A Neuroethol Sens Neural 1991;169:39–50
   PubMed Web of Science ®Google Scholar
• Yoshimura T, Ebihara S. Spectral sensitivity of photoreceptors mediating phase-shifts of circadian rhythms in retinally degenerate CBA/J (rd/rd) and normal CBA/N (+/+)mice. J Comp Physiol A Neuroethol Sens Neural 1996;178:797–802
   PubMed Web of Science ®Google Scholar
• Freedman MS, Lucas RJ, Soni B, et al. Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 1999;284:502–504
   PubMed Web of Science ®Google Scholar
• Lucas RJ, Freedman MS, Munoz M, et al. Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science 1999;284:505–507
   PubMed Web of Science ®Google Scholar
• Brainard GC, Hanifin JP, Greeson JM, et al. Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor. J Neurosci: Off J Soc Neurosci 2001;21:6405–6412
   PubMed Web of Science ®Google Scholar
• Thapan K, Arendt J, Skene DJ. An action spectrum for melatonin suppression: evidence for a novel non-rod, non-cone photoreceptor system in humans. J Physiol 2001;535:261–267
   PubMed Web of Science ®Google Scholar
• Lucas RJ, Douglas RH, Foster RG. Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci 2001;4:621–626
   PubMed Web of Science ®Google Scholar
• Ruby NF, Brennan TJ, Xie X, et al. Role of melanopsin in circadian responses to light. Science 2002;298:2211–2213
   PubMed Web of Science ®Google Scholar
• Panda S, Sato TK, Castrucci AM, et al. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 2002;298:2213–2216
   PubMed Web of Science ®Google Scholar
• Lucas RJ, Hattar S, Takao M, et al. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 2003;299:245–247
   PubMed Web of Science ®Google Scholar
• Hankins MW, Peirson SN, Foster RG. Melanopsin: an exciting photopigment. Trends Neurosci 2008;31:27–36
   PubMed Web of Science ®Google Scholar
• Green CB. Cryptochromes: tailored for distinct functions. Curr Biol: CB 2004;14:R847–R849
   Google Scholar
• Bellingham J, Chaurasia SS, Melyan Z, et al. Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates. PLoS Biology 2006;4:e254
   Google Scholar
• Sexton T, Buhr E, Van Gelder RN. Melanopsin and mechanisms of non-visual ocular photoreception. J Biol Chem 2012;287:1649–1656
   PubMed Web of Science ®Google Scholar
• Hughes S, Hankins MW, Foster RG, Peirson SN. Melanopsin phototransduction: slowly emerging from the dark. Prog Brain Res 2012;199:19–40
   PubMed Web of Science ®Google Scholar
• Do MT, Kang SH, Xue T, et al. Photon capture and signalling by melanopsin retinal ganglion cells. Nature 2009;457:281–287
   PubMed Web of Science ®Google Scholar
• Berson DM, Castrucci AM, Provencio I. Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J Compar Neurol 2010;518:2405–2422
   PubMedGoogle Scholar
• Duffy JF, Czeisler CA. Effect of light on human circadian physiology. Sleep Medicine Clinics 2009;4:165–177
   PubMedGoogle Scholar
• Wong KY. A retinal ganglion cell that can signal irradiance continuously for 10 hours. J Neurosci: Off J Soc Neurosci 2012;32:11478–11485
   PubMedGoogle Scholar
• Tu DC, Owens LA, Anderson L, et al. Inner retinal photoreception independent of the visual retinoid cycle. Proc Natl Acad Sci USA 2006;103:10426–10431
   PubMed Web of Science ®Google Scholar
• Hannibal J, Fahrenkrug J. Melanopsin containing retinal ganglion cells are light responsive from birth. Neuroreport 2004;15:2317–2320
   PubMed Web of Science ®Google Scholar
• Renna JM, Weng S, Berson DM. Light acts through melanopsin to alter retinal waves and segregation of retinogeniculate afferents. Nat Neurosci 2011;14:827–829
   PubMed Web of Science ®Google Scholar
• McNeill DS, Sheely CJ, Ecker JL, et al. Development of melanopsin-based irradiance detecting circuitry. Neural Dev 2011;6:1–10
   PubMedGoogle Scholar
• Rao S, Chun C, Fan J, et al. A direct and melanopsin-dependent fetal light response regulates mouse eye development. Nature 2013;494:243–246
   PubMed Web of Science ®Google Scholar
• Lin B, Koizumi A, Tanaka N, et al. Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc Natl Acad Sci USA 2008;105:16009–16014
   PubMedGoogle Scholar
• Hatori M, Le H, Vollmers C, et al. Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PloS One 2008;3:e2451
   Google Scholar
• Ecker JL, Dumitrescu ON, Wong KY, et al. Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 2010;67:49–60
   PubMed Web of Science ®Google Scholar
• Dkhissi-Benyahya O, Rieux C, Hut RA, Cooper HM. Immunohistochemical evidence of a melanopsin cone in human retina. Invest Ophthalmol Vis Sci 2006;47:1636–1641
   PubMed Web of Science ®Google Scholar
• Xue T, Do MT, Riccio A, et al. Melanopsin signalling in mammalian iris and retina. Nature 2011;479:67–73
   PubMed Web of Science ®Google Scholar
• Baver SB, Pickard GE, Sollars PJ, Pickard GE. Two types of melanopsin retinal ganglion cell differentially innervate the hypothalamic suprachiasmatic nucleus and the olivary pretectal nucleus. Eur J Neurosci 2008;27:1763–1770
   PubMed Web of Science ®Google Scholar
• Schmidt TM, Kofuji P. Structure and function of bistratified intrinsically photosensitive retinal ganglion cells in the mouse. J Compar Neurol 2011;519:1492–1504
   PubMedGoogle Scholar
• Karnas D, Mordel J, Bonnet D, et al. Heterogeneity of intrinsically photosensitive retinal ganglion cells in the mouse revealed by molecular phenotyping. J Compar Neurol 2013;521:912–932
   PubMedGoogle Scholar
• Mu X, Klein WH. A gene regulatory hierarchy for retinal ganglion cell specification and differentiation. Semin Cell Dev Biol 2004;15:115–123
   PubMed Web of Science ®Google Scholar
• Jain V, Ravindran E, Dhingra NK. Differential expression of Brn3 transcription factors in intrinsically photosensitive retinal ganglion cells in mouse. J Compar Neurol 2012;520:742–755
   PubMed Web of Science ®Google Scholar
• Vugler AA, Redgrave P, Semo M, et al. Dopamine neurones form a discrete plexus with melanopsin cells in normal and degenerating retina. Exp Neurol 2007;205:26–35
   PubMedGoogle Scholar
• Hattar S, Lucas RJ, Mrosovsky N, et al. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 2003;424:76–81
   PubMed Web of Science ®Google Scholar
• Semo M, Gias C, Ahmado A, et al. Dissecting a role for melanopsin in behavioural light aversion reveals a response independent of conventional photoreception. PloS One 2010;5:e15009
   Google Scholar
• Hankins MW, Lucas RJ. The primary visual pathway in humans is regulated according to long-term light exposure through the action of a nonclassical photopigment. Curr Biol: CB 2002;12:191–198
   PubMed Web of Science ®Google Scholar
• Goz D, et al. Targeted destruction of photosensitive retinal ganglion cells with a saporin conjugate alters the effects of light on mouse circadian rhythms. PloS One 2008;3:e3153
   PubMed Web of Science ®Google Scholar
• Güler AD, Ecker JL, Lall GS, et al. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 2008;453:102–105
   PubMed Web of Science ®Google Scholar
• Lall GS, Revell VL, Momiji H, et al. Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. Neuron 2010;66:417–428
   PubMed Web of Science ®Google Scholar
• Plautz JD, Kaneko M, Hall JC, Kay SA. Independent photoreceptive circadian clocks throughout Drosophila. Science 1997;278:1632–1635
   PubMed Web of Science ®Google Scholar
• Balsalobre A, Damiola F, Schibler U. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 1998;93:929–937
   PubMed Web of Science ®Google Scholar
• King DP, Zhao Y, Sangoram AM, et al. Positional cloning of the mouse circadian clock gene. Cell 1997;89:641–653
   PubMed Web of Science ®Google Scholar
• Ko CH, Takahashi JS. Molecular components of the mammalian circadian clock. Hum Mol Genet 2006;15 Spec No 2:R271–277
   PubMed Web of Science ®Google Scholar
• Challet E, Caldelas I, Graff C, Pevet P. Synchronization of the molecular clockwork by light- and food-related cues in mammals. Biol Chem 2003;384:711–719
   PubMed Web of Science ®Google Scholar
• Dibner C, Schibler U, Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 2010;72:517–549
   PubMed Web of Science ®Google Scholar
• Cahill GM, Besharse JC. Circadian clock functions localized in xenopus retinal photoreceptors. Neuron 1993;10:573–577
   PubMed Web of Science ®Google Scholar
• Tosini G, Menaker M. Circadian rhythms in cultured mammalian retina. Science 1996;272:419–421
   PubMed Web of Science ®Google Scholar
• Ruan GX, Zhang DQ, Zhou T, et al. Circadian organization of the mammalian retina. Proc Natl Acad Sci USA 2006;103:9703–9708
   PubMed Web of Science ®Google Scholar
• Ruan GX, Allen GC, Yamazaki S, McMahon DG. An autonomous circadian clock in the inner mouse retina regulated by dopamine and GABA. PLoS biology 2008;6:e249
   PubMed Web of Science ®Google Scholar
• 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:e50602
   PubMed Web of Science ®Google Scholar
• Pavan B, Frigato E, Pozzati S, et al. Circadian clocks regulate adenylyl cyclase activity rhythms in human RPE cells. Biochem Biophys Res Commun 2006;350:169–173
   PubMedGoogle Scholar
• Nieto PS, Acosta-Rodriguez VA, Valdez DJ, Guido ME. Differential responses of the mammalian retinal ganglion cell line RGC-5 to physiological stimuli and trophic factors. Neurochem Int 2010;57:216–226
   PubMedGoogle Scholar
• Storch KF, Paz C, Signorovitch J, et al. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 2007;130:730–741
   PubMed Web of Science ®Google Scholar
• Wong KY, Dunn FA, Berson DM. Photoreceptor adaptation in intrinsically photosensitive retinal ganglion cells. Neuron 2005;48:1001–1010
   PubMed Web of Science ®Google Scholar
• Weng S, Wong KY, Berson DM. Circadian modulation of melanopsin-driven light response in rat ganglion-cell photoreceptors. J Biol Rhythms 2009;24:391–402
   PubMedGoogle Scholar
• Castrucci ADL, Ihara N, Doyle SE, et al. The Association for Research in Vision and Ophthalmology, Vol. 45, 4645; Ft. Lauderdale, FL: Invest Ophthalmol Vis Sci, 2004
   Google Scholar
• Hannibal J, Georg B, Fahrenkrug J. Melanopsin changes in neonatal albino rat independent of rods and cones. Neuroreport 2007;18:81–85
   PubMedGoogle Scholar
• Barnard AR, Hattar S, Hankins MW, Lucas RJ. Melanopsin regulates visual processing in the mouse retina. Curr Biol: CB 2006;16:389–395
   PubMed Web of Science ®Google Scholar
• Sakamoto K, Liu C, Kasamatsu M, et al. Dopamine regulates melanopsin mRNA expression in intrinsically photosensitive retinal ganglion cells. Eur J Neurosci 2005;22:3129–3136
   PubMed Web of Science ®Google Scholar
• Dumitrescu ON, Pucci FG, Wong KY, Berson DM. Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: contacts with dopaminergic amacrine cells and melanopsin ganglion cells. J Compar Neurol 2009;517:226–244
   PubMed Web of Science ®Google Scholar
• Witkovsky P, Veisenberger E, LeSauter J, et al. Cellular location and circadian rhythm of expression of the biological clock gene Period 1 in the mouse retina. J Neurosci: Off J Soc Neurosci 2003;23:7670–7676
   PubMed Web of Science ®Google Scholar
• Ostergaard J, Hannibal J, Fahrenkrug J. Synaptic contact between melanopsin-containing retinal ganglion cells and rod bipolar cells. Invest Ophthalmol Vis Sci 2007;48:3812–3820
   PubMed Web of Science ®Google Scholar
• Doyle SE, Grace MS, McIvor W, Menaker M. Circadian rhythms of dopamine in mouse retina: the role of melatonin. Vis Neurosci 2002;19:593–601
   PubMed Web of Science ®Google Scholar
• Zhang DQ, Belenky MA, Sollars PJ, et al. Melanopsin mediates retrograde visual signaling in the retina. PloS One 2012;7:e42647
   PubMed Web of Science ®Google Scholar
• Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. The Br J Ophthalmol 2006;90:262–267
   PubMed Web of Science ®Google Scholar
• Quigley HA. Glaucoma. Lancet 2011;377:1367–1377
   PubMed Web of Science ®Google Scholar
• Liu JH, Kripke DF, Hoffman RE, et al. Nocturnal elevation of intraocular pressure in young adults. Invest Ophthalmol Vis Sci 1998;39:2707–2712
   PubMed Web of Science ®Google Scholar
• Maeda A, Tsujiya S, Higashide T, et al. Circadian intraocular pressure rhythm is generated by clock genes. Invest Ophthalmol Vis Sci 2006;47:4050–4052
   PubMed Web of Science ®Google Scholar
• Tosini G, Pozdeyev N, Sakamoto K, Iuvone PM. The circadian clock system in the mammalian retina. Bioessays 2008;30:624–633
   PubMed Web of Science ®Google Scholar
• Clark CV, Mapstone R. Pupil cycle time in primary closed-angle glaucoma. Canadian Journal of Ophthalmology/Journal Canadien d'Ophtalmologie 1986;21:88–91
   PubMedGoogle Scholar
• Kalaboukhova L, Fridhammar V, Lindblom B. Relative afferent pupillary defect in glaucoma: a pupillometric study. Acta Ophthalmol Scand 2007;85:519–525
   PubMedGoogle Scholar
• Feigl B, Mattes D, Thomas R, Zele AJ. Intrinsically photosensitive (melanopsin) retinal ganglion cell function in glaucoma. Invest Ophthalmol Vis Sci 2011;52:4362–4367
   PubMed Web of Science ®Google Scholar
• Gamlin PD, McDougal DH, Pokorny J, et al. Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vision Res 2007;47:946–954
   PubMed Web of Science ®Google Scholar
• Kankipati L, Girkin CA, Gamlin PD. The post-illumination pupil response is reduced in glaucoma patients. Invest Ophthalmol Vis Sci 2011;52:2287–2292
   PubMed Web of Science ®Google Scholar
• Jakobs TC, Libby RT, Ben Y, et al. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J Cell Biol 2005;171:313–325
   PubMed Web of Science ®Google Scholar
• Li SY, Yau SY, Chen BY, et al. Enhanced survival of melanopsin-expressing retinal ganglion cells after injury is associated with the PI3 K/Akt pathway. Cell Mol Neurobiol 2008;28:1095–1107
   PubMed Web of Science ®Google Scholar
• Li RS, Chen BY, Tay DK, et al. Melanopsin-expressing retinal ganglion cells are more injury-resistant in a chronic ocular hypertension model. Invest Ophthalmol Vis Sci 2006;47:2951–2958
   PubMed Web of Science ®Google Scholar
• Robinson GA, Madison RD. Axotomized mouse retinal ganglion cells containing melanopsin show enhanced survival, but not enhanced axon regrowth into a peripheral nerve graft. Vision Res 2004;44:2667–2674
   PubMed Web of Science ®Google Scholar
• DeParis S, Caprara C, Grimm C. Intrinsically photosensitive retinal ganglion cells are resistant to N-methyl-D-aspartic acid excitotoxicity. Mol Vis 2012;18:2814–2827
   PubMed Web of Science ®Google Scholar
• Wang HZ, Lu QJ, Wang NL, et al. Loss of melanopsin-containing retinal ganglion cells in a rat glaucoma model. Chin Med J (Engl) 2008;121:1015–1019
   PubMed Web of Science ®Google Scholar
• de Zavalía N, Plano SA, Fernandez DC, et al. Effect of experimental glaucoma on the non-image forming visual system. J Neurochem 2011;117:904–914
   PubMed Web of Science ®Google Scholar
• Drouyer E, Dkhissi-Benyahya O, Chiquet C, et al. Glaucoma alters the circadian timing system. PloS One 2008;3:e3931
   PubMed Web of Science ®Google Scholar
• Lanzani MF, de Zavalía N, Fontana H, et al. Alterations of locomotor activity rhythm and sleep parameters in patients with advanced glaucoma. Chronobiol Int 2012;29:911–919
   PubMed Web of Science ®Google Scholar
• Moreno MC, Campanelli J, Sande P, et al. Retinal oxidative stress induced by high intraocular pressure. Free Radic Biol Med 2004;37:803–812
   PubMed Web of Science ®Google Scholar
• Belforte NA, Moreno MC, de Zavalía N, et al. Melatonin: a novel neuroprotectant for the treatment of glaucoma. J Pineal Res 2010;48:353–364
   PubMed Web of Science ®Google Scholar
• Carelli V, Rugolo M, Sgarbi G, et al. Bioenergetics shapes cellular death pathways in Leber's hereditary optic neuropathy: a model of mitochondrial neurodegeneration. Biochim Biophys Acta 2004;1658:172–179
   PubMed Web of Science ®Google Scholar
• Wakakura M, Yokoe J. Evidence for preserved direct pupillary light response in Leber's hereditary optic neuropathy. The Br J Ophthalmol 1995;79:442–446
   PubMed Web of Science ®Google Scholar
• Bremner FD, Tomlin EA, Shallo-Hoffmann J, et al. The pupil in dominant optic atrophy. Invest Ophthalmol Vis Sci 2001;42:675–678
   PubMedGoogle Scholar
• Perez-Rico C, et al. [Alterations in nocturnal melatonin secretion in patients with optic neuropathies]. Arch Soc Esp Oftalmol 2009;84:251–257
   PubMedGoogle Scholar
• Kawasaki A, Herbst K, Sander B, Milea D. Selective wavelength pupillometry in Leber hereditary optic neuropathy. Clin Experiment Ophthalmol 2010;38:322–324
   PubMedGoogle Scholar
• Noseda R, Burstein R. Advances in understanding the mechanisms of migraine-type photophobia. Curr Opin Neurol 2011;24:197–202
   PubMedGoogle Scholar
• Matynia A, Parikh S, Chen B, et al. Intrinsically photosensitive retinal ganglion cells are the primary but not exclusive circuit for light aversion. Exp Eye Res 2012;105:60–69
   PubMed Web of Science ®Google Scholar
• Lewy AJ, Emens J, Jackman A, Yuhas K. Circadian uses of melatonin in humans. Chronobiol Int 2006;23:403–412
   PubMed Web of Science ®Google Scholar
• Challet E, Dumont S, Mehdi MK, et al. Aging-like circadian disturbances in folate-deficient mice. Neurobiol Aging 2013;34:1589–1598
   PubMedGoogle Scholar
• Winn B, Whitaker D, Elliott DB, Phillips NJ. Factors affecting light-adapted pupil size in normal human subjects. Invest Ophthalmol Vis Sci 1994;35:1132–1137
   PubMed Web of Science ®Google Scholar
• Charman WN. Age, lens transmittance, and the possible effects of light on melatonin suppression. Ophthalmic Physiol Opt 2003;23:181–187
   PubMedGoogle Scholar
• Fernandez DC, Sande PH, de Zavalía N, et al. Effect of experimental diabetic retinopathy on the non-image-forming visual system. Chronobiol Int 2013;30:583–597
   PubMed Web of Science ®Google Scholar
• Mainster MA. Violet and blue light blocking intraocular lenses: photoprotection versus photoreception. The Br J Ophthalmol 2006;90:784–792
   PubMed Web of Science ®Google Scholar
• Turner PL, Van Someren EJ, Mainster MA. The role of environmental light in sleep and health: effects of ocular aging and cataract surgery. Sleep medicine reviews 2010;14:269–280
   PubMed Web of Science ®Google Scholar
• Behar-Cohen F, Martinsons C, Viénot F, et al. Light-emitting diodes (LED) for domestic lighting: any risks for the eye? Prog Retin Eye Res 2011;30:239–257
   PubMed Web of Science ®Google Scholar
• Benloucif S, Green K, L'Hermite-Balériaux M, et al. Responsiveness of the aging circadian clock to light. Neurobiol Aging 2006;27:1870–1879
   PubMed Web of Science ®Google Scholar
• Nickla DL. Ocular diurnal rhythms and eye growth regulation: Where we are 50 years after Lauber Exp Eye Res 2013;114:25–34
   PubMed Web of Science ®Google Scholar
• Stone RA, et al. Image defocus and altered retinal gene expression in chick: clues to the pathogenesis of ametropia. Invest Ophthalmol Vis Sci 2011;52:5765–5777
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Rosenthal NE, Sack DA, Gillin JC, et al. Seasonal affective disorder: A description of the syndrome and preliminary findings with light therapy. Arch Gen Psychiatry 1984;41:72–80
   PubMed Web of Science ®Google Scholar
• Lam RW, Levitan RD. Pathophysiology of seasonal affective disorder: A review. J Psychiatry Neurosci 2000;25:469–480
   PubMed Web of Science ®Google Scholar
• Glickman G, Byrne B, Pineda C, et al. Light therapy for seasonal affective disorder with blue narrow-band light-emitting diodes (LEDs). Biol Psychiatry 2006;59:502–507
   PubMed Web of Science ®Google Scholar
• Lewy AJ, Emens JS, Songer JB, et al. Winter Depression: Integrating mood, circadian rhythms, and the sleep/wake and light/dark cycles into a bio-psycho-social-environmental model. Sleep Med Clin 2009;4:285–299
   PubMedGoogle Scholar
• Solomon SG, Lennie P. The machinery of colour vision. Nat Rev Neurosci 2007;8:276–286
   PubMed Web of Science ®Google Scholar