1932

Abstract

The discovery of a third type of photoreceptors in the mammalian retina, intrinsically photosensitive retinal ganglion cells (ipRGCs), has had a revolutionary impact on chronobiology. We can now properly account for numerous non-vision-related functions of light, including its effect on the circadian system. Here, we give an overview of ipRGCs and their function as it relates specifically to mood and biological rhythms. Although circadian disruptions have been traditionally hypothesized to be the mediators of light's effects on mood, here we present an alternative model that dispenses with assumptions of causality between the two phenomena and explains mood regulation by light via another ipRGC-dependent mechanism.

Keyword(s): circadianipRGClightmoodphotoperiodrhythms
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2017-07-25
2024-04-15
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Literature Cited

  1. Altimus CM, Güler AD, Alam NM, Arman AC, Prusky GT. et al. 2010. Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat. Neurosci. 13:91107–12 [Google Scholar]
  2. Altimus CM, Güler AD, Villa KL, McNeill DS, Legates TA, Hattar S. 2008. Rods-cones and melanopsin detect light and dark to modulate sleep independent of image formation. PNAS 105:5019998–20003 [Google Scholar]
  3. Arey RN, Enwright JF III, Spencer SM, Falcon E, Ozburn AR. et al. 2014. An important role for cholecystokinin, a CLOCK target gene, in the development and treatment of manic-like behaviors. Mol. Psychiatry 19:3342–50 [Google Scholar]
  4. Arey RN, McClung CA. 2012. An inhibitor of casein kinase 1 ε/δ partially normalizes the manic-like behaviors of the ClockΔ19 mouse. Behav. Pharmacol. 23:4392–96 [Google Scholar]
  5. Ashkenazy-Frolinger T, Kronfeld-Schor N, Juetten J, Einat H. 2010. It is darkness and not light: depression-like behaviors of diurnal unstriped Nile grass rats maintained under a short photoperiod schedule. J. Neurosci. Methods 186:2165–70 [Google Scholar]
  6. Baltazar RM, Coolen LM, Webb IC. 2013. Diurnal rhythms in neural activation in the mesolimbic reward system: critical role of the medial prefrontal cortex. Eur. J. Neurosci. 38:22319–27 [Google Scholar]
  7. Bechtel W. 2015. Circadian rhythms and mood disorders: Are the phenomena and mechanisms causally related?. Front. Psychiatry 6:118 [Google Scholar]
  8. Benca RM, Obermeyer WH, Thisted RA, Gillin JC. 1992. Sleep and psychiatric disorders: a meta-analysis. Arch. Gen. Psychiatry 49:8651–68 [Google Scholar]
  9. Berson DM, Dunn FA, Takao M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:55571070–73 [Google Scholar]
  10. Birchler-Pedross A, Schröder CM, Münch M, Knoblauch V, Blatter K. et al. 2009. Subjective well-being is modulated by circadian phase, sleep pressure, age, and gender. J. Biol. Rhythm. 24:3232–42 [Google Scholar]
  11. Boivin DB, Czeisler CA, Dijk DJ, Duffy JF, Folkard S. et al. 1997. Complex interaction of the sleep-wake cycle and circadian phase modulates mood in healthy subjects. Arch. Gen. Psychiatry 54:2145–52 [Google Scholar]
  12. Butler MP, Silver R. 2011. Divergent photic thresholds in the non-image-forming visual system: entrainment, masking and pupillary light reflex. Proc. R. Soc. B 278:1706745–50 [Google Scholar]
  13. Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC. et al. 2002. Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417:6887405–10 [Google Scholar]
  14. Chocano-Bedoya PO, Mirzaei F, O'Reilly EJ, Lucas M, Okereke OI. et al. 2014. C-reactive protein, interleukin-6, soluble tumor necrosis factor α receptor 2 and incident clinical depression. J. Affect. Disord. 163:25–32 [Google Scholar]
  15. Ciarleglio CM, Axley JC, Strauss BR, Gamble KL, McMahon DG. 2011. Perinatal photoperiod imprints the circadian clock. Nat. Neurosci. 14:125–27 [Google Scholar]
  16. Coimbra DG, Pereira E, Silva AC, de Sousa-Rodrigues CF, Barbosa FT, de Siqueira Figueredo D. et al. 2016. Do suicide attempts occur more frequently in the spring too? A systematic review and rhythmic analysis. J. Affect. Disord. 196:125–37 [Google Scholar]
  17. CONVERGE Consort. 2015. Sparse whole-genome sequencing identifies two loci for major depressive disorder. Nature 523:7562588–91 [Google Scholar]
  18. Coomans CP, Ramkisoensing A, Meijer JH. 2015. The suprachiasmatic nuclei as a seasonal clock. Front. Neuroendocrinol. 37:29–42 [Google Scholar]
  19. Crasson M, Kjiri S, Colin A, Kjiri K, L'Hermite-Baleriaux M. et al. 2004. Serum melatonin and urinary 6-sulfatoxymelatonin in major depression. Psychoneuroendocrinology 29:11–12 [Google Scholar]
  20. Czeisler CA, Shanahan TL, Klerman EB, Martens H, Brotman DJ. et al. 1995. Suppression of melatonin secretion in some blind patients by exposure to bright light. N. Engl. J. Med. 332:16–11 [Google Scholar]
  21. Davidson AJ, Sellix MT, Daniel J, Yamazaki S, Menaker M, Block GD. 2006. Chronic jet-lag increases mortality in aged mice. Curr. Biol. 16:21R914–16 [Google Scholar]
  22. de la Iglesia HO, Cambras T, Schwartz WJ, Díez-Noguera A. 2004. Forced desynchronization of dual circadian oscillators within the rat suprachiasmatic nucleus. Curr. Biol. 14:9796–800 [Google Scholar]
  23. de Vries GJ, Buijs RM, Swaab DF. 1981. Ontogeny of the vasopressinergic neurons of the suprachiasmatic nucleus and their extrahypothalamic projections in the rat brain—presence of a sex difference in the lateral septum. Brain Res 218:1–267–78 [Google Scholar]
  24. Deats SP, Adidharma W, Yan L. 2015. Hypothalamic dopaminergic neurons in an animal model of seasonal affective disorder. Neurosci. Lett. 602:17–21 [Google Scholar]
  25. Doherty CJ, Kay SA. 2014. Circadian control of global gene expression patterns. Annu. Rev. Genet. 44:419–44 [Google Scholar]
  26. Dulcis D, Jamshidi P, Leutgeb S, Spitzer NC. 2013. Neurotransmitter switching in the adult brain regulates behavior. Science 340:6131449–53 [Google Scholar]
  27. Edgar RS, Stangherlin A, Nagy AD, Nicoll MP, Efstathiou S. et al. 2016. Cell autonomous regulation of herpes and influenza virus infection by the circadian clock. PNAS 113:3610085–90 [Google Scholar]
  28. Edwards BJ, Waterhouse J. 2009. Effects of one night of partial sleep deprivation upon diurnal rhythms of accuracy and consistency in throwing darts. Chronobiol. Int. 26:4756–68 [Google Scholar]
  29. Fava M, Johe K, Ereshefsky L, Gertsik LG, English BA. et al. 2015. A Phase 1B, randomized, double blind, placebo controlled, multiple-dose escalation study of NSI-189 phosphate, a neurogenic compound, in depressed patients. Mol. Psychiatry 21:101372–80 [Google Scholar]
  30. Fonken LK, Aubrecht TG, Meléndez-Fernández OH, Weil ZM, Nelson RJ. 2013. Dim light at night disrupts molecular circadian rhythms and affects metabolism. J. Biol. Rhythm. 28:4262–71 [Google Scholar]
  31. Fonken LK, Kitsmiller E, Smale L, Nelson RJ. 2012. Dim nighttime light impairs cognition and provokes depressive-like responses in a diurnal rodent. J. Biol. Rhythm. 27:4319–27 [Google Scholar]
  32. Foster RG, Kreitzman L. 2014. The rhythms of life: What your body clock means to you!. Exp. Physiol. 99:4599–606 [Google Scholar]
  33. Foster RG, Provencio I, Hudson D, Fiske S, De Grip W, Menaker M. 1991. Circadian photoreception in the retinally degenerate mouse (rd/rd). J. Comp. Physiol. A 169:139–50 [Google Scholar]
  34. Fu Y, Zhong H, Wang MH, Luo DG, Liao HW. et al. 2005. Intrinsically photosensitive retinal ganglion cells detect light with a vitamin A-based photopigment, melanopsin. PNAS 102:2910339–44 [Google Scholar]
  35. Gibbs JE, Blaikley J, Beesley S, Matthews L, Simpson KD. et al. 2012. The nuclear receptor REV-ERBα mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. PNAS 109:2582–87 [Google Scholar]
  36. Glaus J, Vandeleur CL, von Känel R, Lasserre AM, Strippoli MP. et al. 2014. Associations between mood, anxiety or substance use disorders and inflammatory markers after adjustment for multiple covariates in a population-based study. J. Psychiatr. Res. 58:36–45 [Google Scholar]
  37. Gorgulu Y, Caliyurt O. 2009. Rapid antidepressant effects of sleep deprivation therapy correlates with serum BDNF changes in major depression. Brain Res. Bull. 80:3158–62 [Google Scholar]
  38. Gorwood P. 2010. Restoring circadian rhythms: a new way to successfully manage depression. J. Psychopharmacol. 24:2 Suppl.15–19 [Google Scholar]
  39. Göz D, Studholme K, Lappi DA, Rollag MD, Provencio I, Morin LP. 2008. Targeted destruction of photosensitive retinal ganglion cells with a saporin conjugate alters the effects of light on mouse circadian rhythms. PLOS ONE 3:9e3153 [Google Scholar]
  40. Green NH, Jackson CR, Iwamoto H, Tackenberg MC, McMahon DG. 2015. Photoperiod programs dorsal raphe serotonergic neurons and affective behaviors. Curr. Biol. 25:101389–94 [Google Scholar]
  41. Guilding C, Piggins HD. 2007. Challenging the omnipotence of the suprachiasmatic timekeeper: Are circadian oscillators present throughout the mammalian brain. ? Eur. J. Neurosci. 25:113195–216 [Google Scholar]
  42. Güler AD, Altimus CM, Ecker JL, Hattar S. 2007. Multiple photoreceptors contribute to nonimage-forming visual functions predominantly through melanopsin-containing retinal ganglion cells. Cold Spring Harb. Symp. Quant. Biol. 72:509–15 [Google Scholar]
  43. Hallam KT, Olver JS, Horgan JE, McGrath C, Norman TR. 2005. Low doses of lithium carbonate reduce melatonin light sensitivity in healthy volunteers. Int. J. Neuropsychopharmacol. 8:2255–59 [Google Scholar]
  44. Hannibal J, Hindersson P, Østergaard J, Georg B, Heegaard S. et al. 2004. Melanopsin is expressed in PACAP-containing retinal ganglion cells of the retinohypothalamic tract. Investig. Ophthalmol. Vis. Sci. 45:114202–9 [Google Scholar]
  45. Harmatz MG, Well AD, Overtree CE, Kawamura KY, Rosal M, Ockene IS. 2000. Seasonal variation of depression and other moods: a longitudinal approach. J. Biol. Rhythm. 15:4344–50 [Google Scholar]
  46. Hastings M, O'Neill JS, Maywood ES. 2007. Circadian clocks: regulators of endocrine and metabolic rhythms. J. Endocrinol. 195:2187–98 [Google Scholar]
  47. Hattar S, Kumar M, Park A, Tong P, Tung J. et al. 2006. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J. Comp. Neurol. 497:3326–49 [Google Scholar]
  48. Hattar S, Liao HW, Takao M, Berson DM, Yau KW. 2002. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:55571065–70 [Google Scholar]
  49. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH. et al. 2003. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424:694476–81 [Google Scholar]
  50. Hay-Schmidt A, Vrang N, Larsen PJ, Mikkelsen JD. 2003. Projections from the raphe nuclei to the suprachiasmatic nucleus of the rat. J. Chem. Neuroanat. 25:4293–310 [Google Scholar]
  51. Hyde CL, Nagle MW, Tian C, Chen X, Paciga SA. et al. 2016. Identification of 15 genetic loci associated with risk of major depression in individuals of European descent. Nat. Genet. 48:91031–36 [Google Scholar]
  52. Huang W, Ramsey KM, Marcheva B, Bass J. 2011. Circadian rhythms, sleep, and metabolism. J. Clin. Investig. 121:62133–41 [Google Scholar]
  53. Jacobsen FM, Wehr TA, Skwerer RA, Sack DA, Rosenthal NE. 1987. Morning versus midday phototherapy of seasonal affective disorder. Am. J. Psychiatry 144:101301–5 [Google Scholar]
  54. Jain V, Srivastava I, Palchaudhuri S, Goel M, Sinha-Mahapatra SK, Dhingra NK. 2016. Classical photoreceptors are primarily responsible for the pupillary light reflex in mouse. PLOS ONE 11:6e0157226 [Google Scholar]
  55. Johansson AS, Brask J, Owe-Larsson B, Hetta J, Lundkvist GBS. 2011. Valproic acid phase shifts the rhythmic expression of PERIOD2::LUCIFERASE. J. Biol. Rhythm. 26:6541–51 [Google Scholar]
  56. Johnson MP, Duffy JF, Dijk DJ, Ronda JM, Dyal CM, Czeisler CA. 1992. Short-term memory, alertness and performance: a reappraisal of their relationship to body temperature. J. Sleep Res. 1:124–29 [Google Scholar]
  57. Keeler CE. 1927. Iris movements in blind mice. Am. J. Physiol. 81:1107–12 [Google Scholar]
  58. Kiessling S, Eichele G, Oster H. 2010. Adrenal glucocorticoids have a key role in circadian resynchronization in a mouse model of jet lag. J. Clin. Investig. 120:72600–9 [Google Scholar]
  59. Koorengevel KM, Beersma DG, den Boer JA, van den Hoofdakker RH. 2002. A forced desynchrony study of circadian pacemaker characteristics in seasonal affective disorder. J. Biol. Rhythm. 17:5463–75 [Google Scholar]
  60. Kripke DF, Mullaney DJ, Atkinson M, Wolf S. 1978. Circadian rhythm disorders in manic-depressives. Biol. Psychiatry 13:3335–51 [Google Scholar]
  61. Lamers F, Vogelzangs N, Merikangas KR, de Jonge P, Beekman AT, Penninx BW. 2013. Evidence for a differential role of HPA-axis function, inflammation and metabolic syndrome in melancholic versus atypical depression. Mol. Psychiatry 18:6692–99 [Google Scholar]
  62. Landgraf D, McCarthy MJ, Welsh DK. 2014. The role of the circadian clock in animal models of mood disorders. Behav. Neurosci. 128:3344–59 [Google Scholar]
  63. Lavebratt C, Sjöholm LK, Soronen P, Paunio T, Vawter MP. et al. 2010. CRY2 is associated with depression. PLOS ONE 5:2e9407 [Google Scholar]
  64. LeGates TA, Altimus CM, Wang H, Lee HK, Yang S. et al. 2012. Aberrant light directly impairs mood and learning through melanopsin-expressing neurons. Nature 491:7425594–98 [Google Scholar]
  65. LeGates TA, Fernandez DC, Hattar S. 2014. Light as a central modulator of circadian rhythms, sleep and affect. Nat. Rev. Neurosci. 15:7443–54 [Google Scholar]
  66. Lewy AJ, Sack RL, Miller LS, Hoban TM. 1987. Antidepressant and circadian phase-shifting effects of light. Science 235:4786352–54 [Google Scholar]
  67. Li J, Lu WQ, Beesley S, Loudon ASI, Meng QJ. 2012. Lithium impacts on the amplitude and period of the molecular circadian clockwork. PLOS ONE 7:3e33292 [Google Scholar]
  68. Lockley SW, Evans EE, Scheer FA, Brainard GC, Czeisler CA, Aeschbach D. 2006. Short-wavelength sensitivity for the direct effects of light on alertness, vigilance, and the waking electroencephalogram in humans. Sleep 29:2161–68 [Google Scholar]
  69. Loudon ASI, Meng QJ, Maywood ES, Bechtold DA, Boot-Handford RP, Hastings MH. 2007. The biology of the circadian Ck1ε tau mutation in mice and Syrian hamsters: a tale of two species. Cold Spring Harb. Symp. Quant. Biol. 72:261–71 [Google Scholar]
  70. Mairesse J, Silletti V, Laloux C, Zuena AR, Giovine A. et al. 2013. Chronic agomelatine treatment corrects the abnormalities in the circadian rhythm of motor activity and sleep/wake cycle induced by prenatal restraint stress in adult rats. Int. J. Neuropsychopharmacol. 16:2323–38 [Google Scholar]
  71. Mansour HA, Wood J, Logue T, Chowdari KV, Dayal M. et al. 2006. Association study of eight circadian genes with bipolar I disorder, schizoaffective disorder and schizophrenia. Genes Brain Behav 5:2150–57 [Google Scholar]
  72. McCarthy MJ, Nievergelt CM, Kelsoe JR, Welsh DK. 2012. A survey of genomic studies supports association of circadian clock genes with bipolar disorder spectrum illnesses and lithium response. PLOS ONE 7:2e32091 [Google Scholar]
  73. McClung CA. 2013. How might circadian rhythms control mood? Let me count the ways. Biol. Psychiatry 74:4242–49 [Google Scholar]
  74. Miller AH, Raison CL. 2015. The role of inflammation in depression: from evolutionary imperative to modern treatment target. Nat. Rev. Immunol. 16:122–34 [Google Scholar]
  75. Miller BR, Hen R. 2015. The current state of the neurogenic theory of depression and anxiety. Curr. Opin. Neurobiol. 30:51–58 [Google Scholar]
  76. Mohawk JA, Cashen K, Lee TM. 2005. Inhibiting cortisol response accelerates recovery from a photic phase shift. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288:1R221–28 [Google Scholar]
  77. Monk TH, Buysse DJ, Carrier J, Billy BD, Rose LR. 2001. Effects of afternoon “siesta” naps on sleep, alertness, performance, and circadian rhythms in the elderly. Sleep 24:6680–87 [Google Scholar]
  78. Murray G, Allen NB, Trinder J. 2002. Mood and the circadian system: investigation of a circadian component in positive affect. Chronobiol. Int. 19:61151–69 [Google Scholar]
  79. Nagano M, Adachi A, Nakahama K, Nakamura T, Tamada M. et al. 2003. An abrupt shift in the day/night cycle causes desynchrony in the mammalian circadian center. J. Neurosci. 23:146141–51 [Google Scholar]
  80. Narasimamurthy R, Hatori M, Nayak SK, Liu F, Panda S, Verma IM. 2012. Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. PNAS 109:3112662–67 [Google Scholar]
  81. Noh JY, Han DH, Yoon JA, Kim MH, Kim SE. et al. 2011. Circadian rhythms in urinary functions: possible roles of circadian clocks?. Int. Neurourol. J. 15:264–73 [Google Scholar]
  82. Nomura K, Castanon-Cervantes O, Davidson A, Fukuhara C. 2008. Selective serotonin reuptake inhibitors and raft inhibitors shorten the period of Period1-driven circadian bioluminescence rhythms in rat-1 fibroblasts. Life Sci 82:23–241169–74 [Google Scholar]
  83. Noseda R, Kainz V, Jakubowski M, Gooley JJ, Saper CB. et al. 2010. A neural mechanism for exacerbation of headache by light. Nat. Neurosci. 13:2239–45 [Google Scholar]
  84. Paul MJ, Zucker I, Schwartz WJ. 2007. Tracking the seasons: the internal calendars of vertebrates. Philos. Trans. R. Soc. B 363:1490341–61 [Google Scholar]
  85. Peacock WL, Król E, Moar KM, McLaren JS, Mercer JG, Speakman JR. 2004. Photoperiodic effects on body mass, energy balance and hypothalamic gene expression in the bank vole. J. Exp. Biol. 207:Pt. 1165–77 [Google Scholar]
  86. Peterson MJ, Benca RM. 2006. Sleep in mood disorders. Psychiatr. Clin. N. Am. 29:41009–32 [Google Scholar]
  87. Pickard GE. 1987. Circadian rhythm of nociception in the golden hamster. Brain Res 425:2395–400 [Google Scholar]
  88. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. 2000. A novel human opsin in the inner retina. J. Neurosci. 20:2600–5 [Google Scholar]
  89. Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V. et al. 2005. Induction of photosensitivity by heterologous expression of melanopsin. Nature 433:7027745–49 [Google Scholar]
  90. Refinetti R. 1995. Rhythms of temperature selection and body temperature are out of phase in the golden hamster. Behav. Neurosci. 109:3523–27 [Google Scholar]
  91. Refinetti R. 2016. Circadian Physiology Boca Raton, FL: CRC Press, 3rd ed..
  92. Refinetti R, Menaker M. 1993. Effects of imipramine on circadian rhythms in the golden hamster. Pharmacol. Biochem. Behav. 45:127–33 [Google Scholar]
  93. Riemann D, Wiegand M, Lauer CJ, Berger M. 1993. Naps after total sleep deprivation in depressed patients: Are they depressiogenic. ? Psychiatry Res 49:2109–20 [Google Scholar]
  94. Roecklein KA, Rohan KJ. 2005. Seasonal affective disorder: an overview and update. Psychiatry 2:120–26 [Google Scholar]
  95. Roybal K, Theobold D, Graham A, DiNieri JA, Russo SJ. et al. 2007. Mania-like behavior induced by disruption of CLOCK. PNAS 104:156406–11 [Google Scholar]
  96. Schmidt TM, Alam NM, Chen S, Kofuji P, Li W. et al. 2014. A role for melanopsin in alpha retinal ganglion cells and contrast detection. Neuron 82:4781–88 [Google Scholar]
  97. Schmidt TM, Chen SK, Hattar S. 2011a. Intrinsically photosensitive retinal ganglion cells: many subtypes, diverse functions. Trends Neurosci 34:11572–80 [Google Scholar]
  98. Schmidt TM, Do MT, Dacey D, Lucas R, Hattar S, Matynia A. 2011b. Melanopsin-positive intrinsically photosensitive retinal ganglion cells: from form to function. J. Neurosci. 31:4516094–101 [Google Scholar]
  99. Schmidt TM, Kofuji P. 2009. Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J. Neurosci. 29:2476–82 [Google Scholar]
  100. Sidor MM, Spencer SM, Dzirasa K, Parekh PK, Tye KM. et al. 2015. Daytime spikes in dopaminergic activity drive rapid mood-cycling in mice. Mol. Psychiatry 20:111406–19 [Google Scholar]
  101. Smale L, Boverhof J. 1999. The suprachiasmatic nucleus and intergeniculate leaflet of Arvicanthis niloticus, a diurnal murid rodent from East Africa. J. Comp. Neurol. 403:2190–208 [Google Scholar]
  102. Souêtre E, Salvati E, Belugou JL, Pringuey D, Candito M. et al. 1989. Circadian rhythms in depression and recovery: evidence for blunted amplitude as the main chronobiological abnormality. Psychiatry Res 28:3263–78 [Google Scholar]
  103. Spencer S, Falcon E, Kumar J, Krishnan V, Mukherjee S. et al. 2013. Circadian genes Period 1 and Period 2 in the nucleus accumbens regulate anxiety-related behavior. Eur. J. Neurosci. 37:2242–50 [Google Scholar]
  104. Sprouse J, Braselton J, Reynolds L. 2006. Fluoxetine modulates the circadian biological clock via phase advances of suprachiasmatic nucleus neuronal firing. Biol. Psychiatry 60:8896–99 [Google Scholar]
  105. Tamai S, Sanada K, Fukada Y. 2008. Time-of-day-dependent enhancement of adult neurogenesis in the hippocampus. PLOS ONE 3:12e3835 [Google Scholar]
  106. Takahashi JS. 2017. Transcriptional architecture of the mammalian circadian clock. Nat. Rev. Genet. 18:164–79 [Google Scholar]
  107. Tataroğlu O, Aksoy A, Yilmaz A, Canbeyli R. 2004. Effect of lesioning the suprachiasmatic nuclei on behavioral despair in rats. Brain Res 1001:1–2118–24 [Google Scholar]
  108. Tsai JW, Hannibal J, Hagiwara G, Colas D, Ruppert E. et al. 2009. Melanopsin as a sleep modulator: circadian gating of the direct effects of light on sleep and altered sleep homeostasis in Opn4−/− mice. PLOS Biol 7:6e1000125 [Google Scholar]
  109. Van Gelder RN, Buhr ED. 2016. Ocular photoreception for circadian rhythm entrainment in mammals. Annu. Rev. Vis. Sci. 2:153–69 [Google Scholar]
  110. Vandewalle G, Collignon O, Hull JT, Daneault V, Albouy G. et al. 2013. Blue light stimulates cognitive brain activity in visually blind individuals. J. Cogn. Neurosci. 25:122072–85 [Google Scholar]
  111. Voderholzer U, Fiebich BL, Dersch R, Feige B, Piosczyk H. et al. 2012. Effects of sleep deprivation on nocturnal cytokine concentrations in depressed patients and healthy control subjects. J. Neuropsychiatry Clin. Neurosci. 24:3354–66 [Google Scholar]
  112. Walmsley L, Hanna L, Mouland J, Martial F, West A. et al. 2015. Colour as a signal for entraining the mammalian circadian clock. PLOS Biol 13:4e1002127 [Google Scholar]
  113. Wehr TA. 2001. Photoperiodism in humans and other primates: evidence and implications. J. Biol. Rhythm. 16:4348–64 [Google Scholar]
  114. Wehr TA, Jacobsen FM, Sack DA, Arendt J, Tamarkin L, Rosenthal NE. 1986. Phototherapy of seasonal affective disorder: Time of day and suppression of melatonin are not critical for antidepressant effects. Arch. Gen. Psychiatry 43:9870–75 [Google Scholar]
  115. Wehr TA, Wirz-Justice A. 1982. Circadian rhythm mechanisms in affective illness and in antidepressant drug action. Pharmacopsychiatria 15:131–39 [Google Scholar]
  116. Welsh DK, Takahashi JS, Kay SA. 2010. Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 72:551–77 [Google Scholar]
  117. Wolkowitz OM, Burke H, Epel ES, Reus VI. 2009. Glucocorticoids: mood, memory, and mechanisms. Ann. N. Y. Acad. Sci. 1179:19–40 [Google Scholar]
  118. Woo JM, Okusaga O, Postolache TT. 2012. Seasonality of suicidal behavior. Int. J. Environ. Res. Public Health 9:2531–47 [Google Scholar]
  119. Yehuda R, Teicher MH, Trestman RL, Levengood RA, Siever LJ. 1996. Cortisol regulation in posttraumatic stress disorder and major depression: a chronobiological analysis. Biol. Psychiatry 40:279–88 [Google Scholar]
  120. Zaidi FH, Hull JT, Peirson SN, Wulff K, Aeschbach D. et al. 2007. Short-wavelength light sensitivity of circadian, pupillary, and visual awareness in humans lacking an outer retina. Curr. Biol. 17:242122–28 [Google Scholar]
  121. Zhao H, Rusak B. 2005. Circadian firing-rate rhythms and light responses of rat habenular nucleus neurons in vivo and in vitro. Neuroscience 132:2519–28 [Google Scholar]
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