Interactions of the serotonin and circadian systems: Nature and nurture in rhythms and blues

Neuroscience

Volumn 197, Issue , 2011, Pages 8-16

  Ciarleglio, C M ^a,b,c   Resuehr, H E S ^a,b   McMahon, D G ^a,b  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

5 HT; Development; Light; Mood disorders; Seasonality; Suprachiasmatic nucleus (SCN)

Indexed keywords

SEROTONIN;

AUTISM; BEHAVIOR DISORDER; BIPOLAR DISORDER; BRAIN NERVE CELL; CIRCADIAN RHYTHM; DEVELOPMENT; DEVELOPMENTAL DISORDER; DEVELOPMENTAL IMPRINTING; GENE EXPRESSION; GENE REGULATORY NETWORK; GENETIC DISORDER; HUMAN; LIGHT DARK CYCLE; MAJOR DEPRESSION; MOLECULAR GENETICS; MOOD DISORDER; NERVE CELL NETWORK; NEUROANATOMY; NEUROBEHAVIORAL DISORDER; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SEASONAL AFFECTIVE DISORDER; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; TRANSCRIPTION REGULATION;

ANIMALS; BRAIN; CIRCADIAN RHYTHM; HUMANS; MOOD DISORDERS; PHOTOPERIOD; SEROTONIN;

EID: 82855175127     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.09.036     Document Type: Review

References (114)

1. Abe M., Herzog E.D., Yamazaki S., Straume M., Tei H., Sakaki Y., Menaker M., Block G.D. Circadian rhythms in isolated brain regions. J Neurosci 2002, 22:350-356.
2. Amir S., Robinson B., Ratovitski T., Rea M.A., Stewart J., Simantov R. A role for serotonin in the circadian system revealed by the distribution of serotonin transporter and light-induced Fos immunoreactivity in the suprachiasmatic nucleus and intergeniculate leaflet. Neuroscience 1998, 84:1059-1073.
3. Ashkenazy T., Einat H., Kronfeld-Schor N. Effects of bright light treatment on depression- and anxiety-like behaviors of diurnal rodents maintained on a short daylight schedule. Behav Brain Res 2009, 201:343-346.
4. Ashkenazy T., Einat H., Kronfeld-Schor N. We are in the dark here: induction of depression- and anxiety-like behaviours in the diurnal fat sand rat, by short daylight or melatonin injections. Int J Neuropsychopharmacol 2009, 12:83-93.
5. Benedetti F., Serretti A., Colombo C., Barbini B., Lorenzi C., Campori E., Smeraldi E. Influence of CLOCK gene polymorphism on circadian mood fluctuation and illness recurrence in bipolar depression. Am J Med Genet B Neuropsychiatr Genet 2003, 123:23-26.
6. Boivin D.B. Influence of sleep-wake and circadian rhythm disturbances in psychiatric disorders. J Psychiatry Neurosci 2000, 25:446-458.
7. Bosler O. Ultrastructural relationships of serotonin and GABA terminals in the rat suprachiasmatic nucleus. Evidence for a close interconnection between the two afferent systems. J Neurocytol 1989, 18:105-113.
8. Bosler O., Beaudet A. VIP neurons as prime synaptic targets for serotonin afferents in rat suprachiasmatic nucleus: a combined radioautographic and immunocytochemical study. J Neurocytol 1985, 14:749-763.
9. Brown T.M., Piggins H.D. Spatiotemporal heterogeneity in the electrical activity of suprachiasmatic nuclei neurons and their response to photoperiod. J Biol Rhythms 2009, 24:44-54.
10. Cagampang F.R., Inouye S.T. Diurnal and circadian changes of serotonin in the suprachiasmatic nuclei: regulation by light and an endogenous pacemaker. Brain Res 1994, 639:175-179.
11. Cagampang F.R., Yamazaki S., Otori Y., Inouye S.I. Serotonin in the raphe nuclei: regulation by light and an endogenous pacemaker. Neuroreport 1993, 5:49-52.
12. Canal-Corretger M.M., Vilaplana J., Cambras T., Díez-Noguera A. Functioning of the rat circadian system is modified by light applied in critical postnatal days. Am J Physiol Regul Integr Comp Physiol 2001, 280:R1023-R1030.
13. Ciarleglio C.M., Axley J.C., Strauss B.R., Gamble K.L., McMahon D.G. Perinatal photoperiod imprints the circadian clock. Nat Neurosci 2011, 14:25-27.
14. Davis F.C., Menaker M. Development of the mouse circadiant pacemaker: independence from environmental cycles. J Comp Physiol [A] 1981, 143:527-539.
15. Deurveilher S., Semba K. Indirect projections from the suprachiasmatic nucleus to major arousal-promoting cell groups in rat: implications for the circadian control of behavioural state. Neuroscience 2005, 130:165-183.
16. Eastman C.I., Young M.A., Fogg L.F., Liu L., Meaden P.M. Bright light treatment of winter depression: a placebo-controlled trial. Arch Gen Psychiatry 1998, 55:883-889.
17. Edgar D.M., Martin C.E., Dement W.C. Activity feedback to the mammalian circadian pacemaker: influence on observed measures of rhythm period length. J Biol Rhythms 1991, 6:185-199.
18. Edgar D.M., Miller J.D., Prosser R.A., Dean R.R., Dement W.C. Serotonin and the mammalian circadian system: II. Phase-shifting rat behavioral rhythms with serotonergic agonists. J Biol Rhythms 1993, 8:17-31.
19. Einat H., Kronfeld-Schor N., Eilam D. Sand rats see the light: short photoperiod induces a depression-like response in a diurnal rodent. Behav Brain Res 2006, 173:153-157.
20. Foster R.G., Hankins M.W. Circadian vision. Curr Biol 2007, 17:R746-R751.
21. Geiser F., McAllan B.M., Kenagy G.J., Hiebert S.M. Photoperiod affects daily torpor and tissue fatty acid composition in deer mice. Naturwissenschaften 2007, 94:319-325.
22. Glass J.D., Grossman G.H., Farnbauch L., DiNardo L. Midbrain raphe modulation of nonphotic circadian clock resetting and 5-HT release in the mammalian suprachiasmatic nucleus. J Neurosci 2003, 23:7451-7460.
23. Goldman S.L., Goldman B.D. Early photoperiod history and short-day responsiveness in Siberian hamsters. J Exp Zool A Comp Exp Biol 2003, 296:38-45.
24. Gorwood P. Restoring circadian rhythms: a new way to successfully manage depression. J Psychopharmacol 2010, 24:15-19.
25. Guscott M., Bristow L.J., Hadingham K., Rosahl T.W., Beer M.S., Stanton J.A., Bromidge F., Owens A.P., Huscroft I., Myers J., Rupniak N.M., Patel S., Whiting P.J., Hutson P.H., Fone K.C., Biello S.M., Kulagowski J.J., McAllister G. Genetic knockout and pharmacological blockade studies of the 5-HT7 receptor suggest therapeutic potential in depression. Neuropharmacology 2005, 48:492-502.
26. Hanita T., Ohta H., Matsuda T., Miyazawa H. Monitoring preterm infants' vision development with light-only melanopsin is functional. J Pediatr 2009, 155(4). 596-596.e1.
27. Hao H., Rivkees S.A. The biological clock of very premature primate infants is responsive to light. Proc Natl Acad Sci U S A 1999, 96:2426-2429.
28. Hare E.H. Manic-depressive psychosis and season of birth. Acta Psychiatr Scand 1975, 52:69-79.
29. Hare E.H. Season of birth in schizophrenia and neurosis. Am J Psychiatry 1975, 132:1168-1171.
30. Hendricks T., Francis N., Fyodorov D., Deneris E.S. The ETS domain factor Pet-1 is an early and precise marker of central serotonin neurons and interacts with a conserved element in serotonergic genes. J Neurosci 1999, 19:10348-10356.
31. Hendricks T.J., Fyodorov D.V., Wegman L.J., Lelutiu N.B., Pehek E.A., Yamamoto B., Silver J., Weeber E.J., Sweatt J.D., Deneris E.S. Pet-1 ETS gene plays a critical role in 5-HT neuron development and is required for normal anxiety-like and aggressive behavior. Neuron 2003, 37:233-247.
32. Hsu J.L., Yu L., Sullivan E., Bowman M., Mistlberger R.E., Tecott L.H. Enhanced food anticipatory activity associated with enhanced activation of extrahypothalamic neural pathways in serotonin2C receptor null mutant mice. PLoS One 2010, 5:e11802.
33. Hu V.W., Sarachana T., Kim K.S., Nguyen A., Kulkarni S., Steinberg M.E., Luu T., Lai Y., Lee N.H. Gene expression profiling differentiates autism case-controls and phenotypic variants of autism spectrum disorders: evidence for circadian rhythm dysfunction in severe autism. Autism Res 2009, 2:78-97.
34. Hubel D.H., Wiesel T.N. Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J Neurophysiol 1963, 26:994-1002.
35. Inagaki N., Honma S., Ono D., Tanahashi Y., Honma K. Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity. Proc Natl Acad Sci U S A 2007, 104:7664-7669.
36. Johansson C., Willeit M., Levitan R., Partonen T., Smedh C., Del Favero J., Bel Kacem S., Praschak-Rieder N., Neumeister A., Masellis M., Basile V., Zill P., Bondy B., Paunio T., Kasper S., Van Broeckhoven C., Nilsson L.G., Lam R., Schalling M., Adolfsson R. The serotonin transporter promoter repeat length polymorphism, seasonal affective disorder and seasonality. Psychol Med 2003, 33:785-792.
37. Johansson C., Willeit M., Smedh C., Ekholm J., Paunio T., Kieseppa T., Lichtermann D., Praschak-Rieder N., Neumeister A., Nilsson L.G., Kasper S., Peltonen L., Adolfsson R., Schalling M., Partonen T. Circadian clock-related polymorphisms in seasonal affective disorder and their relevance to diurnal preference. Neuropsychopharmacology 2003, 28:734-739.
38. Kalbitzer J., Erritzoe D., Holst K.K., Nielsen F.A., Marner L., Lehel S., Arentzen T., Jernigan T.L., Knudsen G.M. Seasonal changes in brain serotonin transporter binding in short serotonin transporter linked polymorphic region-allele carriers but not in long-allele homozygotes. Biol Psychiatry 2010, 67:1033-1039.
39. Kiss J., Léránth C., Halász B. Serotoninergic endings on VIP-neurons in the suprachiasmatic nucleus and on ACTH-neurons in the arcuate nucleus of the rat hypothalamus. A combination of high resolution autoradiography and electron microscopic immunocytochemistry. Neurosci Lett 1984, 44:119-124.
40. Kripke D.F. Light treatment for nonseasonal depression: speed, efficacy, and combined treatment. J Affect Disord 1998, 49:109-117.
41. Kuhlman S.J., Quintero J.E., McMahon D.G. GFP fluorescence reports period 1 circadian gene regulation in the mammalian biological clock. Neuroreport 2000, 11:1479-1482.
42. Lam R.W., Levitt A.J., Levitan R.D., Enns M.W., Morehouse R., Michalak E.E., Tam E.M. The Can-SAD study: a randomized controlled trial of the effectiveness of light therapy and fluoxetine in patients with winter seasonal affective disorder. Am J Psychiatry 2006, 163:805-812.
43. Lambert G.W., Reid C., Kaye D.M., Jennings G.L., Esler M.D. Effect of sunlight and season on serotonin turnover in the brain. Lancet 2002, 360:1840-1842.
44. Lavebratt C., Sjoholm L.K., Partonen T., Schalling M., Forsell Y. PER2 variation is associated with depression vulnerability. Am J Med Genet B Neuropsychiatr Genet 2010, 153B:570-581.
45. Lavebratt C., Sjoholm L.K., Soronen P., Paunio T., Vawter M.P., Bunney W.E., Adolfsson R., Forsell Y., Wu J.C., Kelsoe J.R., Partonen T., Schalling M. CRY2 is associated with depression. PLoS One 2010, 5:e9407.
46. Lee H.J., Sung S.M., Lim S.W., Paik J.W., Leen K. Seasonality associated with the serotonin 2A receptor-1438 a/g polymorphism. J Affect Disord 2006, 95:145-148.
47. Le-Niculescu H., Patel S.D., Bhat M., Kuczenski R., Faraone S.V., Tsuang M.T., McMahon F.J., Schork N.J., Nurnberger J.I., Niculescu A.B. Convergent functional genomics of genome-wide association data for bipolar disorder: comprehensive identification of candidate genes, pathways and mechanisms. Am J Med Genet B Neuropsychiatr Genet 2009, 150B:155-181.
48. Lewy A.J., Bauer V.K., Cutler N.L., Sack R.L., Ahmed S., Thomas K.H., Blood M.L., Jackson J.M. Morning vs evening light treatment of patients with winter depression. Arch Gen Psychiatry 1998, 55:890-896.
49. Lewy A.J., Lefler B.J., Emens J.S., Bauer V.K. The circadian basis of winter depression. Proc Natl Acad Sci U S A 2006, 103:7414-7419.
50. Lovenberg T.W., Baron B.M., de Lecea L., Miller J.D., Prosser R.A., Rea M.A., Foye P.E., Racke M., Slone A.L., Siegel B.W., et al. A novel adenylyl cyclase-activating serotonin receptor (5-HT7) implicated in the regulation of mammalian circadian rhythms. Neuron 1993, 11:449-458.
51. Loving R.T., Kripke D.F., Shuchter S.R. Bright light augments antidepressant effects of medication and wake therapy. Depress Anxiety 2002, 16:1-3.
52. Malek Z.S., Dardente H., Pevet P., Raison S. Tissue-specific expression of tryptophan hydroxylase mRNAs in the rat midbrain: anatomical evidence and daily profiles. Eur J Neurosci 2005, 22:895-901.
53. Malek Z.S., Sage D., Pévet P., Raison S. Daily rhythm of tryptophan hydroxylase-2 messenger ribonucleic acid within raphe neurons is induced by corticoid daily surge and modulated by enhanced locomotor activity. Endocrinology 2007, 148:5165-5172.
54. Manrique C., François-Bellan A.M., Segu L., Becquet D., Héry M., Faudon M., Héry F. Impairment of serotoninergic transmission is followed by adaptive changes in 5HT1B binding sites in the rat suprachiasmatic nucleus. Brain Res 1994, 663:93-100.
55. Manrique C., Segu L., Héry F., Héry M., Faudon M., François-Bellan A.M. Increase of central 5-HT1B binding sites following 5,7-dihydroxytryptamine axotomy in the adult rat. Brain Res 1993, 623:345-348.
56. Matejù K., Bendová Z., El-Hennamy R., Sládek M., Sosniyenko S., Sumová A. Development of the light sensitivity of the clock genes Period1 and Period2, and immediate-early gene c-fos within the rat suprachiasmatic nucleus. Eur J Neurosci 2009, 29:490-501.
57. Mino Y., Oshima I., Okagami K. Seasonality of birth in patients with mood disorders in Japan. J Affect Disord 2000, 59:41-46.
58. Mistlberger R.E., Bossert J.M., Holmes M.M., Marchant E.G. Serotonin and feedback effects of behavioral activity on circadian rhythms in mice. Behav Brain Res 1998, 96:93-99.
59. Molnar E., Lazary J., Benko A., Gonda X., Pap D., Mekli K., Juhasz G., Kovacs G., Kurimay T., Rihmer Z., Bagdy G. Seasonality and winter-type seasonal depression are associated with the rs731779 polymorphism of the serotonin-2A receptor gene. Eur Neuropsychopharmacol 2010, 20:655-662.
60. Morin L.P., Allen C.N. The circadian visual system. Brain Res Rev 2006, 51:1-60.
61. Naito E., Watanabe T., Tei H., Yoshimura T., Ebihara S. Reorganization of the suprachiasmatic nucleus coding for day length. J Biol Rhythms 2008, 23:140-149.
62. Natale V., Adan A., Chotai J. Season of birth modulates mood seasonality in humans. Psychiatry Res 2007, 153:199-201.
63. Nexon L., Poirel V.J., Clesse D., Pévet P., Raison S. Complex regional influence of photoperiod on the nycthemeral functioning of the dorsal and median raphé serotoninergic system in the Syrian hamster. Eur J Neurosci 2009, 30:1790-1801.
64. Nexon L., Sage D., Pévet P., Raison S. Glucocorticoid-mediated nycthemeral and photoperiodic regulation of tph2 expression. Eur J Neurosci 2011, 33:1308-1317.
65. Ohta H., Mitchell A.C., McMahon D.G. Constant light disrupts the developing mouse biological clock. Pediatr Res 2006, 60:304-308.
66. Ossenkopp K.P., van Anders S.M., Engeland C.G., Kavaliers M. Influence of photoperiod and sex on locomotor behavior of meadow voles (Microtus pennsylvanicus) in an automated light-dark "anxiety" test. Psychoneuroendocrinology 2005, 30:869-879.
67. Pae C.U., Masand P.S., Peindl K., Mannelli P., Han C., Marks D.M., Patkar A.A. An open-label, rater-blinded, flexible-dose, 8-week trial of escitalopram in patients with major depressive disorder with atypical features. Prim Care Companion J Clin Psychiatry 2008, 10:205-210.
68. Partonen T., Treutlein J., Alpman A., Frank J., Johansson C., Depner M., Aron L., Rietschel M., Wellek S., Soronen P., Paunio T., Koch A., Chen P., Lathrop M., Adolfsson R., Persson M.L., Kasper S., Schalling M., Peltonen L., Schumann G. Three circadian clock genes Per2, Arntl, and Npas2 contribute to winter depression. Ann Med 2007, 39:229-238.
69. Pickard G.E., Rea M.A. TFMPP, a 5HT1B receptor agonist, inhibits light-induced phase shifts of the circadian activity rhythm and c-Fos expression in the mouse suprachiasmatic nucleus. Neurosci Lett 1997, 231:95-98.
70. Pickard G.E., Smith B.N., Belenky M., Rea M.A., Dudek F.E., Sollars P.J. 5-HT1B receptor-mediated presynaptic inhibition of retinal input to the suprachiasmatic nucleus. J Neurosci 1999, 19:4034-4045.
71. Pickard G.E., Weber E.T., Scott P.A., Riberdy A.F., Rea M.A. 5HT1B receptor agonists inhibit light-induced phase shifts of behavioral circadian rhythms and expression of the immediate-early gene c-fos in the suprachiasmatic nucleus. J Neurosci 1996, 16:8208-8220.
72. Pittendrigh C., Daan S. A functional analysis of circadian pacemakers in nocturnal rodents: part V. Pacemaker structure: a clock for all seasons. J Comp Physiol A 1976, 106:333-355.
73. Pjrek E., Konstantinidis A., Assem-Hilger E., Praschak-Rieder N., Willeit M., Kasper S., Winkler D. Therapeutic effects of escitalopram and reboxetine in seasonal affective disorder: a pooled analysis. J Psychiatr Res 2009, 43:792-797.
74. Pjrek E., Winkler D., Heiden A., Praschak-Rieder N., Willeit M., Konstantinidis A., Stastny J., Kasper S. Seasonality of birth in seasonal affective disorder. J Clin Psychiatry 2004, 65:1389-1393.
75. Praschak-Rieder N., Willeit M., Wilson A.A., Houle S., Meyer J.H. Seasonal variation in human brain serotonin transporter binding. Arch Gen Psychiatry 2008, 65:1072-1078.
76. Prendergast B.J., Kay L.M. Affective and adrenocorticotrophic responses to photoperiod in Wistar rats. J Neuroendocrinol 2008, 20:261-267.
77. Prendergast B.J., Nelson R.J. Affective responses to changes in day length in Siberian hamsters (Phodopus sungorus). Psychoneuroendocrinology 2005, 30:438-452.
78. Prosser R.A., Dean R.R., Edgar D.M., Heller H.C., Miller J.D. Serotonin and the mammalian circadian system: I. In vitro phase shifts by serotonergic agonists and antagonists. J Biol Rhythms 1993, 8:1-16.
79. Pyter L.M., Adelson J.D., Nelson R.J. Short days increase hypothalamic-pituitary-adrenal axis responsiveness. Endocrinology 2007, 148:3402-3409.
80. Pyter L.M., Nelson R.J. Enduring effects of photoperiod on affective behaviors in Siberian hamsters (Phodopus sungorus). Behav Neurosci 2006, 120:125-134.
81. Pyter L.M., Samuelsson A.R., Quan N., Nelson R.J. Photoperiod alters hypothalamic cytokine gene expression and sickness responses following immune challenge in female Siberian hamsters (Phodopus sungorus). Neuroscience 2005, 131:779-784.
82. Quintero J.E., McMahon D.G. Serotonin modulates glutamate responses in isolated suprachiasmatic nucleus neurons. J Neurophysiol 1999, 82:533-539.
83. Rea M.A., Pickard G.E. A 5-HT(1B) receptor agonist inhibits light-induced suppression of pineal melatonin production. Brain Res 2000, 858:424-428.
84. Reppert S.M., Duncan M.J., Goldman B.D. Photic influences on the developing mammal. Ciba Found Symp 1985, 117:116-128.
85. Rohling J., Meijer J.H., VanderLeest H.T., Admiraal J. Phase differences between SCN neurons and their role in photoperiodic encoding; a simulation of ensemble patterns using recorded single unit electrical activity patterns. J Physiol Paris 2006, 100:261-270.
86. Rosenthal N.E., Mazzanti C.M., Barnett R.L., Hardin T.A., Turner E.H., Lam G.K., Ozaki N., Goldman D. Role of serotonin transporter promoter repeat length polymorphism (5-HTTLPR) in seasonality and seasonal affective disorder. Mol Psychiatry 1998, 3:175-177.
87. Rossignol D.A., Frye R.E. Melatonin in autism spectrum disorders: a systematic review and meta-analysis. Dev Med Child Neurol 2011, 53:783-792.
88. Ruhrmann S., Kasper S., Hawellek B., Martinez B., Höflich G., Nickelsen T., Möller H.J. Effects of fluoxetine versus bright light in the treatment of seasonal affective disorder. Psychol Med 1998, 28:923-933.
89. Sacco R., Curatolo P., Manzi B., Militerni R., Bravaccio C., Frolli A., Lenti C., Saccani M., Elia M., Reichelt K.L., Pascucci T., Puglisi-Allegra S., Persico A.M. Principal pathogenetic components and biological endophenotypes in autism spectrum disorders. Autism Res 2010, 3:237-252.
90. Siebert U., Wollnik F. Effect of photoperiod on the development of wheel-running activity rhythms in LEW/Ztm rats. Physiol Behav 1993, 53:1145-1150.
91. Smith B.N., Sollars P.J., Dudek F.E., Pickard G.E. Serotonergic modulation of retinal input to the mouse suprachiasmatic nucleus mediated by 5-HT1B and 5-HT7 receptors. J Biol Rhythms 2001, 16:25-38.
92. Smith V.M., Sterniczuk R., Phillips C.I., Antle M.C. Altered photic and non-photic phase shifts in 5-HT(1A) receptor knockout mice. Neuroscience 2008, 157:513-523.
93. Sollars P.J., Ogilvie M.D., Simpson A.M., Pickard G.E. Photic entrainment is altered in the 5-HT1B receptor knockout mouse. J Biol Rhythms 2006, 21:21-32.
94. Sollars P.J., Simpson A.M., Ogilvie M.D., Pickard G.E. Light-induced Fos expression is attenuated in the suprachiasmatic nucleus of serotonin 1B receptor knockout mice. Neurosci Lett 2006, 401:209-213.
95. Soria V., Martinez-Amoros E., Escaramis G., Valero J., Perez-Egea R., Garcia C., Gutierrez-Zotes A., Puigdemont D., Bayes M., Crespo J.M., Martorell L., Vilella E., Labad A., Vallejo J., Perez V., Menchon J.M., Estivill X., Gratacos M., Urretavizcaya M. Differential association of circadian genes with mood disorders: CRY1 and NPAS2 are associated with unipolar major depression and CLOCK and VIP with bipolar disorder. Neuropsychopharmacology 2010, 35:1279-1289.
96. Sprouse J., Li X., Stock J., McNeish J., Reynolds L. Circadian rhythm phenotype of 5-HT7 receptor knockout mice: 5-HT and 8-OH-DPAT-induced phase advances of SCN neuronal firing. J Biol Rhythms 2005, 20:122-131.
97. Sumová A., Trávnícková Z., Peters R., Schwartz W.J., Illnerová H. The rat suprachiasmatic nucleus is a clock for all seasons. Proc Natl Acad Sci U S A 1995, 92:7754-7758.
98. Takahashi J.S., Hong H.K., Ko C.H., McDearmon E.L. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 2008, 9:764-775.
99. Terman J.S., Terman M., Lo E.S., Cooper T.B. Circadian time of morning light administration and therapeutic response in winter depression. Arch Gen Psychiatry 2001, 58:69-75.
100. Terracciano A., Tanaka T., Sutin A.R., Sanna S., Deiana B., Lai S., Uda M., Schlessinger D., Abecasis G.R., Ferrucci L., Costa P.T. Genome-wide association scan of trait depression. Biol Psychiatry 2010, 68:811-817.
101. Trávnícková Z., Sumová A., Peters R., Schwartz W.J., Illnerová H. Photoperiod-dependent correlation between light-induced SCN c-fos expression and resetting of circadian phase. Am J Physiol 1996, 271:R825-R831.
102. VanderLeest H.T., Houben T., Michel S., Deboer T., Albus H., Vansteensel M.J., Block G.D., Meijer J.H. Seasonal encoding by the circadian pacemaker of the SCN. Curr Biol 2007, 17:468-473.
103. Vansteensel M.J., Michel S., Meijer J.H. Organization of cell and tissue circadian pacemakers: a comparison among species. Brain Res Rev 2008, 58:18-47.
104. Weil Z.M., Martin L.B., Nelson R.J. Photoperiod differentially affects immune function and reproduction in collared lemmings (Dicrostonyx groenlandicus). J Biol Rhythms 2006, 21:384-393.
105. Weil Z.M., Pyter L.M., Martin L.B., Nelson R.J. Perinatal photoperiod organizes adult immune responses in Siberian hamsters (Phodopus sungorus). Am J Physiol Regul Integr Comp Physiol 2006, 290:R1714-R1719.
106. Wiesel T.N., Hubel D.H. Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. J Neurophysiol 1963, 26:978-993.
107. Wiesel T.N., Hubel D.H. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 1963, 26:1003-1017.
108. Willeit M., Praschak-Rieder N., Neumeister A., Zill P., Leisch F., Stastny J., Hilger E., Thierry N., Konstantinidis A., Winkler D., Fuchs K., Sieghart W., Aschauer H., Ackenheil M., Bondy B., Kasper S. A polymorphism (5-HTTLPR) in the serotonin transporter promoter gene is associated with DSM-IV depression subtypes in seasonal affective disorder. Mol Psychiatry 2003, 8:942-946.
109. Willeit M., Sitte H.H., Thierry N., Michalek K., Praschak-Rieder N., Zill P., Winkler D., Brannath W., Fischer M.B., Bondy B., Kasper S., Singer E.A. Enhanced serotonin transporter function during depression in seasonal affective disorder. Neuropsychopharmacology 2008, 33:1503-1513.
110. Wirz-Justice A. Biological rhythm disturbances in mood disorders. Int Clin Psychopharmacol 2006, 21(Suppl 1):S11-S15.
111. Wirz-Justice A., Graw P., Kräuchi K., Gisin B., Jochum A., Arendt J., Fisch H.U., Buddeberg C., Pöldinger W. Light therapy in seasonal affective disorder is independent of time of day or circadian phase. Arch Gen Psychiatry 1993, 50:929-937.
112. Wirz-Justice A., Quinto C., Cajochen C., Werth E., Hock C. A rapid-cycling bipolar patient treated with long nights, bedrest, and light. Biol Psychiatry 1999, 45:1075-1077.
113. Wirz-Justice A., Schmid A.C., Graw P., Kräuchi K., Kielholz P., Pöldinger W., Fisch H.U., Buddeberg C. Dose relationships of morning bright white light in seasonal affective disorders (SAD). Experientia 1987, 43:574-576.
114. Wulff K., Gatti S., Wettstein J.G., Foster R.G. Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nat Rev Neurosci 2010, 11:589-599.