Verwey, Michael, Dhir, Sabine and Amir, Shimon ORCID: https://orcid.org/0000-0003-1919-5023 (2016) Circadian influences on dopamine circuits of the brain: regulation of striatal rhythms of clock gene expression and implications for psychopathology and disease. F1000Research, 5 (2062). pp. 1-11. ISSN 2046-1402
Preview |
Text (Publisher's version) (application/pdf)
841kBAmir-f1000R-2016.pdf - Published Version Available under License Spectrum Terms of Access. |
Official URL: http://dx.doi.org/10.12688/f1000research.9180.1
Abstract
Circadian clock proteins form an autoregulatory feedback loop that is central to the endogenous generation and transmission of daily rhythms in behavior and physiology. Increasingly, circadian rhythms in clock gene expression are being reported in diverse tissues and brain regions that lie outside of the suprachiasmatic nucleus (SCN), the master circadian clock in mammals. For many of these extra-SCN rhythms, however, the region-specific implications are still emerging. In order to gain important insights into the potential behavioral, physiological, and psychological relevance of these daily oscillations, researchers have begun to focus on describing the neurochemical, hormonal, metabolic, and epigenetic contributions to the regulation of these rhythms. This review will highlight important sites and sources of circadian control within dopaminergic and striatal circuitries of the brain and will discuss potential implications for psychopathology and disease. For example, rhythms in clock gene expression in the dorsal striatum are sensitive to changes in dopamine release, which has potential implications for Parkinson’s disease and drug addiction. Rhythms in the ventral striatum and limbic forebrain are sensitive to psychological and physical stressors, which may have implications for major depressive disorder. Collectively, a rich circadian tapestry has emerged that forces us to expand traditional views and to reconsider the psychopathological, behavioral, and physiological importance of these region-specific rhythms in brain areas that are not immediately linked with the regulation of circadian rhythms.
Divisions: | Concordia University > Research Units > Centre for Studies in Behavioural Neurobiology |
---|---|
Item Type: | Article |
Refereed: | Yes |
Authors: | Verwey, Michael and Dhir, Sabine and Amir, Shimon |
Journal or Publication: | F1000Research |
Date: | 2016 |
Funders: |
|
Digital Object Identifier (DOI): | 10.12688/f1000research.9180.1 |
ID Code: | 983746 |
Deposited By: | Monique Lane |
Deposited On: | 13 Apr 2018 17:58 |
Last Modified: | 13 Apr 2018 17:58 |
References:
1. Aschoff J: Exogenous and endogenous components in circadian rhythms. Cold Spring Harb Symp Quant Biol. 1960; 25: 11–28.2. Pittendrigh CS: Circadian rhythms and the circadian organization of living systems. Cold Spring Harb Symp Quant Biol. 1960; 25: 159–84.
3. Pittendrigh CS, Daan S: A functional analysis of circadian pacemakers in nocturnal rodents. I. The stability and lability of spontaneous frequency. J Comp Physiol. 1976; 106(3): 223–52.
4. Daan S, Pittendrigh CS: A Functional analysis of circadian pacemakers in nocturnal rodents. II. The variability of phase response curves. J Comp Physiol. 1976; 106(3): 253–66.
5. Daan S, Pittendrigh CS: A functional analysis of circadian pacemakers in nocturnal rodents. III. Heavy water and constant light: Homeostasis of frequency? J Comp Physiol. 1976; 106(3): 267–90.
6. Pittendrigh CS, Daan S: A functional analysis of circadian pacemakers in nocturnal rodents. IV. Entrainment: Pacemaker as clock. J Comp Physiol. 1976; 106(3): 291–331.
7. Pittendrigh CS, Daan S: A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: A clock for all seasons. J Comp Physiol. 1976; 106(3): 333–55.
8. Moore RY, Eichler VB: Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res. 1972; 42(1): 201–6.
9. Stephan FK, Zucker I: Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci U S A. 1972; 69(6): 1583–6.
10. Rusak B, Groos G: Suprachiasmatic stimulation phase shifts rodent circadian rhythms. Science. 1982; 215(4538): 1407–9.
11. Ralph MR, Foster RG, Davis FC, et al.: Transplanted suprachiasmatic nucleus determines circadian period. Science. 1990; 247(4945): 975–8. PubMed Abstract | Publisher Full Text
12. Reppert SM, Weaver DR: Coordination of circadian timing in mammals. Nature. 2002; 418(6901): 935–41.
13. Sato TK, Panda S, Miraglia LJ, et al.: A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron. 2004; 43(4): 527–37.
14. Oster H, Damerow S, Kiessling S, et al.: The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. Cell Metab. 2006; 4(2): 163–73.
15. DeBruyne JP, Weaver DR, Reppert SM: CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat Neurosci. 2007; 10(5): 543–5.
16. Kornmann B, Schaad O, Bujard H, et al.: System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol. 2007; 5(2): e34.
17. Yamazaki S, Numano R, Abe M, et al.: Resetting central and peripheral circadian oscillators in transgenic rats. Science. 2000; 288(5466): 682–5.
18. Abe M, Herzog ED, Yamazaki S, et al.: Circadian rhythms in isolated brain regions. J Neurosci. 2002; 22(1): 350–6.
19. Shieh K: Distribution of the rhythm-related genes rPERIOD1, rPERIOD2, and rCLOCK, in the rat brain. Neuroscience. 2003; 118(3): 831–43.
20. Amir S, Lamont EW, Robinson B, et al.: A circadian rhythm in the expression of PERIOD2 protein reveals a novel SCN-controlled oscillator in the oval nucleus of the bed nucleus of the stria terminalis. J Neurosci. 2004; 24(4): 781–90.
21. Granados-Fuentes D, Prolo LM, Abraham U, et al.: The suprachiasmatic nucleus entrains, but does not sustain, circadian rhythmicity in the olfactory bulb. J Neurosci. 2004; 24(3): 615–9.
22. Yoo SH, Yamazaki S, Lowrey PL, et al.: PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A. 2004; 101(15): 5339–46.
23. Lamont EW, Robinson B, Stewart J, et al.: The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proc Natl Acad Sci U S A. 2005; 102(11): 4180–4.
24. Harbour VL, Weigl Y, Robinson B, et al.: Comprehensive mapping of regional expression of the clock protein PERIOD2 in rat forebrain across the 24-h day. PLoS One. 2013; 8(10): e76391.
25. Logan RW, Edgar N, Gillman AG, et al.: Chronic Stress Induces Brain Region-Specific Alterations of Molecular Rhythms that Correlate with Depression-like Behavior in Mice. Biol Psychiatry. 2015; 78(4): 249–58.
26. Martino TA, Tata N, Belsham DD, et al.: Disturbed diurnal rhythm alters gene expression and exacerbates cardiovascular disease with rescue by resynchronization. Hypertension. 2007; 49(5): 1104–13.
27. Martino TA, Oudit GY, Herzenberg AM, et al.: Circadian rhythm disorganization produces profound cardiovascular and renal disease in hamsters. Am J Physiol Regul Integr Comp Physiol. 2008; 294(5): R1675–83.
28. Takahashi JS, Hong HK, Ko CH, et al.: The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet. 2008; 9(10): 764–75.
29. Provencio I, Rodriguez IR, Jiang G, et al.: A novel human opsin in the inner retina. J Neurosci. 2000; 20(2): 600–5.
30. Gooley JJ, Lu J, Chou TC, et al.: Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci. 2001; 4(12): 1165.
31. Hattar S, Liao HW, Takao M, et al.: Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science. 2002; 295(5557): 1065–70.
32. Panda S, Sato TK, Castrucci AM, et al.: Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science. 2002; 298(5601): 2213–6.
33. Abe H, Honma S, Namihira M, et al.: Phase-dependent induction by light of rat Clock gene expression in the suprachiasmatic nucleus. Brain Res Mol Brain Res. 1999; 66(1–2): 104–10.
34. Amaral FG, Castrucci AM, Cipolla-Neto J, et al.: Environmental control of biological rhythms: effects on development, fertility and metabolism. J Neuroendocrinol. 2014; 26(9): 603–12.
35. Boivin DB, Boudreau P: Impacts of shift work on sleep and circadian rhythms. Pathol Biol (Paris). 2014; 62(5): 292–301.
36. Cho Y, Ryu SH, Lee BR, et al.: Effects of artificial light at night on human health: A literature review of observational and experimental studies applied to exposure assessment. Chronobiol Int. 2015; 32(9): 1294–310.
37. Masubuchi S, Honma S, Abe H, et al.: Clock genes outside the suprachiasmatic nucleus involved in manifestation of locomotor activity rhythm in rats. Eur J Neurosci. 2000; 12(12): 4206–14.
38. Asai M, Yoshinobu Y, Kaneko S, et al.: Circadian profile of Per gene mRNA expression in the suprachiasmatic nucleus, paraventricular nucleus, and pineal body of aged rats. J Neurosci Res. 2001; 66(6): 1133–9.
39. Wang LM, Dragich JM, Kudo T, et al.: Expression of the circadian clock gene Period2 in the hippocampus: possible implications for synaptic plasticity and learned behaviour. ASN Neuro. 2009; 1(3): pii: e00012.
40. Inouye ST, Kawamura H: Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. Proc Natl Acad Sci U S A. 1979; 76(11): 5962–6.
41. Segall LA, Perrin JS, Walker CD, et al.: Glucocorticoid rhythms control the rhythm of expression of the clock protein, Period2, in oval nucleus of the bed nucleus of the stria terminalis and central nucleus of the amygdala in rats. Neuroscience. 2006; 140(3): 753–7.
42. Verwey M, Khoja Z, Stewart J, et al.: Differential regulation of the expression of Period2 protein in the limbic forebrain and dorsomedial hypothalamus by daily limited access to highly palatable food in food-deprived and free-fed rats. Neuroscience. 2007; 147(2): 277–85.
43. Verwey M, Khoja Z, Stewart J, et al.: Region-specific modulation of PER2 expression in the limbic forebrain and hypothalamus by nighttime restricted feeding in rats. Neurosci Lett. 2008; 440(1): 54–8.
44. Buhr ED, Yoo SH, Takahashi JS: Temperature as a universal resetting cue for mammalian circadian oscillators. Science. 2010; 330(6002): 379–85.
45. Hood S, Cassidy P, Cossette MP, et al.: Endogenous dopamine regulates the rhythm of expression of the clock protein PER2 in the rat dorsal striatum via daily activation of D2 dopamine receptors. J Neurosci. 2010; 30(42): 14046–58.
46. Granados-Fuentes D, Saxena MT, Prolo LM, et al.: Olfactory bulb neurons express functional, entrainable circadian rhythms. Eur J Neurosci. 2004; 19(4): 898–906.
47. Granados-Fuentes D, Tseng A, Herzog ED: A circadian clock in the olfactory bulb controls olfactory responsivity. J Neurosci. 2006; 26(47): 12219–25.
48. Loh DH, Navarro J, Hagopian A, et al.: Rapid changes in the light/dark cycle disrupt memory of conditioned fear in mice. PLoS One. 2010; 5(9): pii: e12546.
49. Abarca C, Albrecht U, Spanagel R: Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc Natl Acad Sci U S A. 2002; 99(13): 9026–30. PubMed Abstract | Publisher Full Text | Free Full Text
50. McClung CA, Sidiropoulou K, Vitaterna M, et al.: Regulation of dopaminergic transmission and cocaine reward by the Clock gene. Proc Natl Acad Sci U S A. 2005; 102(26): 9377–81.
51. Rutter J, Reick M, McKnight SL: Metabolism and the control of circadian rhythms. Annu Rev Biochem. 2002; 71: 307–31.
52. Inoue I, Shinoda Y, Ikeda M, et al.: CLOCK/BMAL1 is involved in lipid metabolism via transactivation of the peroxisome proliferator-activated receptor (PPAR) response element. J Atheroscler Thromb. 2005; 12(3): 169–74.
53. Satoh Y, Kawai H, Kudo N, et al.: Time-restricted feeding entrains daily rhythms of energy metabolism in mice. Am J Physiol Regul Integr Comp Physiol. 2006; 290(5): R1276–83.
54. Sonoda J, Mehl IR, Chong LW, et al.: PGC-1beta controls mitochondrial metabolism to modulate circadian activity, adaptive thermogenesis, and hepatic steatosis. Proc Natl Acad Sci U S A. 2007; 104(12): 5223–8.
55. Green CB, Takahashi JS, Bass J: The meter of metabolism. Cell. 2008; 134(5): 728–42.
56. Karatsoreos IN, Bhagat S, Bloss EB, et al.: Disruption of circadian clocks has ramifications for metabolism, brain, and behavior. Proc Natl Acad Sci U S A. 2011; 108(4): 1657–62.
57. Verwey M, Amir S: Food-entrainable circadian oscillators in the brain. Eur J Neurosci. 2009; 30(9): 1650–7.
58. Krieger DT, Hauser H, Krey LC: Suprachiasmatic nuclear lesions do not abolish food-shifted circadian adrenal and temperature rhythmicity. Science. 1977; 197(4301): 398–9.
59. Stephan FK: The "other" circadian system: food as a Zeitgeber. J Biol Rhythms. 2002; 17(4): 284–92.
60. Fuller PM, Lu J, Saper CB: Differential rescue of light- and food-entrainable circadian rhythms. Science. 2008; 320(5879): 1074–7.
61. Mistlberger RE, Buijs RM, Challet E, et al.: Standards of evidence in chronobiology: critical review of a report that restoration of Bmal1 expression in the dorsomedial hypothalamus is sufficient to restore circadian food anticipatory rhythms in Bmal1-/- mice. J Circadian Rhythms. 2009; 7: 3.
62. Feillet CA, Ripperger JA, Magnone MC, et al.: Lack of food anticipation in Per2 mutant mice. Curr Biol. 2006; 16(20): 2016–22.
63. Storch KF, Weitz CJ: Daily rhythms of food-anticipatory behavioral activity do not require the known circadian clock. Proc Natl Acad Sci U S A. 2009; 106(16): 6808–13.
64. Arble DM, Bass J, Laposky AD, et al.: Circadian timing of food intake contributes to weight gain. Obesity (Silver Spring). 2009; 17(11): 2100–2.
65. Segall LA, Milet A, Tronche F, et al.: Brain glucocorticoid receptors are necessary for the rhythmic expression of the clock protein, PERIOD2, in the central extended amygdala in mice. Neurosci Lett. 2009; 457(1): 58–60.
66. Segall LA, Amir S: Glucocorticoid regulation of clock gene expression in the mammalian limbic forebrain. J Mol Neurosci. 2010; 42(2): 168–75.
67. Al-Safadi S, Al-Safadi A, Branchaud M, et al.: Stress-induced changes in the expression of the clock protein PERIOD1 in the rat limbic forebrain and hypothalamus: role of stress type, time of day, and predictability. PLoS One. 2014; 9(10): e111166.
68. Al-Safadi S, Branchaud M, Rutherford S, et al.: Glucocorticoids and Stress-Induced Changes in the Expression of PERIOD1 in the Rat Forebrain. PLoS One. 2015; 10(6): e0130085.
69. Wade PA, Pruss D, Wolffe AP: Histone acetylation: Chromatin in action. Trends Biochem Sci. 1997; 22(4): 128–32.
70. Shilatifard A: Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem. 2006; 75: 243–69.
71. Masri S, Orozco-Solis R, Aguilar-Arnal L, et al.: Coupling circadian rhythms of metabolism and chromatin remodelling. Diabetes Obes Metab. 2015; 17(Suppl 1): 17–22.
72. Doi M, Hirayama J, Sassone-Corsi P: Circadian regulator CLOCK is a histone acetyltransferase. Cell. 2006; 125(3): 497–508.
73. Workman JL, Kingston RE: Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem. 1998; 67: 545–79.
74. Naruse Y, Oh-hashi K, Iijima N, et al.: Circadian and light-induced transcription of clock gene Per1 depends on histone acetylation and deacetylation. Mol Cell Biol. 2004; 24(14): 6278–87.
75. FDuong HA, Robles MS, Knutti D, et al.: A molecular mechanism for circadian clock negative feedback. Science. 2011; 332(6036): 1436–9.
76. Ramsey KM, Yoshino J, Brace CS, et al.: Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science. 2009; 324(5927): 651–4.
77. Asher G, Gatfield D, Stratmann M, et al.: SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell. 2008; 134(2): 317–28.
78. Belden WJ, Dunlap JC: SIRT1 is a circadian deacetylase for core clock components. Cell. 2008; 134(2): 212–4.
79. Masri S, Rigor P, Cervantes M, et al.: Partitioning circadian transcription by SIRT6 leads to segregated control of cellular metabolism. Cell. 2014; 158(3): 659–72.
80. Wise RA: Dopamine, learning and motivation. Nat Rev Neurosci. 2004; 5(6): 483–94.
81. Iuvone PM, Galli CL, Garrison-Gund CK, et al.: Light stimulates tyrosine hydroxylase activity and dopamine synthesis in retinal amacrine neurons. Science. 1978; 202(4370): 901–2.
82. Doi M, Yujnovsky I, Hirayama J, et al.: Impaired light masking in dopamine D2 receptor-null mice. Nat Neurosci. 2006; 9(6): 732–4.
83. Yujnovsky I, Hirayama J, Doi M, et al.: 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.
84. Videnovic A, Golombek D: Circadian and sleep disorders in Parkinson's disease. Exp Neurol. 2013; 243: 45–56.
85. Mendoza J, Challet E: Circadian insights into dopamine mechanisms. Neuroscience. 2014; 282: 230–42.
86. Iijima M, Nikaido T, Akiyama M, et al.: Methamphetamine-induced, suprachiasmatic nucleus-independent circadian rhythms of activity and mPer gene expression in the striatum of the mouse. Eur J Neurosci. 2002; 16(5): 921–9.
87. Hampp G, Ripperger JA, Houben T, et al.: Regulation of monoamine oxidase A by circadian-clock components implies clock influence on mood. Curr Biol. 2008; 18(9): 678–83.
88. McGeer EG, McGeer PL: Circadian rhythm in pineal tyrosine hydroxylase. Science. 1966; 153(3731): 73–4.
89. Sidor MM, Spencer SM, Dzirasa K, et al.: Daytime spikes in dopaminergic activity drive rapid mood-cycling in mice. Mol Psychiatry. 2015; 20(11): 1406–19.
90. Gonzalez S, Moreno-Delgado D, Moreno E, et al.: Circadian-related heteromerization of adrenergic and dopamine D4 receptors modulates melatonin synthesis and release in the pineal gland. PLoS Biol. 2012; 10(6): e1001347.
91. Sellix MT, Freeman ME: Circadian rhythms of neuroendocrine dopaminergic neuronal activity in ovariectomized rats. Neuroendocrinology. 2003; 77(1): 59–70.
92. Sellix MT, Egli M, Poletini MO, et al.: Anatomical and functional characterization of clock gene expression in neuroendocrine dopaminergic neurons. Am J Physiol Regul Integr Comp Physiol. 2006; 290(5): R1309–23.
93. Beckstead RM, Domesick VB, Nauta WJ: Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 1979; 175(2): 191–217.
94. Webb IC, Lehman MN, Coolen LM: Diurnal and circadian regulation of reward-related neurophysiology and behavior. Physiol Behav. 2015; 143: 58–69.
95. Ferris MJ, Espana RA, Locke JL, et al.: Dopamine transporters govern diurnal variation in extracellular dopamine tone. Proc Natl Acad Sci U S A. 2014; 111(26): E2751–9.
96. Owasoyo JO, Walker CA, Whitworth UG: Diurnal variation in the dopamine level of rat brain areas: effect of sodium phenobarbital. Life Sci. 1979; 25(2): 119–22.
97. Paulson PE, Robinson TE: Relationship between circadian changes in spontaneous motor activity and dorsal versus ventral striatal dopamine neurotransmission assessed with on-line microdialysis. Behav Neurosci. 1994; 108(3): 624–35.
98. Sleipness EP, Sorg BA, Jansen HT: Diurnal differences in dopamine transporter and tyrosine hydroxylase levels in rat brain: dependence on the suprachiasmatic nucleus. Brain Res. 2007; 1129(1): 34–42.
99. Frederick A, Bourget-Murray J, Chapman CA, et al.: Diurnal influences on electrophysiological oscillations and coupling in the dorsal striatum and cerebellar cortex of the anesthetized rat. Front Syst Neurosci. 2014; 8: 145.
100. Uz T, Akhisaroglu M, Ahmed R, et al.: The pineal gland is critical for circadian Period1 expression in the striatum and for circadian cocaine sensitization in mice. Neuropsychopharmacology. 2003; 28(12): 2117–23.
101. Angeles-Castellanos M, Mendoza J, Escobar C: Restricted feeding schedules phase shift daily rhythms of c-Fos and protein Per1 immunoreactivity in corticolimbic regions in rats. Neuroscience. 2007; 144(1): 344–55.
102. Verwey M, Amir S: Variable restricted feeding disrupts the daily oscillations of Period2 expression in the limbic forebrain and dorsal striatum in rats. J Mol Neurosci. 2012; 46(2): 258–64.
103. Baier PC, Branisa P, Koch R, et al.: Circadian distribution of motor-activity in unilaterally 6-hydroxy-dopamine lesioned rats. Exp Brain Res. 2006; 169(2): 283–8.
104. Gallardo CM, Darvas M, Oviatt M, et al.: Dopamine receptor 1 neurons in the dorsal striatum regulate food anticipatory circadian activity rhythms in mice. eLife. 2014; 3: e03781.
105. Imbesi M, Yildiz S, Dirim Arslan A, et al.: Dopamine receptor-mediated regulation of neuronal "clock" gene expression. Neuroscience. 2009; 158(2): 537–44.
106. Sahar S, Zocchi L, Kinoshita C, et al.: Regulation of BMAL1 protein stability and circadian function by GSK3beta-mediated phosphorylation. PLoS One. 2010; 5(1): e8561.
107. Falcon E, Ozburn A, Mukherjee S, et al.: Differential regulation of the period genes in striatal regions following cocaine exposure. PLoS One. 2013; 8(6): e66438.
108. Natsubori A, Honma K, Honma S: Differential responses of circadian Per2 expression rhythms in discrete brain areas to daily injection of methamphetamine and restricted feeding in rats. Eur J Neurosci. 2013; 37(2): 251–8.
109. Natsubori A, Honma K, Honma S: Differential responses of circadian Per2 rhythms in cultured slices of discrete brain areas from rats showing internal desynchronisation by methamphetamine. Eur J Neurosci. 2013; 38(4): 2566–71.
110. Natsubori A, Honma K, Honma S: Dual regulation of clock gene Per2 expression in discrete brain areas by the circadian pacemaker and methamphetamine-induced oscillator in rats. Eur J Neurosci. 2014; 39(2): 229–40.
111. McClung CA: Circadian genes, rhythms and the biology of mood disorders. Pharmacol Ther. 2007; 114(2): 222–32.
112. Lavebratt C, Sjoholm LK, Partonen T, et al.: PER2 variantion is associated with depression vulnerability. Am J Med Genet B Neuropsychiatr Genet. 2010; 153B(2): 570–81.
113. McCarthy MJ, Nievergelt CM, Kelsoe JR, et al.: A survey of genomic studies supports association of circadian clock genes with bipolar disorder spectrum illnesses and lithium response. PLoS One. 2012; 7(2): e32091.
114. Landgraf D, Long JE, Welsh DK: Depression-like behaviour in mice is associated with disrupted circadian rhythms in nucleus accumbens and periaqueductal grey. Eur J Neurosci. 2016; 43(10): 1309–20.
115. Landgraf D, Long JE, Proulx CD, et al.: Genetic Disruption of Circadian Rhythms in the Suprachiasmatic Nucleus Causes Helplessness, Behavioral Despair, and Anxiety-like Behavior in Mice. Biol Psychiatry. 2016; pii: S0006-3223(16)31101-5.
116. Christoph GR, Leonzio RJ, Wilcox KS: Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat. J Neurosci. 1986; 6(3): 613–9.
117. Zhao H, Rusak B: Circadian firing-rate rhythms and light responses of rat habenular nucleus neurons in vivo and in vitro. Neuroscience. 2005; 132(2): 519–28.
118. Sakhi K, Belle MD, Gossan N, et al.: Daily variation in the electrophysiological activity of mouse medial habenula neurones. J Physiol. 2014; 592(4): 587–603.
119. Li B, Piriz J, Mirrione M, et al.: Synaptic potentiation onto habenula neurons in the learned helplessness model of depression. Nature. 2011; 470(7335): 535–9.
120. Shen X, Ruan X, Zhao H: Stimulation of midbrain dopaminergic structures modifies firing rates of rat lateral habenula neurons. PLoS One. 2012; 7(4): e34323.
121. Faget L, Osakada F, Duan J, et al.: Afferent Inputs to Neurotransmitter-Defined Cell Types in the Ventral Tegmental Area. Cell Rep. 2016; 15(12): 2796–808.
122. Baltazar RM, Coolen LM, Webb IC: Diurnal rhythms in neural activation in the mesolimbic reward system: critical role of the medial prefrontal cortex. Eur J Neurosci. 2013; 38(2): 2319–27.
123. Baltazar RM, Coolen LM, Webb IC: Medial prefrontal cortex inactivation attenuates the diurnal rhythm in amphetamine reward. Neuroscience. 2014; 258: 204–10.
124. Davidson AJ, Sellix MT, Daniel J, et al.: Chronic jet-lag increases mortality in aged mice. Curr Biol. 2006; 16(21): R914–6.
Repository Staff Only: item control page