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The Possible Role of Epigenetics in the Memory Impairment Elicited by Circadian Rhythm Disruption

  • Scott H. Deibel
  • Robert J. McDonald
Chapter
Part of the Healthy Ageing and Longevity book series (HAL, volume 7)

Abstract

Memories are the glue of one’s existence; unfortunately sometimes memories are more transitory then we would like. Aging and various disease states can induce memory impairments, but for the most part the mechanisms for these memory impairments are largely unknown. Circadian rhythms increase an organism’s biological fitness by synchronizing its physiology and behaviour to their environment. Sometimes circadian rhythms become desynchronized from the environment and this circadian misalignment elicits memory impairments in both humans and rodents. Circadian rhythm dysfunction and memory impairments are hallmarks of both aging and chronic shiftwork, therefore it is pertinent to untangle the nature of the relationship between these processes. Epigenetics allow one’s environment to influence gene expression without changing the genome itself. The plasticity of both memory and circadian rhythms are mediated in part by epigenetic modifications. While epigenetics is necessary for both circadian rhythm generation and memory, very little is known about how circadian rhythm disruption affects the epigenome. Epigenetics will be discussed as a mediator between circadian rhythms and memory in conditions where circadian rhythms are in or out of synch with the environment.

Keywords

Circadian Rhythm Disruption Epigentics Memory Aging Age Related Cognitive Decline Circadian Misalignment 

Notes

Acknowledgements

This research line is supported by grants awarded to Robert J. McDonald from Natural Sciences and Engineering Research Council, Canadian Institutes of Health Research, Alzheimer’s Society of Canada, and a Canadian Breast Cancer Foundation grant awarded to Olga Kovalchuk and Robert J. McDonald. Scott H. Deibel currently holds a Natural Sciences and Engineering Research Council CREATE BIP PhD fellowship. The authors declare that they have no conflict of interest.

References

  1. Aguilar-Arnal L, Sassone-Corsi P (2014) Chromatin landscape and circadian dynamics: Spatial and temporal organization of clock transcription. In: Proceedings of the National Academy of Sciences of the United States of America, 2014(22), pp. 1–8. Available at: http://www.ncbi.nlm.nih.gov/pubmed/25378702
  2. Alarcón JM et al (2004) Chromatin acetylation, memory, and LTP are impaired in CBP+/− mice: A model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42:947–959PubMedCrossRefGoogle Scholar
  3. Alterman T et al (2013) Prevalence rates of work organization characteristics among workers in the US: data from the 2010 National Health Interview Survey. Am J Ind Med 56(6):647–659PubMedCrossRefGoogle Scholar
  4. Altimus CM et al (2008) Rods-cones and melanopsin detect light and dark to modulate sleep independent of image formation. Proc Natl Acad Sci U S A 105(50):19998–20003. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2596746&tool=pmcentrez&rendertype=abstract
  5. Antle MC, Mistlberger RE (2000) Circadian clock resetting by sleep deprivation without exercise in the Syrian hamster. J Neurosci 20(24):9326–9332PubMedGoogle Scholar
  6. Antle MC, Silver R (2009) Neural basis of timing and anticipatory behaviors. Eur J Neurosci 30(9):1643–1649PubMedPubMedCentralCrossRefGoogle Scholar
  7. Antoniadis EA, McDonald RJ (2000) Amygdala, hippocampus and discriminative fear conditioning to context. Behav Brain Res 108(1):1–19PubMedCrossRefGoogle Scholar
  8. Antoniadis EA et al (2000) Circadian rhythms, aging and memory. Behav Brain Res 111:25–37PubMedCrossRefGoogle Scholar
  9. Asher G et al (2008) SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134:317–328PubMedCrossRefGoogle Scholar
  10. Azzi A et al (2014) Circadian behavior is light-reprogrammed by plastic DNA methylation. Nat Neurosci 17(3):377–382. Available at: http://www.ncbi.nlm.nih.gov/pubmed/24531307
  11. Barclay JL et al (2012) Circadian desynchrony promotes metabolic disruption in a mouse model of shiftwork. PLoS ONE 7(5):e37150Google Scholar
  12. Banks G, Nolan PM, Peirson SN (2016) Reciprocal interactions between circadian clocks and aging. Mamm Genome 27:332–340. Available at: http://link.springer.com/10.1007/s00335-016-9639-6
  13. Barnard AR, Nolan PM (2008) When clocks go bad: neurobehavioural consequences of disrupted circadian timing. PLoS Genet 4(5):1–8CrossRefGoogle Scholar
  14. Barclay NL et al (2013) Monozygotic twin differences in non-shared environmental factors associated with chronotype. J Biol Rhythms 28:51–61. Available at: http://www.ncbi.nlm.nih.gov/pubmed/23382591
  15. Barnes CA et al (1977) Circadian rhythm of synaptic excitability in rat and monkey central nervous system. Science 197(4298):91–92PubMedCrossRefGoogle Scholar
  16. Borgs L et al (2009) Period 2 regulates neural stem/progenitor cell proliferation in the adult hippocampus. BMC Neurosci 10:30. Available at: http://www.biomedcentral.com/1471-2202/10/30\npapers2://publication/doi/10.1186/1471-2202-10-30
  17. Bedrosian TA et al (2013) Light at night alters daily patterns of cortisol and clock proteins in female siberian hamsters. J Neuroendocrinol 25:590–596Google Scholar
  18. Bellet MM, Sassone-Corsi P (2010) Mammalian circadian clock and metabolism—the epigenetic link. J Cell Sci 123:3837–3848PubMedPubMedCentralCrossRefGoogle Scholar
  19. Benayoun BA, Pollina EA, Brunet A (2015) Epigenetic regulation of ageing: linking environmental inputs to genomic stability. Nat Rev Mol Cell Biol 16(10):593–610. doi 10.1038/rm4048. Available at: http://www.ncbi.nlm.nih.gov/pubmed/26373265; http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC4736728
  20. Bernstein E, Allis CD (2005) RNA meets chromatin. Genes Dev 19:1635–1655PubMedCrossRefGoogle Scholar
  21. Bliss TV, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331–356PubMedPubMedCentralCrossRefGoogle Scholar
  22. Bollati V et al (2010) Epigenetic effects of shiftwork on blood DNA methylation. Chronobiol Int 27(5):1093–1104PubMedPubMedCentralCrossRefGoogle Scholar
  23. Brunet A, Berger SL (2014) Epigenetics of aging and aging-related disease. J Gerontol Ser A Biol Sci Med Sci 69:17–20CrossRefGoogle Scholar
  24. Burke SN, Barnes CA (2006) Neural plasticity in the ageing brain. Nat Rev Neurosci 7:30–40PubMedCrossRefGoogle Scholar
  25. Cain SW, Chou T, Ralph MR (2004a) Circadian modulation of performance on an aversion-based place learning task in hamsters. Behav Brain Res 150(1–2):201–205PubMedCrossRefGoogle Scholar
  26. Cain SW, Karatsoreos I et al (2004b) Blunted cortisol rhythm is associated with learning impairment in aged hamsters. Physiol Behav 82:339–344PubMedCrossRefGoogle Scholar
  27. Cain SW, Ko CH et al (2004c) Time of day modulation of conditioned place preference in rats depends on the strain of rat used. Neurobiol Learn Mem 81(3):217–220PubMedCrossRefGoogle Scholar
  28. Cain SW, Chalmers JA, Ralph MR (2012) Circadian modulation of passive avoidance is not eliminated in arrhythmic hamsters with suprachiasmatic nucleus lesions. Behav Brain Res 230(1):288–290. doi:  10.1016/j.bbr.2012.02.022
  29. Cardinali DP et al (2012) Therapeutic application of melatonin in mild cognitive impairment. Am J Neurodegener Dis 1(3):280–291PubMedPubMedCentralGoogle Scholar
  30. Castanon-Cervantes O et al (2010) Dysregulation of inflammatory responses by chronic circadian disruption. J Immunol (Baltimore, Md. : 1950), 185(10):5796–5805Google Scholar
  31. Cermakian N et al (2011) Circadian clock gene expression in brain regions of Alzheimer’s disease patients and control subjects. J Biol Rhythms 26:160–170PubMedCrossRefGoogle Scholar
  32. Chang HC, Guarente L (2013) SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging. Cell 153(7):1448–1460. doi: 10.1016/j.cell.2013.05.027
  33. Chen D et al (2008) The role of calorie restriction and SIRT1 in prion-mediated neurodegeneration. Exp Gerontol 43(12):1086–1093. doi: 10.1016/j.exger.2008.08.050
  34. Craig LA et al (2009) Cholinergic depletion of the medial septum followed by phase shifting does not impair memory or rest-activity rhythms measured under standard light/dark conditions in rats. Brain Res Bull 79(1):53–62. Available at: http://www.ncbi.nlm.nih.gov/pubmed/19038315
  35. Chang HM, Wu UI, Lan CT (2009) Melatonin preserves longevity protein (sirtuin 1) expression in the hippocampus of total sleep-deprived rats. J Pineal Res 47:211–220PubMedCrossRefGoogle Scholar
  36. Chaudhury D, Colwell CS (2002) Circadian modulation of learning and memory in fear-conditioned mice. Behav Brain Res 133:95–108PubMedCrossRefGoogle Scholar
  37. Chaudhury D, Wang LM, Colwell CS (2005) Circadian regulation of hippocampal long-term potentiation. J Biol Rhythms 20(3):225–236. Available at: http://www.ncbi.nlm.nih.gov/pubmed/18554561
  38. Cho K (2001) Chronic “jet lag” produces temporal lobe atrophy and spatial cognitive deficits. Nat Neurosci 4(6):567–568PubMedCrossRefGoogle Scholar
  39. Cho K et al (2000) Chronic jet lag produces cognitive deficits. J Neurosci Off J Soc Neurosci 20(6):p.RC66Google Scholar
  40. Chrousos GP (1998) Editorial: ultradian, circadian, and stress-related hypothalamic-pituitary-adrenal axis activity—a dynamic digital-to-analog modulation. Endocrinology 139(2):437–440PubMedCrossRefGoogle Scholar
  41. Chwang WB et al (2006) ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning. Learn Memory 13:322–328CrossRefGoogle Scholar
  42. Chwang WB et al (2007) The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation. J Neurosci 27(46):12732–12742. Available at: http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.2522-07.2007
  43. Coogan AN et al (2013) The circadian system in Alzheimer’s disease: disturbances, mechanisms, and opportunities. Biol Psychiatry 74(5):333–339. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0006322312010293
  44. Craig LA, McDonald RJ (2008) Chronic disruption of circadian rhythms impairs hippocampal memory in the rat. Brain Res Bull 76:141–151PubMedCrossRefGoogle Scholar
  45. Craig LA, Hong NS, McDonald RJ (2011) Revisiting the cholinergic hypothesis in the development of Alzheimer’s disease. Neurosci Biobehav Rev 35(6):1397–1409. doi: 10.1016/j.neubiorev.2011.03.001
  46. Crowley K et al (2002) The effects of normal aging on sleep spindle and K-complex production. Clin Neurophysiol 113:1615–1622PubMedCrossRefGoogle Scholar
  47. Daan S, Koene P (1981) On the timing of foraging flights by oystercatchers, Haematopus ostralegus, on tidal mudflats. Neth J Sea Res 15:1–22CrossRefGoogle Scholar
  48. Dagnas M, Mons N (2013) Region- and age-specific patterns of histone acetylation related to spatial and cued learning in the water maze. Hippocampus 23:581–591PubMedCrossRefGoogle Scholar
  49. Dagnas M et al (2013) HDAC inhibition facilitates the switch between memory systems in young but not aged mice. J Neurosci 33(5):1954–1963. Available at: http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.3453-12.2013
  50. Damiola F et al (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14:2950–2961PubMedPubMedCentralCrossRefGoogle Scholar
  51. Davies JA, Navaratnam V, Redfern PH (1974) The effect of phase-shift on the passive avoidance response in rats and the modifying action of chlordiazepoxide. Br J Pharmacol 51:447–451Google Scholar
  52. Deboer T, Détári L, Meijer JH (2007) Long term effects of sleep deprivation on the mammalian circadian pacemaker. Sleep 30(3):257–262PubMedCrossRefGoogle Scholar
  53. Deibel SH, Hong NS et al (2014a) The effects of chronic photoperiod shifting on the physiology of female Long-Evans rats. Brain Res Bull 103:72–81. doi: 10.1016/j.brainresbull.2014.03.001
  54. Deibel SH, Ingram ML et al (2014b) In a daily time-place learning task, time is only used as a discriminative stimulus if each daily session is associated with a distinct spatial location. Learn Behav 246–255. Available at: http://www.ncbi.nlm.nih.gov/pubmed/24906889
  55. Deibel SH, Thorpe CM (2012) The effects of response cost and species-typical behaviors on a daily time–place learning task. Learn Behav 41:42–53Google Scholar
  56. Devan BD et al (2001) Circadian phase-shifted rats show normal acquisition but impaired long-term retention of place information in the water task. Neurobiol Learn Mem 75:51–62PubMedCrossRefGoogle Scholar
  57. Dibner C, Schibler U, Albrecht U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72:517Google Scholar
  58. Dickmeis T (2009) Glucocorticoids and the circadian clock. J Endocrinol 200(1):3–22PubMedCrossRefGoogle Scholar
  59. Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11:114–126PubMedCrossRefGoogle Scholar
  60. Doi M, Hirayama J, Sassone-Corsi P (2006) Circadian regulator CLOCK is a histone acetyltransferase. Cell 125:497–508PubMedCrossRefGoogle Scholar
  61. Driscoll I et al (2008) Enhanced cell death and learning deficits after a mini-stroke in aged hippocampus. Neurobiol Aging 29(12):1847–1858PubMedCrossRefGoogle Scholar
  62. Dubrovsky YV, Samsa WE, Kondratov RV (2010) Deficiency of circadian protein CLOCK reduces lifespan and increases age-related cataract development in mice. Aging 2(12):936–944PubMedPubMedCentralCrossRefGoogle Scholar
  63. Duffield GE et al (2002) Circadian programs of transcriptional activation, signaling, and protein turnover revealed by microarray analysis of mammalian cells. Curr Biol 12(7):551–557. Available at: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11937023
  64. Eckel-Mahan K, Sassone-Corsi P (2013) Metabolism and the circadian clock converge. Physiol Rev 93(1):107–135. Available at: http://www.ncbi.nlm.nih.gov/pubmed/23303907
  65. Eckel-Mahan KL, Storm DR (2009) Circadian rhythms and memory: not so simple as cogs and gears. EMBO Rep 10(6):584–591PubMedPubMedCentralCrossRefGoogle Scholar
  66. Eckel-Mahan KL et al (2008) Circadian oscillation of hippocampal MAPK activity and cAmp: implications for memory persistence. Nat Neurosci 11(9):1074–1082PubMedPubMedCentralCrossRefGoogle Scholar
  67. Eckles-Smith K et al (2000) Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression. Mol Brain Res 78:154–162PubMedCrossRefGoogle Scholar
  68. Ego-Stengel V, Wilson MA (2010) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20(1):1–10PubMedPubMedCentralGoogle Scholar
  69. Epp JR, Chow C, Galea LAM (2013). Hippocampus-dependent learning influences hippocampal neurogenesis. Front Neurosci 7:1–9Google Scholar
  70. Escobar C et al (2011) Circadian disruption leads to loss of homeostasis and disease. Sleep Disord 2011:1–8CrossRefGoogle Scholar
  71. Farajnia S et al (2013) Aging of the suprachiasmatic clock. The Neuroscientist 20:44–55. Available at: http://nro.sagepub.com/cgi/doi/10.1177/1073858413498936
  72. Feil R, Fraga MF (2012) Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 13(2):97–109. doi: 10.1038/nrg3142
  73. Feillet CA et al (2008) Forebrain oscillators ticking with different clock hands. Mol Cell Neurosci 37:209–221PubMedCrossRefGoogle Scholar
  74. Fekete M et al (1985) Disrupting circadian rhythms in rats induces retrograde amnesia. Physiol Behav 34:883–887PubMedCrossRefGoogle Scholar
  75. Fekete M, Van Ree JM, De Wied D (1986) The ACTH-(4–9) analog ORG 2766 and reverse the retrograde amnesia induced by disrupting circadian rhythms in rats. Peptides 7:563–568PubMedCrossRefGoogle Scholar
  76. Fernandez F et al (2014) Dysrhythmia in the suprachiasmatic nucleus inhibits memory processing. Science 346(6211):854–857PubMedPubMedCentralCrossRefGoogle Scholar
  77. Fischer A et al (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature 447:178–182PubMedCrossRefGoogle Scholar
  78. Fonken LK et al (2010) Light at night increases body mass by shifting the time of food intake. Proc Natl Acad Sci U S A 107(43):18664–18669. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2972983&tool=pmcentrez&rendertype=abstract
  79. Froy O (2013) Circadian aspects of energy metabolism and aging. Ageing Res Rev 12(4):931–940. doi: 10.1016/j.arr.2013.09.002
  80. Froy O, Miskin R (2007) The interrelations among feeding, circadian rhythms and ageing. Prog Neurobiol 82:142–150PubMedCrossRefGoogle Scholar
  81. Froy O, Miskin R (2010) Effect of feeding regimens on circadian rhythms: Implications for aging and longevity. Aging 2(1):7–27PubMedPubMedCentralCrossRefGoogle Scholar
  82. Fujioka A et al (2011) Effects of a constant light environment on hippocampal neurogenesis and memory in mice. Neurosci Lett 488(1):41–44. doi: 10.1016/j.neulet.2010.11.001
  83. Gallou-kabani C, Junien C (2007) Lifelong circadian and epigenetic drifts in metabolic syndrome ND ES SC Key words RIB ND ES SC RIB, pp 137–146Google Scholar
  84. Gao J et al (2010) A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466:1105–1109PubMedPubMedCentralCrossRefGoogle Scholar
  85. Gibson EM et al (2010) Experimental “Jet Lag” inhibits adult neurogenesis and produces long-term cognitive deficits in female hamsters. PLoS ONE 5(12):e15267. doi: 10.1371/journal.pone.0015267
  86. Goldberg AD, Allis CD, Bernstein E (2007) Epigenetics: a landscape takes shape. Cell 128:635–638PubMedCrossRefGoogle Scholar
  87. Gritton HJ et al (2012) Bidirectional interactions between circadian entrainment and cognitive performance. Learn Mem 19(3):126–141PubMedPubMedCentralCrossRefGoogle Scholar
  88. Guilding C, Piggins HD (2007) Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain? Eur J Neurosci 25:3195–3216PubMedCrossRefGoogle Scholar
  89. Gutman R et al (2011) Long-lived mice exhibit 24 h locomotor circadian rhythms at young and old age. Exp Gerontol 46(7):606–609. doi: 10.1016/j.exger.2011.02.015
  90. Hara R et al (2001) Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus. Genes Cells 6:269–278PubMedCrossRefGoogle Scholar
  91. Hauber W, Bareiß A (2001) Facilitative effects of an adenosine A1/A2 receptor blockade on spatial memory performance of rats: selective enhancement of reference memory retention during the light period. Behav Brain Res 118(1):43–52PubMedCrossRefGoogle Scholar
  92. Haus E, Smolensky M (2006) Biological clocks and shift work: circadian dysregulation and potential long-term effects. Cancer Causes Control 17:489–500PubMedCrossRefGoogle Scholar
  93. Haus EL, Smolensky MH (2013) Shift work and cancer risk: potential mechanistic roles of circadian disruption, light at night, and sleep deprivation. Sleep Med Rev 17(4):273–284. doi: 10.1016/j.smrv.2012.08.003
  94. Heyward FD et al (2012) Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem 98(1):25–32. doi: 10.1016/j.nlm.2012.04.005
  95. Hirayama J et al (2007) CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature 450:1086–1090PubMedCrossRefGoogle Scholar
  96. Hoffman AE, Yi C-H et al (2010a) Clock in breast tumorigenesis: evidence from genetic, epigenetic, and transcriptional profiling analyses. Cancer Res 70(4):145901468CrossRefGoogle Scholar
  97. Hoffman AE, Zheng T et al (2010b) THe core clock gene cryptochrome 2 influences breast cancer risk, possibly by mediating hormone signaling. Cancer Prev Res 3(4):539–548CrossRefGoogle Scholar
  98. Jacobs DI et al (2013) Methylation alternations at imprinted genes detected among long-term shiftworkers. Environ Mol Mutagen 54:141–146PubMedCrossRefGoogle Scholar
  99. Jean-Louis G, Von Gizycki H, Zizi F (1998) Melatonin effects on sleep, mood, and cognition in elderly with mild cognitive impairment. J Pineal Res 25(3):177–183PubMedCrossRefGoogle Scholar
  100. Jenwitheesuk A et al (2014) Melatonin regulates aging and neurodegeneration through energy metabolism, epigenetics, autophagy and circadian rhythm pathways. Int J Mol Sci 15:16848–16884. Available at: http://www.mdpi.com/1422-0067/15/9/16848/
  101. Jilg A et al (2010) Temporal dynamics of mouse hippocampal clock gene expression support memory processing. Hippocampus 20:377–388PubMedGoogle Scholar
  102. Kalló I et al (2004) Ageing and the diurnal expression of mRNAs for vasoactive intestinal peptide and for the VPAC2 and PAC1 receptors in the suprachiasmatic nucleus of male rats. J Neuroendocrinol 16(28):758–766PubMedCrossRefGoogle Scholar
  103. Katada S, Sassone-Corsi P (2010) The histone methyltransferase MLL1 permits the oscillation of circadian gene expression. Nat Struct Mol Biol 17(12):1414–1421PubMedCrossRefGoogle Scholar
  104. Kawakami F et al (1997) Loss of day-night differences in VIP mRNA levels in the suprachiasmatic nucleus of aged rats. Neurosci Lett 222:99–102PubMedCrossRefGoogle Scholar
  105. Keuker JIH, Luiten PGM, Fuchs E (2003) Preservation of hippocampal neuron numbers in aged rhesus monkeys. Neurobiol Aging 24:157–165PubMedCrossRefGoogle Scholar
  106. Kim D et al (2007) SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer’s disease and amyotrophic lateral sclerosis. EMBO J 26:3169–3179PubMedPubMedCentralCrossRefGoogle Scholar
  107. Ko CH, Takahashi JS (2006) Molecular components of the mammalian circadian clock. Hum Mol Genet 15(SUPPL. 2):271–277CrossRefGoogle Scholar
  108. Ko CH, McDonald RJ, Ralph MR (2003) The suprachiasmatic nucleus is not required for temporal gating of performance on a reward-based learning and memory task. Biol Rhythm Res 34(2):177–192. Available at: http://www.tandfonline.com/doi/abs/10.1076/brhm.34.2.177.14493
  109. Kochan DZ, Kovalchuk O (2015) Circadian disruption and breast cancer. Oncotarget 6(19):16866–16882. Available at: http://content.wkhealth.com/linkback/openurl?sid=WKPTLP:landingpage&an=00001648-200503000-00016
  110. Kochan DZ et al (2015) Circadian disruption-induced microRNAome deregulation in rat mammary gland tissues. Oncoscience 2(4):428–442PubMedPubMedCentralCrossRefGoogle Scholar
  111. Kohsaka A et al (2007) High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab 6:414–421PubMedCrossRefGoogle Scholar
  112. Kolker DE et al (2003) Aging alters circadian and light-induced expression of clock genes in golden hamsters. J Biol Rhythms 18(2):159–169PubMedCrossRefGoogle Scholar
  113. Kondratov RV et al (2006) Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev 20:1868–1873PubMedPubMedCentralCrossRefGoogle Scholar
  114. Kondratova AA et al (2010) Circadian clock proteins control adaptation to novel environment and memery formation. Aging (Albany NY) 2(5):285–297CrossRefGoogle Scholar
  115. Korkmaz A et al (2009) Role of melatonin in the epigenetic regulation of breast cancer. Breast Cancer Res Treat 115:13–27PubMedCrossRefGoogle Scholar
  116. Korzus E, Rosenfeld MG, Mayford M (2004) CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42:961–972PubMedCrossRefGoogle Scholar
  117. Kott J, Leach G, Yan L (2012) Direction-dependent effects of chronic “jet-lag” on hippocampal neurogenesis. Neurosci Lett 515(2):177–180PubMedCrossRefGoogle Scholar
  118. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705PubMedCrossRefGoogle Scholar
  119. Krishnan HC, Lyons LC (2015) Synchrony and desynchrony in circadian clocks: impacts on learning and memory. Learn Mem (Cold Spring Harbor, N.Y.) 22(9):426–437. Available at: http://apps.webofknowledge.com/full_record.do?product=UA&search_mode=GeneralSearch&qid=1&SID=4CWiOb6SSkSmqp2JFsi&page=1&doc=1&cacheurlFromRightClick=no
  120. Kuhn G (2001) Circadian rhythm, shift work, and emergency medicine. Ann Emerg Med 37(1):88–98PubMedCrossRefGoogle Scholar
  121. Logan RW et al (2012) Chronic shift-lag alters the circadian clock of NK cells and promotes lung cancer growth in rats. J Immunol (Baltimore, Md. : 1950) 188:2583–91. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3294088&tool=pmcentrez&rendertype=abstract
  122. Lamont EW et al (2005) 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 102:4180–4184PubMedPubMedCentralCrossRefGoogle Scholar
  123. Larson J et al (2006) Impaired hippocampal long-term potentiation in melatonin MT2 receptor-deficient mice. Neurosci Lett 393(1):23–26PubMedCrossRefGoogle Scholar
  124. Ledón-Rettig CC, Richards CL, Martin LB (2012) Epigenetics for behavioral ecologists. Behav Ecol 24:311–324CrossRefGoogle Scholar
  125. Leube DT et al (2008) Neural correlates of verbal episodic memory in patients with MCI and Alzheimer’s disease-a VBM study. Int J Geriatr Psychiatry 23:1114–1118PubMedCrossRefGoogle Scholar
  126. Levenson JM et al (2004) Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 279(39):40545–40559PubMedCrossRefGoogle Scholar
  127. Lim ASP et al (2012) Increased fragmentation of rest-activity patterns is associated with a characteristic pattern of cognitive impairment in older individuals. Sleep 35(5):633–640PubMedPubMedCentralCrossRefGoogle Scholar
  128. Loh DH et al (2010) Rapid changes in the light/dark cycle disrupt memory of conditioned fear in mice. PLoS ONE 5(9):1–12CrossRefGoogle Scholar
  129. Loh DH et al (2015) Misaligned feeding impairs memories. eLife 4:1–16Google Scholar
  130. Marquié JC et al (2014) Chronic effects of shift work on cognition: findings from the VISAT longitudinal study. Occup Environ Med 72:258–264PubMedCrossRefGoogle Scholar
  131. Masri S, Sassone-Corsi P (2010) Plasticity and specificity of the circadian epigenome. Nat Neurosci 13(11):1324–1329PubMedPubMedCentralCrossRefGoogle Scholar
  132. Masri S, Kinouchi K, Sassone-Corsi P (2015) Circadian clocks, epigenetics, and cancer. Curr Opin Oncol 27(1):50–56PubMedPubMedCentralCrossRefGoogle Scholar
  133. Mattam U, Jagota A (2014) Differential role of melatonin in restoration of age-induced alterations in daily rhythms of expression of various clock genes in suprachiasmatic nucleus of male Wistar rats. Biogerontology 15:257–268PubMedCrossRefGoogle Scholar
  134. McDonald RJ (2002) Multiple combinations of co-factors produce variants of age-related cognitive decline: a theory. Can J Exp Psychol (Revue canadienne de psychologie experimentale) 56:221–239Google Scholar
  135. McDonald RJ et al (2002) No time of day modulation or time stamp on multiple memory tasks in rats. Learn Motiv 33:230–252. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0023969001911117
  136. McDonald RJ, Hong NS (2004) A dissociation of dorso-lateral striatum and amygdala function on the same stimulus-response habit task. Neuroscience 124(3):507–513. Available at: http://ac.els-cdn.com/S0306452203008601/1-s2.0-S0306452203008601-main.pdf?_tid=4c8bc002-df4b-11e3-984e-00000aab0f27&acdnat=1400500205_8eceac914ec24db1bed69d70bdbaa85e
  137. McDonald RJ, Hong NS (2013) How does a specific learning and memory system in the mammalian brain gain control of behavior? Hippocampus 23(11):1084–1102PubMedCrossRefGoogle Scholar
  138. McDonald RJ, White NM (1993) A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav Neurosci 107(1):3–22PubMedCrossRefGoogle Scholar
  139. McDonald HY, Wojtowicz JM (2005) Dynamics of neurogenesis in the dentate gyrus of adult rats. Neurosci Lett 385(1):70–75PubMedCrossRefGoogle Scholar
  140. McDonald RJ, Hong NS, Devan BD (2004) The challenges of understanding mammalian cognition and memory-based behaviours: an interactive learning and memory systems approach. Neurosci Biobehav Rev 28(7):719–745PubMedCrossRefGoogle Scholar
  141. McDonald RJ, Craig LA, Hong NS (2010) The etiology of age-related dementia is more complicated than we think. Behav Brain Res 214:3–11PubMedCrossRefGoogle Scholar
  142. Mendoza J et al (2005) Feeding cues alter clock gene oscillations and photic responses in the suprachiasmatic nuclei of mice exposed to a light/dark cycle. J Neurosci Off J Soc Neurosci 25(6):1514–1522CrossRefGoogle Scholar
  143. Merrow M, Spoelstra K, Roenneberg T (2005) The circadian cycle: daily rhythms from behaviour to genes. EMBO Rep 6(10):930–935PubMedPubMedCentralCrossRefGoogle Scholar
  144. Michán S et al (2010) SIRT1 is essential for normal cognitive function and synaptic plasticity. J Neurosci 30(29):9695–9707PubMedPubMedCentralCrossRefGoogle Scholar
  145. Milagro FI et al (2012) CLOCK, PER2 and BMAL1 DNA methylation: association with obesity and metabolic syndrome characteristics and monounsaturated fat intake. Chronobiol Int 29(9):1180–1194PubMedCrossRefGoogle Scholar
  146. Miller CA, Sweatt JD (2007) Covalent modification of DNA regulates memory formation. Neuron 53:857–869PubMedCrossRefGoogle Scholar
  147. Miller CA et al (2010) Cortical DNA methylation maintains remote memory. Nat Neurosci 13(6):664–666. doi: 10.1038/nn.2560
  148. Mistlberger RE et al (1996) Discrimination of circadian phase in intact and suprachiasmatic nuclei-ablated rats. Brain Res 739(1–2):12–18PubMedCrossRefGoogle Scholar
  149. Mohawk JA, Green CB, Takahashi JS (2012) Central and peripheral circadian clocks in mammals. Annu Rev Neurosci 35(1):445–462Google Scholar
  150. Moore RY (1999) A clock for the ages. Science 284:2102–2104PubMedCrossRefGoogle Scholar
  151. Moore-Ede MC, Sulzman FM, Fuller CA (1982) The clocks that time us: physiology of the circadian timing system. Harvard University Press, CambridgeGoogle Scholar
  152. Morin LP (1988) Age-related changes in hamster circadian period, entrainment, and rhythm splitting. J Biol Rhythms 3:237–248CrossRefGoogle Scholar
  153. Mueller AD, Mear RJ, Mistlberger RE (2011) Inhibition of hippocampal neurogenesis by sleep deprivation is independent of circadian disruption and melatonin suppression. Neuroscience 193:170–181. doi: 10.1016/j.neuroscience.2011.07.019
  154. Mulder C, Gerkema MP, Van der Zee EA (2013a) Circadian clocks and memory: time-place learning. Front Mol Neurosci 6:1–10. Available at: http://journal.frontiersin.org/article/10.3389/fnmol.2013.00008/abstract
  155. Mulder C, Van Der Zee EA et al (2013b) Time-place learning and memory persist in mice lacking functional Per1 and Per2 clock genes. J Biol Rhythms 28(6):367–379. Available at: http://www.ncbi.nlm.nih.gov/pubmed/24336415
  156. Nakahata Y et al (2008) The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134:329–340PubMedPubMedCentralCrossRefGoogle Scholar
  157. Okamura H (2004) Clock genes in cell clocks: roles, actions, and mysteries. J Biol Chem 19:388–399Google Scholar
  158. Orozco-Solis R, Sassone-Corsi P (2014) Circadian clock: linking epigenetics to aging. Curr Opin Genet Dev 26:66–72. doi: 10.1016/j.gde.2014.06.003
  159. Palomba M et al (2008) Decline of the presynaptic network, including GABAergic terminals, in the aging suprachiasmatic nucleus of the mouse. J Biol Rhythms 23(3):220–231PubMedCrossRefGoogle Scholar
  160. Panda S et al (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–320PubMedCrossRefGoogle Scholar
  161. Pandi-perumal SR et al (2002) Senescence, sleep, and circadian rhythms. Ageing Res Rev 1:559–604PubMedCrossRefGoogle Scholar
  162. Peck JS et al (2004) Cognitive effects of exogenous melatonin administration in elderly persons: a pilot study. Am J Geriatr Psychiatry 12(4):432–436. doi: 10.1097/00019442-200407000-00011
  163. Peleg S et al (2010) Altered histone acetylation is associated with age-dependent memory impairment in mice. Science (New York, N.Y.) 328:753–756CrossRefGoogle Scholar
  164. Penev PD et al (1995) Aging alters the phase-resetting properties of a serotonin agonist on hamster circadian rhythmicity. Am J Physiol 268:R293–R298PubMedGoogle Scholar
  165. Penner MR et al (2010) An epigenetic hypothesis of aging-related cognitive dysfunction. Front Aging Neurosci 2:1–11Google Scholar
  166. Petersen RC et al (1999) Mild cognitive impairment. Arch Neurol 56:303–309PubMedCrossRefGoogle Scholar
  167. Phan TH et al (2011) The diurnal oscillation of MAP (mitogen-activated protein) kinase and adenylyl cyclase activities in the hippocampus depends on the suprachiasmatic nucleus. J Neurosci Off J Soc Neurosci 31(29):10640–10647CrossRefGoogle Scholar
  168. Pitsikas N, Algeri S (1992) Deterioration of spatial and nonspatial reference and working memory in aged rats: protective effect of life-long calorie restriction. Neurobiol Aging 13:369–373PubMedCrossRefGoogle Scholar
  169. Pittendrigh CS, Daan S (1974) Circadian oscillations in rodents: a systematic increase of their frequency with age. Science (New York, N.Y.) 186:548–550CrossRefGoogle Scholar
  170. Poeggeler B (2005) Melatonin, aging, and age-related diseases. Endocrine 27(2):201–212PubMedCrossRefGoogle Scholar
  171. Possidente B, McEldowney S, Pabon A (1995) Aging lengthens circadian period for wheel-running activity in C57BL mice. Physiol Behav 57(3):575–579PubMedCrossRefGoogle Scholar
  172. Quintas A et al (2012) Age-associated decrease of SIRT1 expression in rat hippocampus. Prevention by late onset caloric restriction. Exp Gerontol 47(2):198–201. doi: 10.1016/j.exger.2011.11.010
  173. Qin W et al (2008) Regulation of forkhead transcription factor Fox03a contributes to calorie restriction-induced prevention of Alzheimer’s disease-type amyloid neuropathology and spatial memory detrioration. Ann N Y Acad Sci 1147:335–347PubMedPubMedCentralCrossRefGoogle Scholar
  174. Qureshi IA, Mehler MF (2014) Epigenetics of sleep and chronobiology. Curr Neurol Neurosci Rep 14:432Google Scholar
  175. Ralph MR et al (2002) The significance of circadian phase for performance on a reward-based learning task in hamsters. Behav Brain Res 136:179–184PubMedCrossRefGoogle Scholar
  176. Ralph MR et al (2013) Memory for time of day (time memory) is encoded by a circadian oscillator and is distinct from other context memories. Chronobiol Int 30(4):540–547. Available at: http://www.ncbi.nlm.nih.gov/pubmed/23428333
  177. Rapp PR, Gallagher M (1996) Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc Natl Acad Sci U S A 93:9926–9930PubMedPubMedCentralCrossRefGoogle Scholar
  178. Rawashdeh O, Maronde E (2012) The hormonal Zeitgeber melatonin: role as a circadian modulator in memory processing. Front Mol Neurosci 5:27. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3295223&tool=pmcentrez&rendertype=abstract
  179. Rawashdeh O et al (2014) PERIOD1 coordinates hippocampal rhythms and memory processing with daytime. Hippocampus 24:712–723PubMedCrossRefGoogle Scholar
  180. Reiter RJ et al (1981) Age-associated reduction in nocturnal pineal melatonin levels in female rats 1. Endocrinology 109(4):1295–1297PubMedCrossRefGoogle Scholar
  181. Reppert SM, Weaver DR (2001) Molecular analysis of mammalian circadian rhythms. Ann Rev Physiol 63:647–76. Available at: http://www.ncbi.nlm.nih.gov/pubmed/11181971
  182. Roenneberg T et al (2004) A marker for the end of adolescence. Curr Biol 14(24):1038–1039CrossRefGoogle Scholar
  183. Rouch I et al (2005) Shiftwork experience, age and cognitive performance. Ergonomics 48(10):1282–1293PubMedCrossRefGoogle Scholar
  184. Ruby NF et al (2008) Hippocampal-dependent learning requires a functional circadian system. Proc Natl Acad Sci U S A 105(40):15593–15598PubMedPubMedCentralCrossRefGoogle Scholar
  185. Rudenko A, Tsai L-H (2014) Epigenetic regulation in memory and cognitive disorders. Neuroscience 264C:51–63. Available at: http://www.ncbi.nlm.nih.gov/pubmed/23291453
  186. Salgado-Delgado R et al (2008) Internal desynchronization in a model of night-work by forced activity in rats. Neuroscience 154(3):922–931PubMedCrossRefGoogle Scholar
  187. Sapolsky RM, Altmann J (1991) Incidence of hypercortisolism and dexamethasone resistance increases with age among wild baboons. Biol Psychiat 30:1008–1016PubMedCrossRefGoogle Scholar
  188. Satoh A et al (2010) SIRT1 promotes the central adaptive response to diet restriction through activation of the dorsomedial and lateral nuclei of the hypothalamus. J Neurosci Off J Soc Neurosci 30(30):10220–10232CrossRefGoogle Scholar
  189. Scarbrough K et al (1997) Aging and photoperiod affect entrainment and quantitative aspects of locomotor behavior in Syrian hamsters. Am J Physiol 272:R1219–R1225PubMedGoogle Scholar
  190. Schlosser Covell G et al (2012) Disrupted daytime activity and altered sleep-wake patterns may predict transition to mild cognitive impairment or dementia: a critically appraised topic. Neurologist 18:426–429PubMedCrossRefGoogle Scholar
  191. Sei H et al (1992) Effects of an eight-hour advance of the light-dark cycle on sleep-wake rhythm in the rat. Neurosci Lett 137(2):161–164PubMedCrossRefGoogle Scholar
  192. Sei H et al (2003) Single eight-hour shift of light-dark cycle increases brain-derived neurotrophic factor protein levels in the rat hippocampus. Life Sci 73(1):53–59PubMedCrossRefGoogle Scholar
  193. Shi F et al (2013) Abberrant DNA methylation of miR-219 promoter in long-term shiftworkers. Environ Mol Mutagen 54:406–413PubMedCrossRefGoogle Scholar
  194. Shors TJ (2006) Stressful experience and learning across the lifespan. Annu Rev Psychol 57:55–85PubMedPubMedCentralCrossRefGoogle Scholar
  195. Skene DJ et al (1990) Daily variation in the concentration of melatonin and 5-methoxytryptophol in the human pineal gland: effect of age and Alzheimer’s disease. Brain Res 528:170–174PubMedCrossRefGoogle Scholar
  196. Snyder JS et al (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130(4):843–852PubMedCrossRefGoogle Scholar
  197. Snyder J et al (2011) Septo-temporal gradients of neurogenesis and activity in 13- month-old rats. Neurobiol Aging 32(6):1149–1156PubMedCrossRefGoogle Scholar
  198. Souchay C, Isingrini M, Espagnet L (2000) Aging, episodic memory feeling-of-knowing, and frontal functioning. Neuropsychology 14(2):299–309PubMedCrossRefGoogle Scholar
  199. Stephan FK, Kovacevic NS (1978) Multiple retention deficit in passive avoidance in rats is eliminated by suprachiasmatic lesions. Behav Biol 22:456–462PubMedCrossRefGoogle Scholar
  200. Stevenson TJ, Prendergast BJ (2013) Reversible DNA methylation regulates seasonal photoperiodic time measurement. Proc Natl Acad Sci U S A 110:16651–16656. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3799317&tool=pmcentrez&rendertype=abstract
  201. Stone WS et al (1992) Glucose attenuation of deficits in memory retrieval in altered light: dark cycles. Psychobiology 20(1):47–50Google Scholar
  202. Storandt M (2008) Cognitive Deficits in the early stages of Alzheimer’s disease. Curr directions Psychol Sci 17(3):198–202CrossRefGoogle Scholar
  203. Storch K-F et al (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78–83PubMedCrossRefGoogle Scholar
  204. Takahashi Y, Sawa K, Okada T (2013) The diurnal variation of performance of the novel location recognition task in male rats. Behav Brain Res 256:488–493. doi: 10.1016/j.bbr.2013.08.040
  205. Tapp WN, Holloway FA (1981) Phase shifting circadian rhythms produces retrograde amnesia. Science 211(4486):1056–1058PubMedCrossRefGoogle Scholar
  206. Thorpe CM, Wilkie DM (2006) Properties of time–place learning. In: Zentall TR, Wasserman EA (eds) Comparative cognition: experimental explorations of animal intelligence. Oxford University Press, Oxford, pp 229–245Google Scholar
  207. Thorpe CM, Wilkie DM (2007) Rats acquire a low-response-cost daily time-place task with differential amounts of food. Learn Behav 35(1):71–78. Available at: http://www.ncbi.nlm.nih.gov/pubmed/17557393
  208. Thorpe CM et al (2012) Strain differences in a high response-cost daily time—place learning task. Behav Process 90(3):384–391. doi: 10.1016/j.beproc.2012.04.004
  209. Tranah GJ et al (2011) Circadian activity rhythms and risk of incident dementia and MCI in older women. Ann Neurol 70(5):722–732PubMedPubMedCentralCrossRefGoogle Scholar
  210. Tulving E (1993) What is episodic memory? Curr Dir Psychol Sci 2:67–70CrossRefGoogle Scholar
  211. Tulving E et al (1998) Episodic and declarative memory: role of the hippocampus. Trends Cogn Sci 204:198–204Google Scholar
  212. Valentinuzzi VS et al (1997) Effects of aging on the circadian rhythm of wheel-running activity in C57BL/6 mice. Am J Physiol Regul Integr Comp Physiol 273(6):R1957–R1964Google Scholar
  213. Valentinuzzi V et al (2001) Effect of circadian phase on context\rand cued fear conditioning in C57BL/6 J mice. Anim Learn Behav 29(2):133–142CrossRefGoogle Scholar
  214. Valentinuzzi VS, Menna-Barreto L, Xavier GF (2004) Effect of circadian phase on performance of rats in the Morris water maze task. J Biol Rhythms 19(4):312–324. Available at: http://www.ncbi.nlm.nih.gov/pubmed/15245650
  215. Van der Zee EA et al (2008) Circadian time-place learning in mice depends on cry genes. Curr Biol 18(11):844–848PubMedCrossRefGoogle Scholar
  216. Vecsey CG et al (2007) Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J Neurosci Off J Soc Neurosci 27(23):6128–6140CrossRefGoogle Scholar
  217. Wakamatsu H et al (2001) Restricted-feeding-induced anticipatory activity rhythm is associated with a phase-shift of the expression of mPer1 and mPer2 mRNA in the cerebral cortex and hippocampus but not in the suprachiasmatic nucleus of mice. Eur J Neurosci 13:1190–1196PubMedCrossRefGoogle Scholar
  218. Wang LM et al (2005) Melatonin inhibits hippocampal long-term potentiation. Eur J Neurosci 22(9):2231–2237PubMedPubMedCentralCrossRefGoogle Scholar
  219. Wang LM et al (2009) Expression of the circadian clock gene Period2 in the hippocampus: possible implications for synaptic plasticity and learned behaviour. ASN Neuro 1(3):139–152CrossRefGoogle Scholar
  220. Wax TM (1975) Runwheel activity patterns of mature-young and senescent mice: the effect of constant lighting conditions. J Gerontol 30(1):22–27PubMedCrossRefGoogle Scholar
  221. Weinert H et al (2001) Impaired expression of the mPer2 circadian clock gene in the suprachiasmatic nuclei of aging mice. Chronobiol Int 18(3):559–565PubMedCrossRefGoogle Scholar
  222. Welsh DK, Richardson GS, Dement WC (1986) Effect of age on the circadian pattern of sleep and wakefulness in the mouse. J Gerontol 41(5):579–586PubMedCrossRefGoogle Scholar
  223. West MJ et al (1994) Differences in the pattern of hippocampal neuronal loss in normal aging and Alzheimers-disease. Lance 344:769–772CrossRefGoogle Scholar
  224. Wright KP, Bogan RK, Wyatt JK (2013) Shift work and the assessment and management of shift work disorder (SWD). Sleep Med Rev 17(1):41–54. doi: 10.1016/j.smrv.2012.02.002
  225. Wyse CA, Coogan AN (2010) Impact of aging on diurnal expression patterns of CLOCK and BMAL1 in the mouse brain. Brain Res 1337:21–31PubMedCrossRefGoogle Scholar
  226. Yoo S-H et al (2004) PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A 101(15):5339–5346PubMedPubMedCentralCrossRefGoogle Scholar
  227. Young MW, Kay SA (2001) Time zones: a comparative genetics of circadian clocks. Nat Rev Gen 2:702–715CrossRefGoogle Scholar
  228. Zakhary SM et al (2010) Distribution analysis of deacetylase SIRT1 in rodent and human nervous systems. Anat Rec 293:1024–1032CrossRefGoogle Scholar
  229. Zelinski EL et al (2013) Persistent impairments in hippocampal, dorsal striatal, and prefrontal cortical function following repeated photoperiod shifts in rats. Exp Brain Res 224:125–139PubMedCrossRefGoogle Scholar
  230. Zelinski EL, Deibel SH, McDonald RJ (2014a) The trouble with circadian clock dysfunction: multiple deleterious effects on the brain and body. Neurosci Biobehav Rev 40:80–101. doi: 10.1016/j.neubiorev.2014.01.007
  231. Zelinski EL, Hong NS, McDonald RJ (2014b) Persistent impairments in hippocampal function following a brief series of photoperiod shifts in rats. Anim Cogn 17:127–141PubMedCrossRefGoogle Scholar
  232. Zhu Y et al (2011) Epigenetic impact of long-term shiftwork: pilot evidence from circadian genes and whole-genome methylation analysis. Chronobiol Int 28(10):852–861PubMedPubMedCentralCrossRefGoogle Scholar
  233. Zisapel N, Tarrasch R, Laudon M (2005) The relationship between melatonin and cortisol rhythms: clinical implications of melatonin therapy. Drug Dev Res 65:119–125CrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Canadian Centre for Behavioural Neuroscience, Department of NeuroscienceUniversity of LethbridgeLethbridgeCanada

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