Aging of the suprachiasmatic clock

Neuroscientist

Volumn 20, Issue 1, 2014, Pages 44-55

  Farajnia, Sahar ^a   Deboer, Tom ^a   Rohling, Jos H T ^a   Meijer, Johanna H ^a   Michel, Stephan ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

amplitude; circadian clock; membrane properties; modeling; neurodegeneration; neuronal network; synchronization

Indexed keywords

AGING; CELL FUNCTION; CIRCADIAN RHYTHM; ELECTRIC ACTIVITY; NERVE CELL NETWORK; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RESTLESS LEGS SYNDROME; REVIEW; SLEEP; SLEEP DEPRIVATION; SLEEP DISORDER; SUPRACHIASMATIC NUCLEUS;

AMPLITUDE; CIRCADIAN CLOCK; MEMBRANE PROPERTIES; MODELING; NEURODEGENERATION; NEURONAL NETWORK; SYNCHRONIZATION;

AGING; ANIMALS; CIRCADIAN CLOCKS; HUMANS; SLEEP; SUPRACHIASMATIC NUCLEUS;

EID: 84892925592     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858413498936     Document Type: Review

References (90)

1. Achermann P, Borbely AA Principles and practice of sleep medicine. 2011. Sleep homeostasis and models of sleep regulation. In: KrygerMHRothTDementWC, editors. Principles and practice of sleep medicine. 5th ed.St. Louis, MO: Elsevier Saunders. p 431-44. Kryger MH Roth T Dement WC, ed. St. Louis, MO: Elsevier Saunders ; 2011: 431-44.
2. Albus H, Vansteensel MJ, Michel S, Block GD, Meijer JH. A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol. 2005 ; 15: 886-93 (Pubitemid 40772058)
3. Annunziato L, Pannaccione A, Cataldi M, Secondo A, Castaldo P, Di Renzo G. Modulation of ion channels by reactive oxygen and nitrogen species: a pathophysiological role in brain aging? Neurobiol Aging.. 2002 ; 23: 819-34
4. Antle MC, Smith VM, Sterniczuk R, Yamakawa GR, Rakai BD. Physiological responses of the circadian clock to acute light exposure at night. Rev Endocr Metab Disord. 2009 ; 10: 279-91
5. Asai M, Yoshinobu Y, Kaneko S, Mori A, Nikaido T, Moriya T. Circadian profile of Per gene mRNA expression in the suprachiasmatic nucleus, paraventricular nucleus, and pineal body of aged rats. J Neurosci Res. 2001 ; 66: 1133-9 (Pubitemid 33135599)
6. Aujard F, Cayetanot F, Bentivoglio M, Perret M. Age-related effects on the biological clock and its behavioral output in a primate. Chronobiol Int. 2006 ; 23: 451-60 (Pubitemid 43739056)
7. Aujard F, Herzog ED, Block GD. Circadian rhythms in firing rate of individual suprachiasmatic nucleus neurons from adult and middle-aged mice. Neuroscience. 2001 ; 106: 255-61 (Pubitemid 32889627)
8. Benloucif S, Masana MI, Dubocovich ML. Light-induced phase shifts of circadian activity rhythms and immediate early gene expression in the suprachiasmatic nucleus are attenuated in old C3H/HeN mice. Brain Res. 1997 ; 747: 34-42 (Pubitemid 27063796)
9. Biello SM. Circadian clock resetting in the mouse changes with age. Age. 2009 ; 31: 293-303
10. Bliwise DL Principles and practice of sleep medicine. 2011. Normal aging. In: KrygerMHRothTDementWC, editors. Principles and practice of sleep medicine. 5th ed.St. Louis, MO: Elsevier Saunders. p 27-41. Kryger MH Roth T Dement WC, ed. St. Louis, MO: Elsevier Saunders ; 2011: 27-41.
11. Brown TM, Piggins HD. Electrophysiology of the suprachiasmatic circadian clock. Prog Neurobiol. 2007 ; 82: 229-55 (Pubitemid 47088768)
12. Cai A, Lehman MN, Lloyd JM, Wise PM. Transplantation of fetal suprachiasmatic nuclei into middle-aged rats restores diurnal Fos expression in host. Am J Physiol. 1997 ; 272 (1 Pt 2). R422-8
13. Chang H-C, Guarente L. SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging. Cell. 2013 ; 153: 1448-60
14. Chee CA, Roozendaal B, Swaab DF, Goudsmit E, Mirmiran M. Vasoactive intestinal polypeptide neuron changes in the senile rat suprachiasmatic nucleus. Neurobiol Aging. 1988 ; 9: 307-12 (Pubitemid 19268098)
15. Colas D, Bezin L, Gharib A, Morales A, Cespuglio R, Sarda N. REM sleep control during aging in SAM mice: a role for inducible nitric oxide synthase. Neurobiol Aging.. 2005 ; 26: 1375-84
16. Colwell CS, Michel S, Itri J, Rodriguez W, Tam J, Lelievre V. Disrupted circadian rhythms in VIP- and PHI-deficient mice. Am J Physiol Regul Integr Comp Physiol. 2003 ; 285: R939-49
17. Czeisler CA, Duffy JF, Shanahan TL, Brown EN, Mitchell JF, Rimmer DW. Stability, precision, and near-24-hour period of the human circadian pacemaker. Science. 1999 ; 284: 2177-81 (Pubitemid 29297478)
18. Czeisler CA, Dumont M, Duffy JF, Steinberg JD, Richardson GS, Brown EN. Association of sleep-wake habits in older people with changes in output of circadian pacemaker. Lancet. 1992 ; 340: 933-6
19. Deboer T. Technologies of sleep research. Cell Mol Life Sci. 2007 ; 64: 1227-35 (Pubitemid 46791059)
20. Dibner C, Schibler U, Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol. 2010 ; 72: 517-49
21. Dijk DJ, Duffy JF. Circadian regulation of human sleep and age-related changes in its timing, consolidation and EEG characteristics. Ann Med. 1999 ; 31: 130-40 (Pubitemid 29209869)
22. Dirksen RT. Reactive oxygen/nitrogen species and the aged brain: radical impact of ion channel function. Neurobiol Aging. 2002 ; 23: 837-9 (Pubitemid 35217708)
23. Duncan MJ, Crafton CJ, Wheeler DL. Aging regulates 5-HT(1B) receptors and serotonin reuptake sites in the SCN. Brain Res. 2000 ; 856: 213-9 (Pubitemid 30085528)
24. Duncan MJ, Hester JM, Hopper JA, Franklin KM. The effects of aging and chronic fluoxetine treatment on circadian rhythms and suprachiasmatic nucleus expression of neuropeptide genes and 5-HT1B receptors. Eur J Neurosci. 2010 ; 31: 1646-54
25. Farajnia S, Michel S, Deboer T, vanderLeest HT, Houben T, Rohling JH. Evidence for neuronal desynchrony in the aged suprachiasmatic nucleus clock. J Neurosci. 2012 ; 32: 5891-9
26. Foster TC. Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell. 2007 ; 6: 319-25 (Pubitemid 46785137)
27. Gomez D, Barbosa A, Thery M, Aujard F, Perret M. Age affects photoentrainment in a nocturnal primate. J Biol Rhythms. 2012 ; 27: 164-71
28. Gutman R, Genzer Y, Chapnik N, Miskin R, Froy O. Long-lived mice exhibit 24 h locomotor circadian rhythms at young and old age. Exp Gerontol. 2011 ; 46: 606-9
29. Hannibal J, Hindersson P, Knudsen SM, Georg B, Fahrenkrug J. The photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. J Neurosci. 2002 ; 22: RC191
30. Hasan S, Dauvilliers Y, Mongrain V, Franken P, Tafti M. Age-related changes in sleep in inbred mice are genotype dependent. Neurobiol Aging. 2012 ; 33: 195.e13-26
31. Herzog ED, Aton SJ, Numano R, Sakaki Y, Tei H. Temporal precision in the mammalian circadian system: a reliable clock from less reliable neurons. J Biol Rhythms. 2004 ; 19: 35-46 (Pubitemid 38084513)
32. Honma S, Shirakawa T, Katsuno Y, Namihira M, Honma K. Circadian periods of single suprachiasmatic neurons in rats. Neurosci Lett. 1998 ; 250: 157-60 (Pubitemid 28355801)
33. Hughes AT, Piggins HD. Feedback actions of locomotor activity to the circadian clock. Prog Brain Res. 2012 ; 199: 305-36
34. Hurd MW, Ralph MR. The significance of circadian organization for longevity in the golden hamster. J Biol Rhythms. 1998 ; 13: 430-6 (Pubitemid 128478940)
35. Itri JN, Michel S, Vansteensel MJ, Meijer JH, Colwell CS. Fast delayed rectifier potassium current is required for circadian neural activity. Nat Neurosci. 2005 ; 8: 650-6 (Pubitemid 40594207)
36. Itri JN, Vosko AM, Schroeder A, Dragich JM, Michel S, Colwell CS. Circadian regulation of A-type potassium currents in the suprachiasmatic nucleus. J Neurophysiol. 2010 ; 103: 632-40
37. Johnston JD. Measuring seasonal time within the circadian system: regulation of the suprachiasmatic nuclei by photoperiod. J Neuroendocrinol. 2005 ; 17: 459-65 (Pubitemid 40873283)
38. Kallo I, Kalamatianos T, Piggins HD, Coen CW. 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. 2004 ; 16: 758-66 (Pubitemid 39307222)
39. Kawakami F, Okamura H, Tamada Y, Maebayashi Y, Fukui K, Ibata Y. Loss of day-night differences in VIP mRNA levels in the suprachiasmatic nucleus of aged rats. Neurosci Lett. 1997 ; 222: 99-102 (Pubitemid 27077319)
40. Klerman EB, Duffy JF, Dijk DJ, Czeisler CA. Circadian phase resetting in older people by ocular bright light exposure. J Investig Med. 2001 ; 49: 30-40 (Pubitemid 32112581)
41. Koh K, Evans JM, Hendricks JC, Sehgal A. A Drosophila model for age-associated changes in sleep:wake cycles. Proc Natl Acad Sci U S A. 2006 ; 103: 13843-7 (Pubitemid 44413995)
42. Kolker DE, Fukuyama H, Huang DS, Takahashi JS, Horton TH, Turek FW. Aging alters circadian and light-induced expression of clock genes in golden hamsters. J Biol Rhythms. 2003 ; 18: 159-69 (Pubitemid 37187300)
43. Kondratova AA, Kondratov RV. The circadian clock and pathology of the ageing brain. Nature Rev Neurosci. 2012 ; 13: 325-35
44. Kopp C, Albrecht U, Zheng B, Tobler I. Homeostatic sleep regulation is preserved in mPer1 and mPer2 mutant mice. Eur J Neurosci. 2002 ; 16: 1099-106 (Pubitemid 35463559)
45. Landolt HP, Borbely AA. Age-dependent changes in sleep EEG topography. Clin Neurophysiol. 2001 ; 112: 369-77 (Pubitemid 32126473)
46. Landolt HP, Dijk DJ, Achermann P, Borbely AA. Effect of age on the sleep EEG: slow-wave activity and spindle frequency activity in young and middle-aged men. Brain Res. 1996 ; 738: 205-12 (Pubitemid 26378913)
47. Libert S, Bonkowski MS, Pointer K, Pletcher SD, Guarente L. Deviation of innate circadian period from 24 h reduces longevity in mice. Aging Cell. 2012 ; 11: 794-800
48. Lupi D, Semo M, Foster RG. Impact of age and retinal degeneration on the light input to circadian brain structures. Neurobiol Aging. 2012 ; 33: 383-92
49. McAuley JD, Miller JP, Beck E, Nagy ZM, Pang KC. Age-related disruptions in circadian timing: evidence for "split" activity rhythms in the SAMP8. Neurobiol Aging. 2002 ; 23: 625-32 (Pubitemid 34493893)
50. Meijer JH, Colwell CS, Rohling JH, Houben T, Michel S. Dynamic neuronal network organization of the circadian clock and possible deterioration in disease. Prog Brain Res. 2012 ; 199: 143-62
51. Miller MM, Gould BE, Nelson JF. Aging and long-term ovariectomy alter the cytoarchitecture of the hypothalamic-preoptic area of the C57BL/6J mouse. Neurobiol Aging. 1989 ; 10: 683-90 (Pubitemid 20059502)
52. Munch M, Knoblauch V, Blatter K, Schroder C, Schnitzler C, Krauchi K. The frontal predominance in human EEG delta activity after sleep loss decreases with age. Eur J Neurosci. 2004 ; 20: 1402-10 (Pubitemid 39233591)
53. Nakamura TJ, Nakamura W, Yamazaki S, Kudo T, Cutler T, Colwell CS. Age-related decline in circadian output. J Neurosci. 2011 ; 31: 10201-5
54. Naylor RM, Baker DJ, van Deursen JM. Senescent cells: a novel therapeutic target for aging and age-related diseases. Clin Pharmacol Ther.. 2013 ; 93: 105-16
55. Novakova M, Sladek M, Sumova A. Human chronotype is determined in bodily cells under real-life conditions. Chronobiol Int. 2013 ; 30: 607-17
56. Nygard M, Hill RH, Wikstrom MA, Kristensson K. Age-related changes in electrophysiological properties of the mouse suprachiasmatic nucleus in vitro. Brain Res Bull. 2005 ; 65: 149-54 (Pubitemid 40348800)
57. O'Neill JS, Reddy AB. The essential role of cAMP/Ca2+ signalling in mammalian circadian timekeeping. Biochem Soc Trans. 2012 ; 40: 44-50
58. Oosterman JM, van Someren EJ, Vogels RL, Van Harten B, Scherder EJ. Fragmentation of the rest-activity rhythm correlates with age-related cognitive deficits. J Sleep Res. 2009 ; 18: 129-35
59. Palomba M, Nygard M, Florenzano F, Bertini G, Kristensson K, Bentivoglio M. Decline of the presynaptic network, including GABAergic terminals, in the aging suprachiasmatic nucleus of the mouse. J Biol Rhythms. 2008 ; 23: 220-31 (Pubitemid 351652373)
60. Pittendrigh CS, Daan S. Circadian oscillations in rodents: a systematic increase of their frequency with age. Science.. 1974 ; 186: 548-50
61. Riemersma-van der Lek RF, Swaab DF, Twisk J, Hol EM, Hoogendijk WJ, Van Someren EJ. Effect of bright light and melatonin on cognitive and noncognitive function in elderly residents of group care facilities: a randomized controlled trial. JAMA.. 2008 ; 299: 2642-55
62. Roenneberg T, Kuehnle T, Juda M, Kantermann T, Allebrandt K, Gordijn M. Epidemiology of the human circadian clock. Sleep Med Rev. 2007 ; 11: 429-38 (Pubitemid 350087711)
63. Rohling J, Wolters L, Meijer JH. Simulation of day-length encoding in the SCN: from single-cell to tissue-level organization. J Biol Rhythms.. 2006 ; 21: 301-13
64. Roozendaal B, van Gool WA, Swaab DF, Hoogendijk JE, Mirmiran M. Changes in vasopressin cells of the rat suprachiasmatic nucleus with aging. Brain Res. 1987 ; 409: 259-64 (Pubitemid 17077546)
65. Saper CB. The central circadian timing system. Curr Opin Neurobio.l. 2013 ;:
66. Satinoff E, Li H, Tcheng TK, Liu C, McArthur AJ, Medanic M. Do the suprachiasmatic nuclei oscillate in old rats as they do in young ones?. Am J Physiol. 1993 ; 265 (5 Pt 2). R1216-22
67. Schaap J, Pennartz CM, Meijer JH. Electrophysiology of the circadian pacemaker in mammals. Chronobiol Int. 2003 ; 20: 171-88 (Pubitemid 36505395)
68. Sesti F, Liu S, Cai SQ. Oxidation of potassium channels by ROS: a general mechanism of aging and neurodegeneration?. Trends Cell Biol. 2010 ; 20: 45-51
69. Shiromani PJ, Xu M, Winston EM, Shiromani SN, Gerashchenko D, Weaver DR. Sleep rhythmicity and homeostasis in mice with targeted disruption of mPeriod genes. Am J Physiol Regul Integr Comp Physiol. 2004 ; 287: R47-57
70. Swaab DF, Fliers E, Fisser B. The vasopressin containing neurons in the human brain; changes during ageing and senile dementia. Br J Clin Pract Suppl. 1985 ; 39: 7-10
71. Toh KL, Jones CR, He Y, Eide EJ, Hinz WA, Virshup DM. An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science. 2001 ; 291: 1040-3 (Pubitemid 32157412)
72. Turner PL, Mainster MA. Circadian photoreception: ageing and the eye's important role in systemic health. Br J Ophthalmol. 2008 ; 92: 1439-44
73. Valentinuzzi VS, Scarbrough K, Takahashi JS, Turek FW. Effects of aging on the circadian rhythm of wheel-running activity in C57BL/6 mice. Am J Physiol. 1997 ; 273 (6 Pt 2). R1957-64
74. van Gool WA, Witting W, Mirmiran M. Age-related changes in circadian sleep-wakefulness rhythms in male rats isolated from time cues. Brain Res. 1987 ; 413: 384-7 (Pubitemid 17112991)
75. Van Reeth O, Zhang Y, Zee PC, Turek FW. Grafting fetal suprachiasmatic nuclei in the hypothalamus of old hamsters restores responsiveness of the circadian clock to a phase shifting stimulus. Brain Res. 1994 ; 643: 338-42 (Pubitemid 24115112)
76. Vanderleest HT, Houben T, Michel S, Deboer T, Albus H, Vansteensel MJ. Seasonal encoding by the circadian pacemaker of the SCN. Curr Biol. 2007 ; 17: 468-73
77. Vanderleest HT, Rohling JH, Michel S, Meijer JH. Phase shifting capacity of the circadian pacemaker determined by the SCN neuronal network organization. Plos One. 2009 ; 4: e4976
78. Watanabe A, Shibata S, Watanabe S. Circadian rhythm of spontaneous neuronal activity in the suprachiasmatic nucleus of old hamster in vitro. Brain Res. 1995 ; 695: 237-9
79. Weinert D, Waterhouse J. The circadian rhythm of core temperature: effects of physical activity and aging. Physiol Behav. 2007 ; 90: 246-56 (Pubitemid 46177083)
80. Weinert H, Weinert D, Schurov I, Maywood ES, Hastings MH. Impaired expression of the mPer2 circadian clock gene in the suprachiasmatic nuclei of aging mice. Chronobiol Int. 2001 ; 18: 559-65 (Pubitemid 32666424)
81. Welsh DK, Logothetis DE, Meister M, Reppert SM. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron. 1995 ; 14: 697-706
82. Welsh DK, Richardson GS, Dement WC. Effect of age on the circadian pattern of sleep and wakefulness in the mouse. J Gerontol. 1986 ; 41: 579-86 (Pubitemid 16030478)
83. Welsh DK, Takahashi JS, Kay SA. Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol. 2010 ; 72: 551-77
84. Wyse CA, Coogan AN. Impact of aging on diurnal expression patterns of CLOCK and BMAL1 in the mouse brain. Brain Res. 2010 ; 1337: 21-31
85. Wyse CA, Coogan AN, Selman C, Hazlerigg DG, Speakman JR. Association between mammalian lifespan and circadian free-running period: the circadian resonance hypothesis revisited. Biol Lett. 2010 ; 6: 696-8
86. Yeoman M, Scutt G, Faragher R. Insights into CNS ageing from animal models of senescence. Nat Rev Neurosci. 2012 ; 13: 435-45
87. Zee PC, Rosenberg RS, Turek FW. Effects of aging on entrainment and rate of resynchronization of circadian locomotor activity. Am J Physiol. 1992 ; 263 (5 Pt 2). R1099-103
88. Zhang Y, Kornhauser JM, Zee PC, Mayo KE, Takahashi JS, Turek FW. Effects of aging on light-induced phase-shifting of circadian behavioral rhythms, fos expression and CREB phosphorylation in the hamster suprachiasmatic nucleus. Neuroscience. 1996 ; 70: 951-61 (Pubitemid 26014859)
89. Zhdanova IV, Masuda K, Quasarano-Kourkoulis C, Rosene DL, Killiany RJ, Wang S. Aging of intrinsic circadian rhythms and sleep in a diurnal nonhuman primate, Macaca mulatta. J Biol Rhythms. 2011 ; 26: 149-59
90. Zhou JN, Hofman MA, Swaab DF. VIP neurons in the human SCN in relation to sex, age, and Alzheimer's disease. Neurobiol Aging. 1995 ; 16: 571-6