Skip to main content
Top
Published in: Journal of Neural Transmission 1/2017

01-02-2017 | Psychiatry and Preclinical Psychiatric Studies - Review article

How does healthy aging impact on the circadian clock?

Authors: Aurel Popa-Wagner, Ana-Maria Buga, Dinu Iuliu Dumitrascu, Adriana Uzoni, Johannes Thome, Andrew N. Coogan

Published in: Journal of Neural Transmission | Special Issue 1/2017

Login to get access

Abstract

Circadian rhythms are recurring patterns in a host of physiological and other parameters that recur with periods of near 24 h. These rhythms reflect the temporal organization of an organism’s homeostatic control systems and as such are key processes in ensuring optimal physiological performance. Dysfunction of circadian processes is linked with adverse health conditions. In this review we highlight the evidence that normal, healthy aging is associated with changes in the circadian system; we examine the molecular mechanisms through which such changes may arise, discuss whether more robust circadian function is a predictor of longevity and highlight the role of circadian rhythms in age-related diseases. Overall, the literature shows that aging is associated with marked changes in circadian processes, both at the behavioral and molecular levels, and the molecular mechanisms through which such changes arise remain to be elucidated, but may involve inflammatory process, redox homeostasis and epigenetic modifications. Understanding the nature of age-related circadian dysfunction will allow for the design of chronotherapeutic intervention strategies to attenuate circadian dysfunction and thus improve health and quality of life.
Literature
go back to reference Asai M, Yoshinobu Y, Kaneko S, Mori A, Nikaido T, Moriya T, Akiyama M, Shibata S (2001) Circadian profile of Per gene mRNA expression in the suprachiasmatic nucleus, paraventricular nucleus, and pineal body of aged rats. J Neurosci Res 66(6):1133–1139PubMedCrossRef Asai M, Yoshinobu Y, Kaneko S, Mori A, Nikaido T, Moriya T, Akiyama M, Shibata S (2001) Circadian profile of Per gene mRNA expression in the suprachiasmatic nucleus, paraventricular nucleus, and pineal body of aged rats. J Neurosci Res 66(6):1133–1139PubMedCrossRef
go back to reference Baird AL, Coogan AN, Siddiqui A, Donev RM, Thome J (2012) Adult attention-deficit hyperactivity disorder is associated with alterations in circadian rhythms at the behavioural, endocrine and molecular levels. Mol Psychiatry 17(10):988–995. doi:10.1038/mp.2011.149 PubMedCrossRef Baird AL, Coogan AN, Siddiqui A, Donev RM, Thome J (2012) Adult attention-deficit hyperactivity disorder is associated with alterations in circadian rhythms at the behavioural, endocrine and molecular levels. Mol Psychiatry 17(10):988–995. doi:10.​1038/​mp.​2011.​149 PubMedCrossRef
go back to reference Belancio VP, Blask DE, Deininger P, Hill SM, Jazwinski SM (2015) The aging clock and circadian control of metabolism and genome stability. Front Genet. 14(5):455. doi:10.3389/fgene.2014.00455 Belancio VP, Blask DE, Deininger P, Hill SM, Jazwinski SM (2015) The aging clock and circadian control of metabolism and genome stability. Front Genet. 14(5):455. doi:10.​3389/​fgene.​2014.​00455
go back to reference Beynon AL, Thome J, Coogan AN (2009) Age and time of day influences on the expression of transforming growth factor-beta and phosphorylated SMAD3 in the mouse suprachiasmatic and paraventricular nuclei. NeuroImmunoModulation 16(6):392–399. doi:10.1159/000228914 PubMedCrossRef Beynon AL, Thome J, Coogan AN (2009) Age and time of day influences on the expression of transforming growth factor-beta and phosphorylated SMAD3 in the mouse suprachiasmatic and paraventricular nuclei. NeuroImmunoModulation 16(6):392–399. doi:10.​1159/​000228914 PubMedCrossRef
go back to reference Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, Simon MC, Takahashi JS, Bradfield CA (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103(7):1009–1017PubMedPubMedCentralCrossRef Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, Simon MC, Takahashi JS, Bradfield CA (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103(7):1009–1017PubMedPubMedCentralCrossRef
go back to reference Campos Costa I, Nogueira Carvalho H, Fernandes L (2013) Aging, circadian rhythms and depressive disorders: a review. Am J Neurodegener Dis 2(4):228–246PubMedPubMedCentral Campos Costa I, Nogueira Carvalho H, Fernandes L (2013) Aging, circadian rhythms and depressive disorders: a review. Am J Neurodegener Dis 2(4):228–246PubMedPubMedCentral
go back to reference Cao R, Robinson B, Xu H, Gkogkas C, Khoutorsky A, Alain T, Yanagiya A, Nevarko T, Liu AC, Amir S, Sonenberg N (2013) Translational control of entrainment and synchrony of the suprachiasmatic circadian clock by mTOR/4E-BP1 signaling. Neuron 79(4):712–724. doi:10.1016/j.neuron.2013.06.026 PubMedCrossRef Cao R, Robinson B, Xu H, Gkogkas C, Khoutorsky A, Alain T, Yanagiya A, Nevarko T, Liu AC, Amir S, Sonenberg N (2013) Translational control of entrainment and synchrony of the suprachiasmatic circadian clock by mTOR/4E-BP1 signaling. Neuron 79(4):712–724. doi:10.​1016/​j.​neuron.​2013.​06.​026 PubMedCrossRef
go back to reference Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, DiTacchio L, Atkins AR, Glass CK, Liddle C, Auwerx J, Downes M, Panda S, Evans RM (2012) Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 485(7396):123–127. doi:10.1038/nature11048 PubMedPubMedCentralCrossRef Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, DiTacchio L, Atkins AR, Glass CK, Liddle C, Auwerx J, Downes M, Panda S, Evans RM (2012) Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 485(7396):123–127. doi:10.​1038/​nature11048 PubMedPubMedCentralCrossRef
go back to reference Czeisler CA, Duffy JF, Shanahan TL, Brown EN, Mitchell JF, Rimmer DW, Ronda JM, Silva EJ, Allan JS, Emens JS, Dijk DJ, Kronauer RE (1999) Stability, precision, and near-24-hour period of the human circadian pacemaker. Science 284(5423):2177–2181PubMedCrossRef Czeisler CA, Duffy JF, Shanahan TL, Brown EN, Mitchell JF, Rimmer DW, Ronda JM, Silva EJ, Allan JS, Emens JS, Dijk DJ, Kronauer RE (1999) Stability, precision, and near-24-hour period of the human circadian pacemaker. Science 284(5423):2177–2181PubMedCrossRef
go back to reference Deng XH, Bertini G, Palomba M, Xu YZ, Bonaconsa M, Nygård M, Bentivoglio M (2010) Glial transcripts and immune-challenged glia in the suprachiasmatic nucleus of young and aged mice. Chronobiol Int 27(4):742–767. doi:10.3109/07420521003681498 PubMedCrossRef Deng XH, Bertini G, Palomba M, Xu YZ, Bonaconsa M, Nygård M, Bentivoglio M (2010) Glial transcripts and immune-challenged glia in the suprachiasmatic nucleus of young and aged mice. Chronobiol Int 27(4):742–767. doi:10.​3109/​0742052100368149​8 PubMedCrossRef
go back to reference Dubrovsky YV, Samsa WE, Kondratov RV (2010) Deficiency of circadian protein CLOCK reduces lifespan and increases age-related cataract development in mice. Aging (Albany NY) 2(12):936–944CrossRef Dubrovsky YV, Samsa WE, Kondratov RV (2010) Deficiency of circadian protein CLOCK reduces lifespan and increases age-related cataract development in mice. Aging (Albany NY) 2(12):936–944CrossRef
go back to reference Duffy JF, Czeisler CA (2002) Age-related change in the relationship between circadian period, circadian phase, and diurnal preference in humans. Neurosci Lett 318(3):117–120PubMedCrossRef Duffy JF, Czeisler CA (2002) Age-related change in the relationship between circadian period, circadian phase, and diurnal preference in humans. Neurosci Lett 318(3):117–120PubMedCrossRef
go back to reference Frey DJ, Fleshner M, Wright KP Jr (2007) The effects of 40 hours of total sleep deprivation on inflammatory markers in healthy young adults. Brain Behav Immun 21(8):1050–1057PubMedCrossRef Frey DJ, Fleshner M, Wright KP Jr (2007) The effects of 40 hours of total sleep deprivation on inflammatory markers in healthy young adults. Brain Behav Immun 21(8):1050–1057PubMedCrossRef
go back to reference Hardeland R, Cardinali DP, Brown GM, Pandi-Perumal SR (2015) Melatonin and brain inflammaging. Prog Neurobiol 127–128C:46–63 Hardeland R, Cardinali DP, Brown GM, Pandi-Perumal SR (2015) Melatonin and brain inflammaging. Prog Neurobiol 127–128C:46–63
go back to reference Hida A, Kusanagi H, Satoh K, Kato T, Matsumoto Y, Echizenya M, Shimizu T, Higuchi S, Mishima K (2009) Expression profiles of PERIOD1, 2, and 3 in peripheral blood mononuclear cells from older subjects. Life Sci 84(1–2):33–37. doi:10.1016/j.lfs.2008.10.012 PubMedCrossRef Hida A, Kusanagi H, Satoh K, Kato T, Matsumoto Y, Echizenya M, Shimizu T, Higuchi S, Mishima K (2009) Expression profiles of PERIOD1, 2, and 3 in peripheral blood mononuclear cells from older subjects. Life Sci 84(1–2):33–37. doi:10.​1016/​j.​lfs.​2008.​10.​012 PubMedCrossRef
go back to reference Hofman MA, Swaab DF (1994) Alterations in circadian rhythmicity of the vasopressin-producing neurons of the human suprachiasmatic nucleus (SCN) with aging. Brain Res 651(1–2):134–142PubMedCrossRef Hofman MA, Swaab DF (1994) Alterations in circadian rhythmicity of the vasopressin-producing neurons of the human suprachiasmatic nucleus (SCN) with aging. Brain Res 651(1–2):134–142PubMedCrossRef
go back to reference Hurd MW, Ralph MR (1998) The significance of circadian organization for longevity in the golden hamster. J Biol Rhythms 13(5):430–436PubMedCrossRef Hurd MW, Ralph MR (1998) The significance of circadian organization for longevity in the golden hamster. J Biol Rhythms 13(5):430–436PubMedCrossRef
go back to reference Khapre RV, Kondratova AA, Patel S, Dubrovsky Y, Wrobel M, Antoch MP, Kondratov RV (2014) BMAL1-dependent regulation of the mTOR signaling pathway delays aging. Aging (Albany NY) 6(1):48–57CrossRef Khapre RV, Kondratova AA, Patel S, Dubrovsky Y, Wrobel M, Antoch MP, Kondratov RV (2014) BMAL1-dependent regulation of the mTOR signaling pathway delays aging. Aging (Albany NY) 6(1):48–57CrossRef
go back to reference Kolker DE, Fukuyama H, Huang DS, Takahashi JS, Horton TH, Turek FW (2003) Aging alters circadian and light-induced expression of clock genes in golden hamsters. J Biol Rhythms 18(2):159–169PubMedCrossRef Kolker DE, Fukuyama H, Huang DS, Takahashi JS, Horton TH, Turek FW (2003) Aging alters circadian and light-induced expression of clock genes in golden hamsters. J Biol Rhythms 18(2):159–169PubMedCrossRef
go back to reference Kwak Y, Lundkvist GB, Brask J, Davidson A, Menaker M, Kristensson K, Block GD (2008) Interferon-gamma alters electrical activity and clock gene expression in suprachiasmatic nucleus neurons. J Biol Rhythms 23(2):150–159. doi:10.1177/0748730407313355 PubMedCrossRef Kwak Y, Lundkvist GB, Brask J, Davidson A, Menaker M, Kristensson K, Block GD (2008) Interferon-gamma alters electrical activity and clock gene expression in suprachiasmatic nucleus neurons. J Biol Rhythms 23(2):150–159. doi:10.​1177/​0748730407313355​ PubMedCrossRef
go back to reference Leise TL, Harrington ME, Molyneux PC, Song I, Queenan H, Zimmerman E, Lall GS, Biello SM (2013) Voluntary exercise can strengthen the circadian system in aged mice. Age (Dordr) 35(6):2137–2152. doi:10.1007/s11357-012-9502-y CrossRef Leise TL, Harrington ME, Molyneux PC, Song I, Queenan H, Zimmerman E, Lall GS, Biello SM (2013) Voluntary exercise can strengthen the circadian system in aged mice. Age (Dordr) 35(6):2137–2152. doi:10.​1007/​s11357-012-9502-y CrossRef
go back to reference Liu C, Li S, Liu T, Borjigin J, Lin JD (2007) Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 447:477–481PubMedCrossRef Liu C, Li S, Liu T, Borjigin J, Lin JD (2007) Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 447:477–481PubMedCrossRef
go back to reference Mazzoccoli G, Carughi S, Sperandeo M, Pazienza V, Giuliani F, Greco A (2011) Alteration of circadian rhythmicity of CD3+ CD4+ lymphocyte subpopulation in healthy aging. J Biol Regul Homeost Agents 25(3):405–416PubMed Mazzoccoli G, Carughi S, Sperandeo M, Pazienza V, Giuliani F, Greco A (2011) Alteration of circadian rhythmicity of CD3+ CD4+ lymphocyte subpopulation in healthy aging. J Biol Regul Homeost Agents 25(3):405–416PubMed
go back to reference Moore RY (2007) Suprachiasmatic nucleus in sleep-wake regulation. Sleep Med Suppl 3:27–33CrossRef Moore RY (2007) Suprachiasmatic nucleus in sleep-wake regulation. Sleep Med Suppl 3:27–33CrossRef
go back to reference Musiek ES, Lim MM, Yang G, Bauer AQ, Qi L, Lee Y, Roh JH, Ortiz-Gonzalez X, Dearborn JT, Culver JP, Herzog ED, Hogenesch JB, Wozniak DF, Dikranian K, Giasson BI, Weaver DR, Holtzman DM, Fitzgerald GA (2013) Circadian clock proteins regulate neuronal redox homeostasis and neurodegeneration. J Clin Invest 123(12):5389–5400. doi:10.1172/JCI70317 PubMedPubMedCentralCrossRef Musiek ES, Lim MM, Yang G, Bauer AQ, Qi L, Lee Y, Roh JH, Ortiz-Gonzalez X, Dearborn JT, Culver JP, Herzog ED, Hogenesch JB, Wozniak DF, Dikranian K, Giasson BI, Weaver DR, Holtzman DM, Fitzgerald GA (2013) Circadian clock proteins regulate neuronal redox homeostasis and neurodegeneration. J Clin Invest 123(12):5389–5400. doi:10.​1172/​JCI70317 PubMedPubMedCentralCrossRef
go back to reference Nagoshi E, Sugino K, Kula E, Okazaki E, Tachibana T, Nelson S (2010) Dissecting differential gene expression within the circadian neuronal circuit of Drosophila. Nat Neurosci 13:60–68. doi:10.1038/nn.2451 PubMedCrossRef Nagoshi E, Sugino K, Kula E, Okazaki E, Tachibana T, Nelson S (2010) Dissecting differential gene expression within the circadian neuronal circuit of Drosophila. Nat Neurosci 13:60–68. doi:10.​1038/​nn.​2451 PubMedCrossRef
go back to reference Naismith SL, Hickie IB, Terpening Z, Rajaratnam SM, Rajaratnam SW, Hodges JR, Bolitho S, Rogers NL, Lewis SJ (2014) Circadian misalignment and sleep disruption in mild cognitive impairment. J Alzheimers Dis 38(4):857–866. doi:10.3233/JAD-131217 PubMed Naismith SL, Hickie IB, Terpening Z, Rajaratnam SM, Rajaratnam SW, Hodges JR, Bolitho S, Rogers NL, Lewis SJ (2014) Circadian misalignment and sleep disruption in mild cognitive impairment. J Alzheimers Dis 38(4):857–866. doi:10.​3233/​JAD-131217 PubMed
go back to reference Obayashi K, Saeki K, Kurumatani N (2014) Association between urinary 6-sulfatoxymelatonin excretion and arterial stiffness in the general elderly population: the HEIJO-KYO cohort. J Clin Endocrinol Metab 99(9):3233–3239PubMedCrossRef Obayashi K, Saeki K, Kurumatani N (2014) Association between urinary 6-sulfatoxymelatonin excretion and arterial stiffness in the general elderly population: the HEIJO-KYO cohort. J Clin Endocrinol Metab 99(9):3233–3239PubMedCrossRef
go back to reference Obayashi K, Saeki K, Iwamoto J, Tone N, Tanaka K, Kataoka H, Morikawa M (2015a) Kurumatani N (2015a). Physiological levels of melatonin relate to cognitive function and depressive symptoms, The HEIJO-KYO Cohort. J Clin Endocrinol Metab Obayashi K, Saeki K, Iwamoto J, Tone N, Tanaka K, Kataoka H, Morikawa M (2015a) Kurumatani N (2015a). Physiological levels of melatonin relate to cognitive function and depressive symptoms, The HEIJO-KYO Cohort. J Clin Endocrinol Metab
go back to reference Obayashi K, Saeki K, Kurumatani N (2015b) Higher melatonin secretion is associated with lower leukocyte and platelet counts in the general elderly population: the HEIJO-KYO cohort. J Pineal Res 58(2):227–233PubMedCrossRef Obayashi K, Saeki K, Kurumatani N (2015b) Higher melatonin secretion is associated with lower leukocyte and platelet counts in the general elderly population: the HEIJO-KYO cohort. J Pineal Res 58(2):227–233PubMedCrossRef
go back to reference Oklejewicz M, Daan S (2002) Enhanced longevity in tau mutant Syrian hamsters. Mesocricetus auratus. J Biol Rhythms 17(3):210–216PubMedCrossRef Oklejewicz M, Daan S (2002) Enhanced longevity in tau mutant Syrian hamsters. Mesocricetus auratus. J Biol Rhythms 17(3):210–216PubMedCrossRef
go back to reference Ortiz-Tudela E, Martinez-Nicolas A, Díaz-Mardomingo C, García-Herranz S, Pereda-Pérez I, Valencia A, Peraita H, Venero C, Madrid JA, Rol MA (2014) The characterization of biological rhythms in mild cognitive impairment. Biomed Res Int 2014:524971. doi:10.1155/2014/524971 PubMedPubMedCentralCrossRef Ortiz-Tudela E, Martinez-Nicolas A, Díaz-Mardomingo C, García-Herranz S, Pereda-Pérez I, Valencia A, Peraita H, Venero C, Madrid JA, Rol MA (2014) The characterization of biological rhythms in mild cognitive impairment. Biomed Res Int 2014:524971. doi:10.​1155/​2014/​524971 PubMedPubMedCentralCrossRef
go back to reference Palesh O, Aldridge-Gerry A, Zeitzer JM, Koopman C, Neri E, Giese-Davis J, Jo B, Kraemer H, Nouriani B, Spiegel D (2014) Actigraphy-measured sleep disruption as a predictor of survival among women with advanced breast cancer. Sleep 37(5):837–842. doi:10.5665/sleep.3642 PubMedPubMedCentral Palesh O, Aldridge-Gerry A, Zeitzer JM, Koopman C, Neri E, Giese-Davis J, Jo B, Kraemer H, Nouriani B, Spiegel D (2014) Actigraphy-measured sleep disruption as a predictor of survival among women with advanced breast cancer. Sleep 37(5):837–842. doi:10.​5665/​sleep.​3642 PubMedPubMedCentral
go back to reference Palomba M, Nygård M, Florenzano F, Bertini G, Kristensson K, Bentivoglio M (2008) Decline of the presynaptic network, including GABAergic terminals, in the aging suprachiasmatic nucleus of the mouse. J Biol Rhythms 23(3):220–231. doi:10.1177/0748730408316998 PubMedCrossRef Palomba M, Nygård M, Florenzano F, Bertini G, Kristensson K, Bentivoglio M (2008) Decline of the presynaptic network, including GABAergic terminals, in the aging suprachiasmatic nucleus of the mouse. J Biol Rhythms 23(3):220–231. doi:10.​1177/​0748730408316998​ PubMedCrossRef
go back to reference Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109(3):307–320PubMedCrossRef Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109(3):307–320PubMedCrossRef
go back to reference Reiter RJ, Tan DX, Galano A (2014) Melatonin: exceeding expectations. Physiol (Bethesda) 29(5):325–333 Reiter RJ, Tan DX, Galano A (2014) Melatonin: exceeding expectations. Physiol (Bethesda) 29(5):325–333
go back to reference Riemersa-van der Lek RF, Swaab DF, Twisk J, Hol EM, Hoogendijk WJ, Van Someren EJ (2008) Effect of bright light and melatonin on cognitive and noncognitive function in elderly residents of group care facilities: a randomized controlled trial. JAMA 299(22):2642–2655. doi:10.1001/jama.299.22.2642 CrossRef Riemersa-van der Lek RF, Swaab DF, Twisk J, Hol EM, Hoogendijk WJ, Van Someren EJ (2008) Effect of bright light and melatonin on cognitive and noncognitive function in elderly residents of group care facilities: a randomized controlled trial. JAMA 299(22):2642–2655. doi:10.​1001/​jama.​299.​22.​2642 CrossRef
go back to reference Roenneberg T, Wirz-Justice A, Merrow M (2003) Life between clocks: daily temporal patterns of human chronotypes. J Biol Rhythms 18(1):80–90PubMedCrossRef Roenneberg T, Wirz-Justice A, Merrow M (2003) Life between clocks: daily temporal patterns of human chronotypes. J Biol Rhythms 18(1):80–90PubMedCrossRef
go back to reference Smolensky MH, Portaluppi F, Manfredini R, Hermida RC, Tiseo R, Sackett-Lundeen LL, L Haus E (2015) Diurnal and twenty-four hour patterning of human diseases: acute and chronic common and uncommon medical conditions. Sleep Med Rev 21:3–11. doi:10.1016/j.smrv.2014.07.001 Smolensky MH, Portaluppi F, Manfredini R, Hermida RC, Tiseo R, Sackett-Lundeen LL, L Haus E (2015) Diurnal and twenty-four hour patterning of human diseases: acute and chronic common and uncommon medical conditions. Sleep Med Rev 21:3–11. doi:10.​1016/​j.​smrv.​2014.​07.​001
go back to reference Spengler ML, Kuropatwinski KK, Comas M, Gasparian AV, Fedtsova N, Gleiberman AS, Gitlin II, Artemicheva NM, Deluca KA, Gudkov AV, Antoch MP (2012) Core circadian protein CLOCK is a positive regulator of NF-κB-mediated transcription. Proc Natl Acad Sci USA 109(37):E2457–E2465. doi:10.1073/pnas.1206274109 PubMedPubMedCentralCrossRef Spengler ML, Kuropatwinski KK, Comas M, Gasparian AV, Fedtsova N, Gleiberman AS, Gitlin II, Artemicheva NM, Deluca KA, Gudkov AV, Antoch MP (2012) Core circadian protein CLOCK is a positive regulator of NF-κB-mediated transcription. Proc Natl Acad Sci USA 109(37):E2457–E2465. doi:10.​1073/​pnas.​1206274109 PubMedPubMedCentralCrossRef
go back to reference Stiller JW, Postolache TT (2005) Sleep-wake and other biological rhythms: functional neuroanatomy. Clin Sports Med 24(2):205–235PubMedCrossRef Stiller JW, Postolache TT (2005) Sleep-wake and other biological rhythms: functional neuroanatomy. Clin Sports Med 24(2):205–235PubMedCrossRef
go back to reference Tranah GJ, Blackwell T, Stone KL, Ancoli-Israel S, Paudel ML, Ensrud KE, Cauley JA, Redline S, Hillier TA, Cummings SR, Yaffe K, Group SR (2011) Circadian activity rhythms and risk of incident dementia and mild cognitive impairment in older women. Ann Neurol 70(5):722–732. doi:10.1002/ana.22468 PubMedPubMedCentralCrossRef Tranah GJ, Blackwell T, Stone KL, Ancoli-Israel S, Paudel ML, Ensrud KE, Cauley JA, Redline S, Hillier TA, Cummings SR, Yaffe K, Group SR (2011) Circadian activity rhythms and risk of incident dementia and mild cognitive impairment in older women. Ann Neurol 70(5):722–732. doi:10.​1002/​ana.​22468 PubMedPubMedCentralCrossRef
go back to reference Vartanian GV, Li BY, Chervenak AP, Walch OJ, Pack W, Ala-Laurila P, Wong KY (2015) Melatonin suppression by light in humans is more sensitive than previously reported. J Biol Rhythms 30(4):351–354. doi:10.1177/0748730415585413 Vartanian GV, Li BY, Chervenak AP, Walch OJ, Pack W, Ala-Laurila P, Wong KY (2015) Melatonin suppression by light in humans is more sensitive than previously reported. J Biol Rhythms 30(4):351–354. doi:10.​1177/​0748730415585413​
go back to reference Vural EM, van Munster BC, de Rooij SE (2014) Optimal dosages for melatonin supplementation therapy in older adults: a systematic review of current literature. Drugs Aging 31(6):441–451PubMedCrossRef Vural EM, van Munster BC, de Rooij SE (2014) Optimal dosages for melatonin supplementation therapy in older adults: a systematic review of current literature. Drugs Aging 31(6):441–451PubMedCrossRef
go back to reference Watanabe A, Shibata S, Watanabe S (1995) Circadian rhythm of spontaneous neuronal activity in the suprachiasmatic nucleus of old hamster in vitro. Brain Res 695(2):237–239PubMedCrossRef Watanabe A, Shibata S, Watanabe S (1995) Circadian rhythm of spontaneous neuronal activity in the suprachiasmatic nucleus of old hamster in vitro. Brain Res 695(2):237–239PubMedCrossRef
go back to reference Weinert H, Weinert D, Schurov I, Maywood ES, Hastings MH (2001) Impaired expression of the mPer2 circadian clock gene in the suprachiasmatic nuclei of aging mice. Chronobiol Int 18(3):559–565PubMedCrossRef Weinert H, Weinert D, Schurov I, Maywood ES, Hastings MH (2001) Impaired expression of the mPer2 circadian clock gene in the suprachiasmatic nuclei of aging mice. Chronobiol Int 18(3):559–565PubMedCrossRef
go back to reference Yamaguchi Y, Suzuki T, Mizoro Y, Kori H, Okada K, Chen Y, Fustin JM, Yamazaki F, Mizuguchi N, Zhang J, Dong X, Tsujimoto G, Okuno Y, Doi M, Okamura H (2013) Mice genetically deficient in vasopressin V1a and V1b receptors are resistant to jet lag. Science 342(6154):85–90. doi:10.1126/science.1238599 PubMedCrossRef Yamaguchi Y, Suzuki T, Mizoro Y, Kori H, Okada K, Chen Y, Fustin JM, Yamazaki F, Mizuguchi N, Zhang J, Dong X, Tsujimoto G, Okuno Y, Doi M, Okamura H (2013) Mice genetically deficient in vasopressin V1a and V1b receptors are resistant to jet lag. Science 342(6154):85–90. doi:10.​1126/​science.​1238599 PubMedCrossRef
go back to reference Yoon IY, Kripke DF, Youngstedt SD, Elliott JA (2003) Actigraphy suggests age-related differences in napping and nocturnal sleep, J Sleep Res 12(2):87–93 Yoon IY, Kripke DF, Youngstedt SD, Elliott JA (2003) Actigraphy suggests age-related differences in napping and nocturnal sleep, J Sleep Res 12(2):87–93
go back to reference Zhang L, Lin QL, Lu L, Yang CC, Li YL, Sun FL, Wang DH, Cai YN, Li L (2013b) Tissue-specific modification of clock methylation in aging mice. Eur Rev Med Pharmacol Sci 17(14):1874–1880PubMed Zhang L, Lin QL, Lu L, Yang CC, Li YL, Sun FL, Wang DH, Cai YN, Li L (2013b) Tissue-specific modification of clock methylation in aging mice. Eur Rev Med Pharmacol Sci 17(14):1874–1880PubMed
Metadata
Title
How does healthy aging impact on the circadian clock?
Authors
Aurel Popa-Wagner
Ana-Maria Buga
Dinu Iuliu Dumitrascu
Adriana Uzoni
Johannes Thome
Andrew N. Coogan
Publication date
01-02-2017
Publisher
Springer Vienna
Published in
Journal of Neural Transmission / Issue Special Issue 1/2017
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-015-1424-2

Other articles of this Special Issue 1/2017

Journal of Neural Transmission 1/2017 Go to the issue

Psychiatry and Preclinical Psychiatric Studies - Review Article

Driving and attention deficit hyperactivity disorder

Psychiatry and Preclinical Psychiatric Studies - Review Article

Sleep-dependent memory consolidation and its implications for psychiatry

Psychiatry and Preclinical Psychiatric Studies - Original Article

Sustained attention in adult ADHD: time-on-task effects of various measures of attention