Age-related changes in electrophysiological properties of the mouse suprachiasmatic nucleus in vitro
Abstract
Endogenous biological rhythms are altered at several functional levels during aging. The major pacemaker driving biological rhythms in mammals is the suprachiasmatic nucleus of the hypothalamus. In the present study we used tissue slices from young and old mice to analyze the electrophysiological properties of the retinorecipient ventrolateral part of the suprachiasmatic nucleus. Loose patch and whole-cell recordings were performed during day and night. Both young and old mice displayed a significant variation between day and night in the mean firing rate of suprachiasmatic nucleus neurons. The proportion of cells not firing spontaneous action potentials showed a clear day/night rhythm in young but not in old animals, that had an elevated number of such silent cells during the day compared to young animals. Analysis of firing patterns revealed a more regular spontaneous firing during the day than during the night in the old mice, while there was no difference between day and night in young animals. The frequency of spontaneous inhibitory postsynaptic currents was reduced in ventrolateral suprachiasmatic nucleus neurons in the old animals. Since the inhibitory input to these neurons is mainly derived from within the suprachiasmatic nucleus, this reduction most likely reflects the greater proportion of silent cells found in old animals. The results show that the suprachiasmatic nucleus of old mice is subject to marked electrophysiological changes, which may contribute to physiological and behavioral changes associated with aging.
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Some SCN cells become silent in older animals, and SCN neurons lose phase coherence with age.
“some SCN cells become silent in older animals (as measured in vitro), and SCN neurons lose phase coherence with age247,248”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [247]
Cites
Welsh, D. K., Logothetis, D., Meister, M., & Reppert, S. (1995) · Neuron · doi:10.1016/0896-6273(95)90214-7 · Cited by 1,535 · see citing works
A clockwork web: circadian timing in brain and periphery, in health and disease
Hastings, M. H., Reddy, A. B., & Maywood, E. S. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1177 · Cited by 1,189 · see citing works
Abrahamson, E. E., & Moore, R. Y. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02890-6 · Cited by 788 · see citing works
GABA is the principal neurotransmitter of the circadian system
Moore, R. Y., & Speh, J. C. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90120-a · Cited by 555 · see citing works
Cellular Construction of a Circadian Clock: Period Determination in the Suprachiasmatic Nuclei
Liu, C., Weaver, D. R., Strogatz, S. H., & Reppert, S. M. (1997) · Cell · doi:10.1016/s0092-8674(00)80473-0 · Cited by 508 · see citing works
GABA Synchronizes Clock Cells within the Suprachiasmatic Circadian Clock
Liu, C., & Reppert, S. M. (2000) · Neuron · doi:10.1016/s0896-6273(00)80876-4 · Cited by 340 · see citing works
Effects of aging on central and peripheral mammalian clocks
Yamazaki, S., Straume, M., Tei, H., Sakaki, Y., Menaker, M., & Block, G. D. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152318499 · Cited by 317 · see citing works
Schaap, J., Albus, H., vanderLeest, H. T., Eilers, P. H. C., Détári, L., & Meijer, J. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2436298100 · Cited by 216 · see citing works
AGE-DEPENDENT CHANGES OF THE CIRCADIAN SYSTEM
Weinert, D. (2000) · Chronobiology International · doi:10.1081/cbi-100101048 · Cited by 199 · see citing works
Changes in vasopressin cells of the rat suprachiasmatic nucleus with aging
Roozendaal, B., van Gool, W. A., Swaab, D. F., Hoogendijk, J. E., & Mirmiran, M. (1987) · Brain Research · doi:10.1016/0006-8993(87)90710-4 · Cited by 178 · see citing works
Do the suprachiasmatic nuclei oscillate in old rats as they do in young ones?
Satinoff, E., Li, H., Tcheng, T. K., Liu, C., McArthur, A. J., Medanic, M., & Gillette, M. U. (1993) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1993.265.5.r1216 · Cited by 159 · see citing works
Asai, M., Yoshinobu, Y., Kaneko, S., Mori, A., Nikaido, T., Moriya, T., Akiyama, M., & Shibata, S. (2001) · Journal of Neuroscience Research · doi:10.1002/jnr.10010 · Cited by 151 · see citing works
Zhang, Y., Kornhauser, J. M., Zee, P. C., Mayo, K. E., Takahashi, J. S., & Turek, F. W. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00408-4 · Cited by 147 · see citing works
Madeira, M. D., Sousa, N., Santer, R. M., Paula‐Barbosa, M. M., & Gundersen, H. J. G. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903610404 · Cited by 126 · see citing works
Krajnak, K., Kashon, M. L., Rosewell, K. L., & Wise, P. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-12-04767.1998 · Cited by 125 · see citing works
Pennartz, C. M. A., de Jeu, M. T. G., Geurtsen, A. M. S., Sluiter, A. A., & Hermes, M. L. H. J. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.775bv.x · Cited by 114 · see citing works
Regional pacemakers composed of multiple oscillator neurons in the rat suprachiasmatic nucleus
Nakamura, W., Honma, S., Shirakawa, T., & Honma, K.-I. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01684.x · Cited by 113 · see citing works
Vasoactive intestinal polypeptide neuron changes in the senile rat suprachiasmatic nucleus
Chee, C. A., Roozendaal, B., Swaab, D. F., Goudsmit, E., & Mirmiran, M. (1988) · Neurobiology of Aging · doi:10.1016/s0197-4580(88)80070-8 · Cited by 101 · see citing works
Nunemaker, C. S., DeFazio, R. A., & Moenter, S. M. (2003) · Biological Procedures Online · doi:10.1251/bpo46 · Cited by 99 · see citing works
Watanabe, A., Shibata, S., & Watanabe, S. (1995) · Brain Research · doi:10.1016/0006-8993(95)00713-z · Cited by 96 · see citing works
Aujard, F., Herzog, E. D., & Block, G. D. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00285-8 · Cited by 92 · see citing works
Light-induced gene expression in the suprachiasmatic nucleus of young and aging rats
Sutin, E. L., Dement, W. C., Heller, H. C., & Kilduff, T. S. (1993) · Neurobiology of Aging · doi:10.1016/0197-4580(93)90102-h · Cited by 84 · see citing works
Circadian Rhythm in Inhibitory Synaptic Transmission in the Mouse Suprachiasmatic Nucleus
Itri, J. N., Michel, S. H., Waschek, J. A., & Colwell, C. S. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01078.2003 · Cited by 83 · see citing works
Itri, J. N., & Colwell, C. S. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00332.2003 · Cited by 81 · see citing works
Circadian modulation of membrane properties in slices of rat suprachiasmatic nucleus
de Jeu, M. T. G., Hermes, M. L. H. J., & Pennartz, C. M. A. (1998) · Neuroreport · doi:10.1097/00001756-199811160-00028 · Cited by 81 · see citing works
Loss of day-night differences in VIP mRNA levels in the suprachiasmatic nucleus of aged rats
Kawakami, F., Okamura, H., Tamada, Y., Maebayashi, Y., Fukui, K., & Ibata, Y. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)13355-9 · Cited by 74 · see citing works
Schaap, J., Bos, N. P. A., de Jeu, M. T. G., Geurtsen, A. M. S., Meijer, J. H., & Pennartz, C. M. A. (1999) · Brain Research · doi:10.1016/s0006-8993(98)01025-7 · Cited by 73 · see citing works
Duncan, M. J., Herron, J. M., & Hill, S. (2001) · Molecular Brain Research · doi:10.1016/s0169-328x(01)00015-8 · Cited by 67 · see citing works
Krajnak, K., Kashon, M. L., Rosewell, K. L., & Wise, P. M. (1998) · Endocrinology · doi:10.1210/endo.139.10.6259 · Cited by 62 · see citing works
Saeb‐Parsy, K., & Dyball, R. E. J. (2003) · Journal of Biological Rhythms · doi:10.1177/0748730402239674 · Cited by 60 · see citing works
Mechanism of Irregular Firing of Suprachiasmatic Nucleus Neurons in Rat Hypothalamic Slices
Kononenko, N. I., & Dudek, F. E. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00314.2003 · Cited by 55 · see citing works
Kalló, I., Κalamatianos, T., Piggins, H. D., & Coen, C. W. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2004.01232.x · Cited by 50 · see citing works
Krajnak, K. (1998) · Endocrinology · doi:10.1210/en.139.10.4189 · Cited by 20 · see citing works
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Schmidt, C., Collette, F., Cajochen, C., & Peigneux, P. (2007) · Cognitive Neuropsychology · doi:10.1080/02643290701754158 · Cited by 778 · see citing works
Rhythms of life: circadian disruption and brain disorders across the lifespan
Logan, R. W., & McClung, C. A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0088-y · Cited by 713 · see citing works
Tranah, G. J., Blackwell, T., Stone, K. L., Ancoli‐Israel, S., Paudel, M. L., Ensrud, K. E., Cauley, J. A., Redline, S., Hillier, T. A., Cummings, S. R., et al. (2011) · Annals of Neurology · doi:10.1002/ana.22468 · Cited by 525 · see citing works
The circadian clock and pathology of the ageing brain
Kondratova, A. A., & Kondratov, R. V. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3208 · Cited by 482 · see citing works
Age-Related Decline in Circadian Output
Nakamura, T. J., Nakamura, W., Yamazaki, S., Kudo, T., Cutler, T., Colwell, C. S., & Block, G. D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0451-11.2011 · Cited by 386 · see citing works
Circadian Rhythms, Sleep, and Disorders of Aging
Mattis, J., & Sehgal, A. (2016) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2016.02.003 · Cited by 369 · see citing works
Circadian rhythms, time-restricted feeding, and healthy aging
Manoogian, E. N. C., & Panda, S. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2016.12.006 · Cited by 330 · see citing works
Evidence for Neuronal Desynchrony in the Aged Suprachiasmatic Nucleus Clock
Farajnia, S., Michel, S., Deboer, T., vanderLeest, H. T., Houben, T., Rohling, J. H. T., Ramkisoensing, A., Yasenkov, R., & Meijer, J. H. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0469-12.2012 · Cited by 230 · see citing works
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Satoh, A., Imai, S., & Guarente, L. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2017.42 · Cited by 198 · see citing works
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Barnard, A. R., & Nolan, P. M. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000040 · Cited by 181 · see citing works
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Wyse, C. A., & Coogan, A. N. (2010) · Brain Research · doi:10.1016/j.brainres.2010.03.113 · Cited by 167 · see citing works
Circadian Rhythms, Aging, and Life Span in Mammals
Froy, O. (2011) · Physiology · doi:10.1152/physiol.00012.2011 · Cited by 156 · see citing works
Ramkisoensing, A., & Meijer, J. H. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00128 · Cited by 152 · see citing works
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Coogan, A. N., & Wyse, C. A. (2008) · Brain Research · doi:10.1016/j.brainres.2008.07.087 · Cited by 131 · see citing works
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Carrier, J., Semba, K., Deurveilher, S., Drogos, L. L., Cyr-Cronier, J., Lord, C., & Sekerovick, Z. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.07.004 · Cited by 130 · see citing works
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Erum, J. V., Dam, D. V., & Deyn, P. P. D. (2017) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2017.07.005 · Cited by 117 · see citing works
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Nakamura, T. J., Nakamura, W., Tokuda, I. T., Ishikawa, T., Kudo, T., Colwell, C. S., & Block, G. D. (2015) · eNeuro · doi:10.1523/eneuro.0064-15.2015 · Cited by 109 · see citing works
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Balogiannis, S., Mavroudis, I. A., Mitilineos, D., Baloyannis, I. S., & Costa, V. (2014) · American Journal of Alzheimer s Disease & Other Dementias® · doi:10.1177/1533317514556876 · Cited by 95 · see citing works
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Wimmer, M. E., Rising, J., Galante, R. J., Wyner, A. J., Pack, A. I., & Abel, T. G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0081880 · Cited by 94 · see citing works
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Hasan, S., Dauvilliers, Y., Mongrain, V., Franken, P., & Tafti, M. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.05.010 · Cited by 92 · see citing works
A metabolic and functional overview of brain aging linked to neurological disorders
Baquer, N. Z., Taha, A., Kumar, P., McLean, P., Cowsik, S. M., Kale, R. K., Singh, R., & Sharma, D. (2009) · Biogerontology · doi:10.1007/s10522-009-9226-2 · Cited by 87 · see citing works
Palomba, M. L., Nygård, M., Florenzano, F., Bertini, G., Kristensson, K., & Bentivoglio, M. (2008) · Journal of Biological Rhythms · doi:10.1177/0748730408316998 · Cited by 81 · see citing works
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Paschos, G. K., & FitzGerald, G. A. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.07.010 · Cited by 77 · see citing works
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Jiang, X., Zheng, J., Zhang, S., Wang, B., Wu, C., & Guo, X. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.00361 · Cited by 79 · see citing works
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Biello, S. M. (2009) · AGE · doi:10.1007/s11357-009-9102-7 · Cited by 76 · see citing works
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Allen, C. N., Nitabach, M. N., & Colwell, C. S. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a027714 · Cited by 71 · see citing works
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Kumar, A., Vaca-Dempere, M., Mortimer, T., Deryagin, O., Smith, J. G., Petrus, P., Koronowski, K. B., Greco, C. M., Segalés, J., Andrés, E., et al. (2024) · Science · doi:10.1126/science.adj8533 · Cited by 70 · see citing works
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Ketchesin, K. D., Becker‐Krail, D. D., & McClung, C. A. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14253 · Cited by 60 · see citing works
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Panagiotou, M., Michel, S. H., Meijer, J. H., & Deboer, T. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114563 · Cited by 59 · see citing works
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Banks, G. T., Nolan, P. M., & Peirson, S. N. (2016) · Mammalian Genome · doi:10.1007/s00335-016-9639-6 · Cited by 57 · see citing works
Beynon, A. L., & Coogan, A. N. (2010) · Chronobiology International · doi:10.3109/07420528.2010.501927 · Cited by 52 · see citing works
Suppressors, receptors and effects of cytokines on the aging mouse biological clock
Sadki, A., Bentivoglio, M., Kristensson, K., & Nygård, M. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.12.007 · Cited by 49 · see citing works
Self-citationEvidence for Weakened Intercellular Coupling in the Mammalian Circadian Clock under Long Photoperiod
Buijink, M. R., Almog, A., Wit, C. B., Roethler, O., Engberink, A. H. O. O., Meijer, J. H., Garlaschelli, D., Rohling, J. H. T., & Michel, S. H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0168954 · Cited by 48 · see citing works
From clock to functional pacemaker
Michel, S. H., & Meijer, J. H. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14388 · Cited by 50 · see citing works
The functional changes of the circadian system organization in aging
Zhao, J., Warman, G. R., & Cheeseman, J. F. (2019) · Ageing Research Reviews · doi:10.1016/j.arr.2019.04.006 · Cited by 44 · see citing works
Amidfar, M., Garcez, M. L., & Kim, Y. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110721 · Cited by 43 · see citing works
A multi‐level assessment of the bidirectional relationship between aging and the circadian clock
Buijink, M. R., & Michel, S. H. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15286 · Cited by 41 · see citing works
Beynon, A. L., Thome, J., & Coogan, A. N. (2009) · NeuroImmunoModulation · doi:10.1159/000228914 · Cited by 40 · see citing works
Gu, C., Ramkisoensing, A., Liu, Z., Meijer, J. H., & Rohling, J. H. T. (2014) · Journal of Biological Rhythms · doi:10.1177/0748730413516752 · Cited by 39 · see citing works
Dynamic neuronal network organization of the circadian clock and possible deterioration in disease
Meijer, J. H., Colwell, C. S., Rohling, J. H. T., Houben, T., & Michel, S. H. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59427-3.00009-5 · Cited by 38 · see citing works
Circadian aspects of energy metabolism and aging
Froy, O. (2013) · Ageing Research Reviews · doi:10.1016/j.arr.2013.09.002 · Cited by 39 · see citing works
Geniculohypothalamic GABAergic projections gate suprachiasmatic nucleus responses to retinal input
Hanna, L., Walmsley, L., Pienaar, A., Howarth, M., & Brown, T. M. (2017) · The Journal of Physiology · doi:10.1113/jp273850 · Cited by 31 · see citing works
The clock is ticking. Ageing of the circadian system: From physiology to cell cycle
Terzibasi-Tozzini, E., Martínez-Nicolás, A., & Lucas-Sánchez, A. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.06.011 · Cited by 32 · see citing works
Nygård, M., & Palomba, M. L. (2006) · Chronobiology International · doi:10.1080/07420520500545938 · Cited by 30 · see citing works
Self-citationHozer, C., Pifferi, F., Aujard, F., & Perret, M. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01033 · Cited by 29 · see citing works
He, Q., Wu, B., Price, J. L., & Zhao, Z. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18040886 · Cited by 27 · see citing works
Garau, C., Aparicio, S., Rial, R. V., Nicolau, M. C., & Esteban, S. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.09.010 · Cited by 27 · see citing works
Bentivoglio, M., Deng, X., Nygård, M., Sadki, A., & Kristensson, K. (2006) · Chronobiology International · doi:10.1080/07420520500545797 · Cited by 27 · see citing works
Self-citationTanaka, M., Yamaguchi, E., Takahashi, M., Hashimura, K., Shibata, T., Nakamura, W., & Nakamura, T. J. (2012) · Neuroscience Research · doi:10.1016/j.neures.2012.09.005 · Cited by 26 · see citing works
To sleep or not to sleep – Effects on memory in normal aging and disease
Kroeger, D., & Vetrivelan, R. (2023) · Aging Brain · doi:10.1016/j.nbas.2023.100068 · Cited by 25 · see citing works
Nygård, M., Lundkvist, G., Hill, R., & Kristensson, K. (2009) · NeuroReport · doi:10.1097/wnr.0b013e32831f1ca2 · Cited by 31 · see citing works
Self-citationSeasonality and light phase-resetting in the mammalian circadian rhythm
Hannay, K. M., Forger, D. B., & Booth, V. (2020) · Scientific Reports · doi:10.1038/s41598-020-74002-2 · Cited by 19 · see citing works
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Akhmedov, K., Rizzo, V., Kadakkuzha, B. M., Carter, C. J., Magoski, N. S., Capo, T. R., & Puthanveettil, S. V. (2013) · PLoS ONE · doi:10.1371/journal.pone.0084793 · Cited by 19 · see citing works
Resetting the Aging Clock: Implications for Managing Age-Related Diseases
Nobrega, A. K. D., Luz, K. V., & Lyons, L. C. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-42667-5_9 · Cited by 18 · see citing works
Aging affects GABAergic function and calcium homeostasis in the mammalian central clock
Engberink, A. H. O. O., Gutiérrez, P. D. T., Chiosso, A., Das, A., Meijer, J. H., & Michel, S. H. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1178457 · Cited by 15 · see citing works
Duncan, M. J. (2006) · Neuroembryology and Aging · doi:10.1159/000103735 · Cited by 14 · see citing works
Bliwise, D. L., & Scullin, M. K. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-24288-2.00003-9 · Cited by 14 · see citing works
Bliwise, D. L. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-6645-3.00003-7 · Cited by 13 · see citing works
Changes in the suprachiasmatic nucleus during aging: Implications for biological rhythms.
Engelberth, R. C. G. J., de Pontes, A. L. B., Fiuza, F. P., Silva, K. D. D. A., Resende, N. D. S., de Azevedo, C. V. M., Costa, M. S. M. O., Cavalcante, J. C., do Nascimento, E. S., Gavioli, E. C., et al. (2013) · Psychology & Neuroscience · doi:10.3922/j.psns.2013.3.07 · Cited by 13 · see citing works
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Goto, K., & Beneragama, C. K. (2009) · Ageing Research Reviews · doi:10.1016/j.arr.2009.09.003 · Cited by 12 · see citing works
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Garbarino, S., Lanteri, P., Prada, V., Falkenstein, M., & Sannita, W. G. (2020) · Journal of Psychophysiology · doi:10.1027/0269-8803/a000267 · Cited by 11 · see citing works
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Farajnia, S., Meijer, J. H., & Michel, S. H. (2016) · ASN NEURO · doi:10.1177/1759091416670778 · Cited by 10 · see citing works
Marrero, H. G., & Lémos, J. R. (2007) · Neuromethods · doi:10.1007/978-1-59745-492-6_11 · Cited by 9 · see citing works
ASIC1a affects hypothalamic signaling and regulates the daily rhythm of body temperature in mice
Peng, Z., Ziros, P. G., Martini, T., Liao, X.-H., Stoop, R., Refetoff, S., Albrecht, U., Sykiotis, G. P., & Kellenberger, S. B. (2023) · Communications Biology · doi:10.1038/s42003-023-05221-2 · Cited by 8 · see citing works
Aging and circadian rhythms: general trends
Pandi-Perumal, S. R., Spence, D. W., & Sharma, V. K. (2009) · Cambridge University Press eBooks · doi:10.1017/cbo9780511770661.004 · Cited by 6 · see citing works
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Netzer, N. C., Pramsohler, S., & Frohnhofen, H. (2018) · Somnologie - Schlafforschung und Schlafmedizin · doi:10.1007/s11818-018-0185-1 · Cited by 4 · see citing works
Singh, R. (2016) · Springer eBooks · doi:10.1007/978-981-10-2155-8_16 · Cited by 4 · see citing works
Zhong, Z., Ahmed, A., & Wang, H. (2023) · Healthy ageing and longevity · doi:10.1007/978-3-031-22468-3_3 · Cited by 4 · see citing works
The Hypothalamus in Alzheimer’s Disease: A Golgi and Electron and Microscope Study
Baloyannis, S. J., Mavroudis, I., Mitilineos, D., Baloyannis, I. S., & Costa, V. (2018) · Cognitive Disorders · doi:10.5772/intechopen.81475 · Cited by 48 · see citing works
Michel, S. H., Block, G. D., & Meijer, J. H. (2015) · doi:10.1002/9781118467831.ch22 · Cited by 2 · see citing works
Modeling the geometry of circadian synchronization and period across aging
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Circadian rhythms, NRF2 signalling and redox homeostasis: A holy grail for a healthy life course?
Sutton, E., & Pekovic‐Vaughan, V. (2026) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2026.05.318 · Cited by 1 · see citing works
Kaladchibachi, S., Negelspach, D., Zeitzer, J. M., & Fernandez, F. (2022) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2022.112389 · Cited by 1 · see citing works
Clocks, Brain Function, and Dysfunction
Feillet, C. A., & Albrecht, U. (2009) · Springer eBooks · doi:10.1007/978-1-4419-1262-6_10
Molecular Mechanisms Of Sleep/wake Regulation And Memory Formation In Young And Aged Mice
Wimmer, M. E. (2012) · ScholarlyCommons (University of Pennsylvania)
The Hypothalamus in Alzheimer’s Disease: A Golgi and Electron and Microscope Study
Balogiannis, S., Mavroudis, I. A., Mitilineos, D., Baloyannis, I. S., & Costa, V. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.75887
Trastornos circadianos del sueño y enfermedades neurodegenerativas
Lillo-Triguero, L. (2022) · Kranion · doi:10.24875/kranion.m22000021
Clocks and steroids interaction across the life span
Pilorz, V., Chang, P., Newbold, S. A., Nied, E., Simonneaux, V., Astiz, M., & Piggins, H. D. (2026) · Journal of Neuroendocrinology · doi:10.1111/jne.70291
- Authors
- Nygård, M., Hill, R. H., Wikström, M. A., & Kristensson, K.
- Affiliations
- Karolinska Institutet (SE)
- Corresponding author
- Wikström, Martin A.
- Venue
- Brain Research Bulletin
- Publisher
- Elsevier BV
- Published
- 2005-03
- Volume
- 65
- Issue
- 2
- Pages
- 149-154
- ISSN
- 0361-9230 (ISSN-L)
- OpenAlex
- W2000631168
- Cited by
- 82
- References
- 33
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 5 · 2022: 2 · 2021: 1 · 2020: 5 · 2019: 4 · 2018: 4 · 2017: 9 · 2016: 7 · 2015: 3 · 2014: 2 · 2013: 5 · 2012: 5
- FWCI
- 1.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research Bulletin (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- suprachiasmatic nucleus, aging, circadian rhythm, biological rhythms, spontaneous firing rate, day-night rhythm, inhibitory postsynaptic currents, neuronal firing patterns
- MeSH terms
- Action Potentials, Aging, Animals, Biological Clocks, Circadian Rhythm, Male, Mice, Inbred C57BL, Neural Inhibition, Synaptic Transmission, Neurons, Organ Culture Techniques, Suprachiasmatic Nucleus, Patch-Clamp Techniques, Mice
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