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Age-Related Decline in Circadian Output
Open accessAbstract
Disruptions in sleep/wake cycles, including decreased amplitude of rhythmic behaviors and fragmentation of the sleep episodes, are commonly associated with aging in humans and other mammals. While there are undoubtedly many factors contributing to these changes, a body of literature is emerging, suggesting that an age-related decline in the central circadian clock in the suprachiasmatic nucleus (SCN) may be a key element responsible. To explore age-related changes in the SCN, we have performed in vivo multiunit neural activity (MUA) recordings from the SCN of freely moving young (3-5 months) and middle-aged (13-18 months) mice. Importantly, the amplitude of day-night difference in MUA was significantly reduced in the older mice. We also found that the neural activity rhythms are clearly degraded in the subparaventricular zone, one of the main neural outputs of the SCN. Surprisingly, parallel studies indicate that the molecular clockwork in the SCN as measured by PER2 exhibited only minor deficits at this same age. Thus, the circadian output measured at the level of neural activity rhythms in the SCN is degraded by aging, and this decline occurs before the disruption of key components of the molecular clockwork.
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“These SCN network changes result in desynchronization and a reduction in the amplitude of neuronal activity rhythms248,249 and, ultimately, physiological and behavioural rhythms241.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [249]
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Yoo, S.-H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., Buhr, E. D., Siepka, S. M., Hong, H.-K., Oh, W. J., Yoo, O. J., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308709101 · Cited by 2,329
Self-citationStability, precision, and near-24-hour period of the human circadian pacemaker
Czeisler, C. A., Duffy, J. F., Shanahan, T. L., Brown, E. N., Mitchell, J. F., Rimmer, D. W., Ronda, J. M., Silva, E. J., Allan, J. S., Emens, J. S., et al. (1999) · Science · doi:10.1126/science.284.5423.2177 · Cited by 1,705
The genetics of mammalian circadian order and disorder: implications for physiology and disease
Takahashi, J. S., Hong, H.-K., Ko, C. H., & McDearmon, E. L. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2430 · Cited by 1,611
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 1,223
Inouye, S. T., & Kawamura, H. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.11.5962 · Cited by 985
Sleep in Normal Aging and Dementia
Bliwise, D. L. (1993) · SLEEP · doi:10.1093/sleep/16.1.40 · Cited by 854
Circadian rhythms in isolated brain regions
Abe, M., Herzog, E. D., Yamazaki, S., Straume, M., Tei, H., Sakaki, Y., Menaker, M., & Block, G. D. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00350.2002 · Cited by 681
Self-citationDijk, D., Duffy, J. F., Riel, E., Shanahan, T. L., & Czeisler, C. A. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0611v.x · Cited by 467
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Deboer, T., Vansteensel, M. J., Détári, L., & Meijer, J. H. (2003) · Nature Neuroscience · doi:10.1038/nn1122 · Cited by 328
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Schwarz, J. E., Mrčela, A., Lahens, N. F., Li, Y., Hsu, C. T., Grant, G. R., Skarke, C., Zhang, S., & Sehgal, A. (2024) · eLife · doi:10.7554/elife.88322.2
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Chang, F., Xu, J., Guo, M., Xu, H., Li, D., Covassin, N., Somers, V. K., Wang, K., Wang, Y., & Li, J. (2026) · Journal of the American Heart Association · doi:10.1161/jaha.125.048656
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Todd, W. D. (2012) · doi:10.17077/etd.6mzpucsa
Metadata
- Authors
- Nakamura, T. J., Nakamura, W., Yamazaki, S., Kudo, T., Cutler, T., Colwell, C. S., & Block, G. D.
- Affiliations
- University of California, Los Angeles (US)
- The University of Osaka (JP)
- Vanderbilt University (US)
- Corresponding author
- Colwell, C. S.
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-07-13
- Volume
- 31
- Issue
- 28
- Pages
- 10201-10205
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3155746
- OpenAlex
- W2094874423
- Cited by
- 386
- References
- 35
- Citations by year
- 2026: 17 · 2025: 27 · 2024: 27 · 2023: 33 · 2022: 25 · 2021: 34 · 2020: 36 · 2019: 31 · 2018: 19 · 2017: 24 · 2016: 21 · 2015: 28 · 2014: 14 · 2013: 23 · 2012: 26
- FWCI
- 9.46
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- CHDI Foundation
- National Institutes of Health (AG028748)
- Japan Society for the Promotion of Science (23659871)
- National Institute on Aging (P30AG028748)
- National Institute of Mental Health (R01MH062517)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Keywords
- suprachiasmatic nucleus, sleep-wake cycle, Per2, sleep fragmentation, mice
- MeSH terms
- Aging, Animals, Biological Clocks, Circadian Rhythm, Electrodes, Implanted, Electrophysiology, Male, Motor Activity, Suprachiasmatic Nucleus, Mice, Period Circadian Proteins
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