The DOI matches its Crossref record; 56 of the 57 references it cites were found in a registry or an index.
Hippocampal-dependent learning requires a functional circadian system
Open accessAbstract
Decades of studies have shown that eliminating circadian rhythms of mammals does not compromise their health or longevity in the laboratory in any obvious way. These observations have raised questions about the functional significance of the mammalian circadian system, but have been difficult to address for lack of an appropriate animal model. Surgical ablation of the suprachiasmatic nucleus (SCN) and clock gene knockouts eliminate rhythms, but also damage adjacent brain regions or cause developmental effects that may impair cognitive or other physiological functions. We developed a method that avoids these problems and eliminates rhythms by noninvasive means in Siberian hamsters (Phodopus sungorus). The present study evaluated cognitive function in arrhythmic animals by using a hippocampal-dependent learning task. Control hamsters exhibited normal circadian modulation of performance in a delayed novel-object recognition task. By contrast, arrhythmic animals could not discriminate a novel object from a familiar one only 20 or 60 min after training. Memory performance was not related to prior sleep history as sleep manipulations had no effect on performance. The GABA antagonist pentylenetetrazol restored learning without restoring circadian rhythms. We conclude that the circadian system is involved in memory function in a manner that is independent of sleep. Circadian influence on learning may be exerted via cyclic GABA output from the SCN to target sites involved in learning. Arrhythmic hamsters may have failed to perform this task because of chronic inhibitory signaling from the SCN that interfered with the plastic mechanisms that encode learning in the hippocampus.
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“In confirmation of these findings in mice, studies in Siberian hamsters also show that alterations in the photoperiod sometimes lead to loss of circadian rhyhtmicity and concomitant loss of recall of a novel object (Ruby et al., 2008).”
From Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges (2009) · cites this paper as Ruby et al., 2008
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Cites
Coordination of circadian timing in mammals
Reppert, S. M., & Weaver, D. R. (2002) · Nature · doi:10.1038/nature00965 · Cited by 4,379
Squire, L. R., Stark, C. E. L., & Clark, R. E. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144130 · Cited by 2,680
A functional analysis of circadian pacemakers in nocturnal rodents
Pittendrigh, C. S., & Daan, S. (1976) · Journal of Comparative Physiology A · doi:10.1007/bf01417856 · Cited by 2,129
Applications of the Morris water maze in the study of learning and memory
D’Hooge, R., & Deyn, P. P. D. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00067-4 · Cited by 2,083
Pittendrigh, C. S., & Daan, S. (1976) · Journal of Comparative Physiology ? A · doi:10.1007/bf01417860 · Cited by 1,636
Neural regulation of circadian rhythms.
Rusak, B., & Zucker, I. (1979) · Physiological Reviews · doi:10.1152/physrev.1979.59.3.449 · Cited by 1,402
Walker, M. P., & Stickgold, R. (2006) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070307 · Cited by 1,075 · cited 2×
“literature that has described how sleep improves learning (29), there is evidence that short periods of sleep (e.”
BackgroundRecognition memory and the medial temporal lobe: a new perspective
Squire, L. R., Wixted, J. T., & Clark, R. E. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2154 · Cited by 1,059
Spatial memory, recognition memory, and the hippocampus
Broadbent, N. J., Squire, L. R., & Clark, R. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406344101 · Cited by 985
Watts, A. G., Swanson, L. W., & Sanchez‐Watts, G. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902580204 · Cited by 678
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Light as a central modulator of circadian rhythms, sleep and affect
LeGates, T. A., Fernandez, D. C., & Hattar, S. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3743 · Cited by 1,001
Light Affects Mood and Learning through Distinct Retina-Brain Pathways
Fernandez, D. C., Fogerson, P. M., Lazzerini Ospri, L., Thomsen, M. B., Layne, R. M., Severin, D., Zhan, J., Singer, J. H., Kirkwood, A., Zhao, H., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.004 · Cited by 505
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
Agorastos, A., Pervanidou, P., Chrousos, G. P., & Baker, D. G. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00118 · Cited by 385
“Memory processing, formation and consolidation are directly influenced by the circadian clock and stress (322, 324, 325).”
BackgroundCircadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance.
Liston, C., Cichon, J. M., Jeanneteau, F., Jia, Z., Chao, M. V., & Gan, W.-B. (2013) · Nature Neuroscience · doi:10.1038/nn.3387 · Cited by 358
Metadata
- Authors
- Ruby, N. F., Hwang, C. E., Wessells, C., Fernandez, F., Zhang, P., Sapolsky, R., & Heller, H. C.
- Affiliations
- Stanford University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2008-10-07
- Volume
- 105
- Issue
- 40
- Pages
- 15593-15598
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2563080
- OpenAlex
- W2140995643
- Cited by
- 234
- References
- 57
- Citations by year
- 2026: 7 · 2025: 3 · 2024: 7 · 2023: 4 · 2022: 9 · 2021: 23 · 2020: 19 · 2019: 13 · 2018: 13 · 2017: 16 · 2016: 16 · 2015: 15 · 2014: 18 · 2013: 23 · 2012: 11
- FWCI
- 5.50
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute (52003745)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- circadian rhythm, hippocampus-dependent learning, memory, Siberian hamster, cardiac arrhythmias, suprachiasmatic nucleus, GABAergic neurotransmission, pentylenetetrazole, novel object recognition
- MeSH terms
- Animals, Circadian Rhythm, Female, gamma-Aminobutyric Acid, Cricetinae, Hippocampus, Learning, Male, Pentylenetetrazole, Sleep, Phodopus
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