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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Studies in Siberian hamsters show that alterations in the photoperiod sometimes lead to loss of circadian rhythmicity and concomitant loss of recall of a novel object.
“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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- 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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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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