Cited by 234Circadian rhythm and melatoninMemory and Neural MechanismsSleep and Wakefulness Research

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Hippocampal-dependent learning requires a functional circadian system

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Ruby, Norman F., Hwang, Calvin E., Wessells, Colin, Fernandez, Fabian, Zhang, Pei, Sapolsky, Robert, Heller, H. Craig·2008·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0808259105PMC PMC2563080

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Abstract

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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Authors: Ruby, N. F., Hwang, C. E., Wessells, C., Fernandez, F., Zhang, P., Sapolsky, R., & Heller, H. C.
Affiliations: Stanford University (US)
ORCID: Ruby, Norman F.
Hwang, Calvin E.
Fernandez, Fabian
Zhang, Pei
Sapolsky, Robert
Heller, H. Craig
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
DOI: 10.1073/pnas.0808259105
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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Hippocampal-dependent learning requires a functional circadian system

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