Circadian regulation of hippocampal long-term potentiation
Open accessAbstract
The goal of this study is to investigate the possible circadian regulation of hippocampal excitability and long-term potentiation (LTP) measured by stimulating the Schaffer collaterals (SC) and recording the field excitatory postsynaptic potential (fEPSP) from the CA1 dendritic layer or the population spike (PS) from the soma in brain slices of C3H and C57 mice. These 2 strains of mice were of interest because the C3H mice secrete melatonin rhythmically while the C57 mice do not. The authors found that the magnitude of the enhancement of the PS was significantly greater in LTP recorded from night slices compared to day slices of both C3H and C57 mice. They also found significant diurnal variation in the decay of LTP measured with fEPSPs, with the decay slower during the night in both strains of mice. There was evidence for a diurnal rhythm in the input/output function of pyramidal neurons measured at the soma in C57 but not C3H mice. Furthermore, LTP in the PS, measured in slices prepared during the day but recorded during the night, had a profile remarkably similar to the night group. Finally, PS recordings were carried out in slices from C3H mice maintained in constant darkness prior to experimentation. Again, the authors found that the magnitude of the enhancement of the PS was significantly greater in LTP recorded from subjective night slices compared to subjective day slices. These results provide the 1st evidence that an endogenous circadian oscillator modulates synaptic plasticity in the hippocampus.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Projections from the suprachiasmatic nucleus to the locus coeruleus are important for contextual fear conditioning, circadian regulation of the sleep-wake cycle, and synaptic plasticity including long-term potentiation.
“contextual fear conditioning, circadian regulation of the sleep-wake cycle (Gonzales and Aston-Jones, 2006), and synaptic plasticity including long-term potentiation- (Chaudhury et al., 2005; Chaudhury and Colwell, 2002).”
From Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges (2009) · cites this paper as Chaudhury et al., 2005
Circadian rhythms in contextual fear conditioning and synaptic plasticity (long-term potentiation) have been reported in mice.
“For example, circadian rhythms in contextual fear conditioning and synaptic plasticity (long-term potentiation, LTP) have been reported in mice (Chaudhury et al., 2005; Chaudhury and Colwell, 2002).”
From Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges (2009) · cites this paper as Chaudhury et al., 2005
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Coordination of circadian timing in mammals
Reppert, S. M., & Weaver, D. R. (2002) · Nature · doi:10.1038/nature00965 · Cited by 4,379 · see citing works
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,423 · see citing works
Running enhances neurogenesis, learning, and long-term potentiation in mice
van Praag, H., Christie, B. R., Sejnowski, T. J., & Gage, F. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13427 · Cited by 2,904 · see citing works
Synaptic Plasticity and Memory: An Evaluation of the Hypothesis
Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.649 · Cited by 2,794 · see citing works
Resetting central and peripheral circadian oscillators in transgenic rats
Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R.-I., Ueda, M., Block, G. D., Sakaki, Y., Menaker, M., & Tei, H. (2000) · Science · doi:10.1126/science.288.5466.682 · Cited by 1,907 · see citing works
Practice with Sleep Makes Perfect
Walker, M. P., Brakefield, T., Morgan, A., Hobson, J. A., & Stickgold, R. (2002) · Neuron · doi:10.1016/s0896-6273(02)00746-8 · Cited by 1,307 · see citing works
A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons
Magee, J. C., & Johnston, D. (1997) · Science · doi:10.1126/science.275.5297.209 · Cited by 1,303 · see citing works
The role of sleep in learning and memory
Maquet, P. (2001) · Science · doi:10.1126/science.1062856 · Cited by 1,177 · see citing works
Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition
Pouille, F., & Scanziani, M. (2001) · Science · doi:10.1126/science.1060342 · Cited by 1,097 · see citing works
Dissociable stages of human memory consolidation and reconsolidation
Walker, M. P., Brakefield, T., Allan Hobson, J., & Stickgold, R. (2003) · Nature · doi:10.1038/nature01930 · Cited by 1,025 · see citing works
The acute effects of corticosteroids on cognition: integration of animal and human model studies
LUPIEN, S., & MCEWEN, B. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00004-0 · Cited by 1,024 · see citing works
Farmer, J., Zhao, X., van Praag, H., Wodtke, K., Gage, F. H., & Christie, B. R. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.09.029 · Cited by 836 · see citing works
Sleep, learning, and dreams: off-line memory reprocessing
Stickgold, R., Hobson, J. A., Fosse, R., & Fosse, M. (2001) · Science · doi:10.1126/science.1063530 · Cited by 762 · see citing works
Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance
Dijk, D., Duffy, J. F., & Czeisler, C. A. (1992) · Journal of Sleep Research · doi:10.1111/j.1365-2869.1992.tb00021.x · Cited by 602 · see citing works
The REM sleep-memory consolidation hypothesis
Siegel, J. M. (2001) · Science · doi:10.1126/science.1063049 · Cited by 568 · see citing works
Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice
Green, D. J., & Gillette, R. (1982) · Brain Research · doi:10.1016/0006-8993(82)90361-4 · Cited by 503 · cited 1× · see citing works
“It is already well established that cells in the SCN continue to show circadian oscillations when isolated from the animal in a hypothalamic brain slice preparation (e.g., Green and Gillette, 1982) and we sought to determine if diurnal differences in LTP could also be found in the hippocampus.”
McDermott, C. M., LaHoste, G. J., Chen, C., Musto, A., Bazan, N. G., & Magee, J. C. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-29-09687.2003 · Cited by 407 · see citing works
Buijs, R. M., van Eden, C. G., Goncharuk, V. D., & Kalsbeek, A. (2003) · Journal of Endocrinology · doi:10.1677/joe.0.1770017 · Cited by 387 · see citing works
Localization and characterization of melatonin receptors in rodent brain by in vitro autoradiography
Weaver, D. R., Rivkees, S., & Reppert, S. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-07-02581.1989 · Cited by 357 · see citing works
Genetic Control of Melatonin Synthesis in the Pineal Gland of the Mouse
Ebihara, S., Marks, T. N., Hudson, D. J., & Menaker, M. (1986) · Science · doi:10.1126/science.3941912 · Cited by 354 · see citing works
Effects of chronic stress on hippocampal long‐term potentiation
Pavlides, C., Nivón, L. G., & McEwen, B. S. (2002) · Hippocampus · doi:10.1002/hipo.1116 · Cited by 316 · see citing works
Wakamatsu, H., Yoshinobu, Y., Aida, R., Moriya, T., Akiyama, M., & Shibata, S. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01483.x · Cited by 308 · see citing works
Circadian modulation of learning and memory in fear-conditioned mice.
Chaudhury, D., & Colwell, C. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00471-5 · Cited by 282 · see citing works
Self-citationMolecular and cellular cognitive studies of the role of synaptic plasticity in memory
Silva, A. J. (2002) · Journal of Neurobiology · doi:10.1002/neu.10169 · Cited by 279 · see citing works
Neuronal transmission through hippocampal pathways dependent on behavior
Winson, J., & Abzug, C. (1978) · Journal of Neurophysiology · doi:10.1152/jn.1978.41.3.716 · Cited by 262 · see citing works
Long-term potentiation: outstanding questions and attempted synthesis
Lisman, J. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1242 · Cited by 240 · see citing works
Role of adenosine in behavioral state modulation: a microdialysis study in the freely moving cat
Portas, C. M., Thakkar, M. M., Rainnie, D. G., Greene, R. W., & McCarley, R. W. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00640-9 · Cited by 208 · see citing works
Differential modulation of GABAA receptor function by Mel1a and Mel1b receptors
Wan, Q., Man, H., Liu, F., Braunton, J., Niznik, H. B., Pang, S. F., Brown, G. M., & Wang, Y. T. (1999) · Nature Neuroscience · doi:10.1038/8062 · Cited by 194 · see citing works
Huston, J. P., Haas, H. L., Boix, F., Pfister, M., Decking, U. K. M., Schrader, J., & Schwarting, R. K. W. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00021-8 · Cited by 184 · see citing works
Sleep Deprivation Impairs Long-Term Potentiation in Rat Hippocampal Slices
Campbell, I. G., Guinan, M. J., & Horowitz, J. M. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.2.1073 · Cited by 169 · see citing works
Melatonin receptors in rat hippocampus: molecular and functional investigations
Mußhoff, U., Riewenherm, D., Berger, E., Fauteck, J., & Speckmann, E. (2002) · Hippocampus · doi:10.1002/hipo.1105 · Cited by 169 · see citing works
Winson, J., & Abzug, C. (1977) · Science · doi:10.1126/science.193192 · Cited by 143 · see citing works
Circadian Rhythm of Synaptic Excitability in Rat And Monkey Central Nervous System
Barnes, C. A., McNaughton, B. L., Goddard, G. V., Douglas, R. M., & Adamec, R. E. (1977) · Science · doi:10.1126/science.194313 · Cited by 138 · see citing works
Multiphasic Retention Deficits at Periodic Intervals after Passive-Avoidance Learning
Holloway, F. A., & Wansley, R. A. (1973) · Science · doi:10.1126/science.180.4082.208 · Cited by 136 · see citing works
Cholinergic Activity Enhances Hippocampal Long-Term Potentiation in CA1 during Walking in Rats
Leung, L.-W. S., Bixia Shen, A., Rajakumar, N., & Ma, J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-28-09297.2003 · Cited by 129 · see citing works
Multiple retention deficits at periodic intervals after active and passive avoidance learning
Holloway, F. A., & Wansley, R. A. (1973) · Behavioral Biology · doi:10.1016/s0091-6773(73)80164-6 · Cited by 127 · see citing works
Davis, C. J., Harding, J. W., & Wright, J. W. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02508-3 · Cited by 115 · see citing works
Melatonin regulates neuronal plasticity in the hippocampus
El‐Sherif, Y., Tesoriero, J., Hogan, M. V., & Wieraszko, A. (2003) · Journal of Neuroscience Research · doi:10.1002/jnr.10605 · Cited by 114 · see citing works
Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity
McBain, C. J., Freund, T. F., & Mody, I. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01347-2 · Cited by 113 · see citing works
Discrimination of circadian phase in intact and suprachiasmatic nuclei-ablated rats
Mistlberger, R. E., de Groot, M. H. M., Bossert, J. M., & Marchant, E. G. (1996) · Brain Research · doi:10.1016/s0006-8993(96)00466-0 · Cited by 112 · see citing works
Effect of Circadian Phase on Performance of Rats in the Morris Water Maze Task
Valentinuzzi, V. S., Menna-Barreto, L. S., & Xavier, G. F. (2004) · Journal of Biological Rhythms · doi:10.1177/0748730404265688 · Cited by 94 · see citing works
Multiple retention deficit in passive avoidance in rats is eliminated by suprachiasmatic lesions
Stephan, F. K., & Kovacević, N. (1978) · Behavioral Biology · doi:10.1016/s0091-6773(78)92565-8 · Cited by 88 · see citing works
Age differences in a circadian influence on hippocamapl LTP
Harris, K. M., & Teyler, T. J. (1983) · Brain Research · doi:10.1016/0006-8993(83)91284-2 · Cited by 85 · see citing works
Biebach, H., Falk, H., & Krebs, J. R. (1991) · Journal of Biological Rhythms · doi:10.1177/074873049100600406 · Cited by 82 · see citing works
Rats use an ordinal timer in a daily time-place learning task.
Carr, J., & Wilkie, D. M. (1997) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.23.2.232 · Cited by 65 · see citing works
Siuciak, J. A., Fang, J., & Dubocovich, M. L. (1990) · European Journal of Pharmacology · doi:10.1016/0014-2999(90)90328-4 · Cited by 65 · see citing works
Effect of adrenalectomy on the circadian rhythm of LTP
Dana, R. C., & Martinez, J. L. (1984) · Brain Research · doi:10.1016/0006-8993(84)91086-2 · Cited by 64 · see citing works
Circadian modulation of long-term sensitization in Aplysia
Fernandez, R. I., Lyons, L. C., Levenson, J. M., Khabour, O. F., & Eskin, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2336172100 · Cited by 62 · see citing works
Multiple retention deficits following one-trial appetitive training
Wansley, R. A., & Holloway, F. A. (1975) · Behavioral Biology · doi:10.1016/s0091-6773(75)90135-2 · Cited by 59 · see citing works
Effect of circadian phase on context and cued fear conditioning in C57BL/6J mice
Valentinuzzi, V. S., Kolker, D. E., Vitaterna, M. H., Ferrari, E. A. M., Takahashi, J. S., & Turek, F. W. (2001) · Animal Learning & Behavior · doi:10.3758/bf03192822 · Cited by 58 · see citing works
Marder, C. P., & Buonomano, D. V. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00112.2003 · Cited by 55 · see citing works
Electrophysiological characterisation of the dentate gyrus in five inbred strains of mouse
Bampton, E. T. W., Gray, R., & Large, C. H. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01811-9 · Cited by 50 · see citing works
Diurnal modulation of long-term potentiation in the hamster hippocampal slice
Raghavan, A. V., Horowitz, J. M., & Fuller, C. A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01523-1 · Cited by 50 · see citing works
Cossart, R., Hirsch, J., Cannon, R. C., Dinoncourt, C., Wheal, H., Ben-Ari, Y., Esclapez, M., & Bernard, C. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00231-1 · Cited by 46 · see citing works
Memory mechanisms: The yin and yang of protein phosphorylation
Sweatt, J. D. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00216-0 · Cited by 46 · see citing works
Collins, D. R., & Davies, S. N. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00733-6 · Cited by 44 · see citing works
Kole, M. H. P., Koolhaas, J. M., Luiten, P. G. M., & Fuchs, E. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)01926-7 · Cited by 40 · see citing works
Brunel, S., & de Montigny, C. (1987) · Brain Research Bulletin · doi:10.1016/0361-9230(87)90191-2 · Cited by 30 · see citing works
Breakfast in the nook and dinner in the dining room: time-of-day discrimination in rats
Means, L. W., Ginn, S. R., Arolfo, M. P., et al. (2000) · Behavioural Processes · doi:10.1016/s0376-6357(00)00068-1 · Cited by 27 · see citing works
Circadian differences in maze performance of C57BI/6 Ola mice
Hoffmann, H. J., & Balschun, D. (1992) · Behavioural Processes · doi:10.1016/0376-6357(92)90017-8 · Cited by 27 · see citing works
Learning and Circadian Behavior
Daan, S. (2000) · Journal of Biological Rhythms · doi:10.1177/074873000129001396 · Cited by 24 · see citing works
Circadian modulation of granule cell response to perforant path synaptic input in the rat
West, M. O., & Deadwyler, S. A. (1980) · Neuroscience · doi:10.1016/0306-4522(80)90023-8 · Cited by 20 · see citing works
Cauller, L. J., Boulos, Z., & Goddard, G. V. (1985) · Brain Research · doi:10.1016/0006-8993(85)90517-7 · Cited by 18 · see citing works
Liu, D. K.-C., Horner, R. L., & Wojtowicz, J. M. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)00881-8 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mechanisms linking circadian clocks, sleep, and neurodegeneration
Musiek, E. S., & Holtzman, D. M. (2016) · Science · doi:10.1126/science.aah4968 · Cited by 878 · see citing works
Ridding, M. C., & Ziemann, U. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.190314 · Cited by 787 · see citing works
Reactive Oxygen Species in the Regulation of Synaptic Plasticity and Memory
Massaad, C. A., & Klann, E. (2011) · Antioxidants & Redox Signaling · doi:10.1089/ars.2010.3208 · Cited by 635 · 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
Neuroplasticity Mediated by Altered Gene Expression
McClung, C. A., & Nestler, E. J. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301544 · Cited by 347 · see citing works
Sleep and wakefulness out of phase with internal biological time impairs learning in humans
Wright, K. P., Hull, J. T., Hughes, R. J., Ronda, J. M., & Czeisler, C. A. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.4.508 · Cited by 191 · see citing works
A time to remember: The role of circadian clocks in learning and memory.
Smarr, B. L., Jennings, K. J., Driscoll, J. R., & Kriegsfeld, L. J. (2014) · Behavioral Neuroscience · doi:10.1037/a0035963 · Cited by 166 · see citing works
Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges
Benca, R., Duncan, M. J., Frank, E., McClung, C., Nelson, R. J., & Vicentic, A. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.09.005 · Cited by 125 · see citing works
Exercising our brains: how physical activity impacts synaptic plasticity in the dentate gyrus.
Christie, B. R., Eadie, B. D., Kannangara, T. S., Robillard, J. M., Shin, J., & Titterness, A. K. (2008) · NeuroMolecular Medicine · doi:10.1007/s12017-008-8033-2 · Cited by 99 · see citing works
Hoyt, K. R., & Obrietan, K. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00537-9 · Cited by 77 · see citing works
Koresh, O., Kozlovsky, N., Kaplan, Z., Zohar, J., Matar, M. A., & Cohen, H. (2012) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2011.07.012 · Cited by 40 · see citing works
- Authors
- Chaudhury, D., Wang, L. M., & Colwell, C. S.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Colwell, Christopher S.
- Venue
- Journal of Biological Rhythms
- Publisher
- SAGE Publications
- Published
- 2005-06
- Volume
- 20
- Issue
- 3
- Pages
- 225-236
- ISSN
- 0748-7304 (ISSN-L)
- 1552-4531
- PMC
- PMC2581477
- OpenAlex
- W2117889752
- Cited by
- 231
- References
- 64
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 2 · 2023: 16 · 2022: 10 · 2021: 16 · 2020: 13 · 2019: 16 · 2018: 13 · 2017: 10 · 2016: 13 · 2015: 6 · 2014: 14 · 2013: 6 · 2012: 13
- FWCI
- 2.66
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Journal of Biological Rhythms (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Mental Health (R03MH059186)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- circadian rhythm, long-term potentiation, hippocampus, melatonin, C3H mice, C57 mice, diurnal variation, synaptic plasticity, Schaffer collateral stimulation, CA1, population spike, input-output function, pyramidal neurons, constant darkness
- MeSH terms
- Animals, Circadian Rhythm, Darkness, Dendrites, Electrophysiology, Hippocampus, Male, Mice, Inbred C3H, Mice, Inbred C57BL, Long-Term Potentiation, Excitatory Postsynaptic Potentials, Mice, In Vitro Techniques
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
