The DOI matches its Crossref record; 49 of the 49 references it cites were found in a registry or an index.
A Role for Extracellular Adenosine in Time-Dependent Reversal of Long-Term Potentiation by Low-Frequency Stimulation at Hippocampal CA1 Synapses
Open accessAbstract
The involvement of adenosine on the development of time-dependent reversal of long-term potentiation (LTP) by low-frequency stimulation (LFS) was investigated at Schaffer collateral–CA1 synapses of rat hippocampal slices. A train of LFS (2 Hz, 10 min, 1200 pulses) had no long-term effects on synaptic transmission but produced lasting depression of previously potentiated responses. This reversal of LTP (depotentiation) was observed when the stimulus was delivered ≤3 min after induction of LTP. However, application at 10 min after induction had no detectable effect on potentiation. This time-dependent reversal of LTP by LFS appeared to be mediated by extracellular adenosine, because it was mimicked by bath-applied adenosine and was specifically inhibited by the selective A 1 adenosine receptor antagonist 8-cyclopentyl-1,3-dipropylxanthine (100 n m). The effect of adenosine could be mimicked by 5-HT 1A receptor agonist buspirone, but the LFS-induced depotentiation could not be antagonized by 5-HT 1A receptor antagonist NAN-190. The source of extracellular adenosine in response to LFS appeared to be attributable to the efflux of cAMP. In addition, this LFS-induced depotentiation was blocked by bath application of adenylyl cyclase activator forskolin or injection of a cAMP analog Sp-adenosine cAMP (10 m m) into postsynaptic neurons. Moreover, the selective protein phosphatase 1 and 2A inhibitors okadaic acid and calyculin A prevented the LFS-induced depotentiation. These results thus suggest that increasing extracellular adenosine appears to underlie the LFS-induced depotentiation via acting on the A 1 receptor subtype to interrupt the cAMP-dependent biochemical processes leading to the LTP expression.
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“LTP induced at hippocampal Schaffer collateral synapses can be reversed by low-frequency (1-2 Hz) stimulation mimicking basal conditions as they could occur during SWS, and this depotentiation appears to be essentially mediated through diffuse activation of A1 receptors (576).”
From About Sleep's Role in Memory (2013) · cites this paper as [576]
Experimental — accuracy not yet measuredIn the citing paper
“several types of studies point to the conclusion that the elaborate processes yielding fully developed LTP reach completion within 10–15 min (5, 7, 8);”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [8]
In the citing paper
“Low-frequency (5-Hz) stimulation erases LTP1 if applied shortly after TBS but then becomes progressively less effective over the following 30 min (8, 14);”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [8]
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Citations
Cites
A synaptic model of memory: long-term potentiation in the hippocampus
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Okadaic acid: a new probe for the study of cellular regulation
Cohen, P., Holmes, C. F. B., & Tsukitani, Y. (1990) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(90)90192-e · Cited by 1,373
Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons
Frey, U., Huang, Y.-Y., & Kandel, E. R. (1993) · Science · doi:10.1126/science.8389057 · Cited by 1,218
Abel, T., Nguyen, P. V., Barad, M., Deuel, T. A. S., Kandel, E. R., & Bourtchouladze, R. (1997) · Cell · doi:10.1016/s0092-8674(00)81904-2 · Cited by 1,217
Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation
Barria, A., Muller, D., Derkach, V., Griffith, L. C., & Soderling, T. R. (1997) · Science · doi:10.1126/science.276.5321.2042 · Cited by 1,049
Calyculin A and okadaic acid: Inhibitors of protein phosphatase activity
Ishihara, H., Martin, B. L., Brautigan, D. L., Karaki, H., Ozaki, H., Kato, Y., Fusetani, N., Watabe, S., Hashimoto, K., Uemura, D., et al. (1989) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(89)92189-x · Cited by 1,044
Contrasting properties of two forms of long-term potentiation in the hippocampus
Nicoll, R. A., & Malenka, R. C. (1995) · Nature · doi:10.1038/377115a0 · Cited by 861
An Essential Role for Protein Phosphatases in Hippocampal Long-Term Depression
Mulkey, R. M., Herron, C. E., & Malenka, R. C. (1993) · Science · doi:10.1126/science.8394601 · Cited by 699
Andrade, R., & Nicoll, R. A. (1987) · The Journal of Physiology · doi:10.1113/jphysiol.1987.sp016862 · Cited by 552
The CaM kinase II hypothesis for the storage of synaptic memory.
Lisman, J. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90014-0 · Cited by 526
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Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783
“Encoding induces synaptic long-term potentiation (LTP) or long-term depression (LTD) as major forms of learning-induced synaptic plasticity (222, 527, 616, 629, 1209).”
BackgroundInwardly Rectifying Potassium Channels: Their Structure, Function, and Physiological Roles
Hibino, H., Inanobe, A., Furutani, K., Murakami, S., Findlay, I., & Kurachi, Y. (2010) · Physiological Reviews · doi:10.1152/physrev.00021.2009 · Cited by 1,579
How does adenosine control neuronal dysfunction and neurodegeneration?
Cunha, R. A. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13724 · Cited by 456
New life in an old idea: The synaptic plasticity and memory hypothesis revisited
Martin, S. J., & Morris, R. (2002) · Hippocampus · doi:10.1002/hipo.10107 · Cited by 461
Glial Cell Inhibition of Neurons by Release of ATP
Newman, E. A. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-05-01659.2003 · Cited by 427
Metadata
- Authors
- Huang, C.-C., Liang, Y.-C., & Hsu, K.-S.
- Affiliations
- National Cheng Kung University (TW)
- ORCID
- Hsu, Kuei-Sen
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1999-11-15
- Volume
- 19
- Issue
- 22
- Pages
- 9728-9738
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6782980
- OpenAlex
- W1536302928
- Cited by
- 127
- References
- 49
- Citations by year
- 2025: 2 · 2022: 1 · 2021: 3 · 2020: 1 · 2019: 5 · 2018: 2 · 2017: 4 · 2016: 7 · 2015: 6 · 2014: 9 · 2013: 6 · 2012: 7
- FWCI
- 1.69
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- extracellular adenosine, long-term potentiation, depotentiation, low-frequency stimulation, adenosine A1 receptor, Schaffer collateral-CA1 synapses, hippocampus, cAMP signaling, protein phosphatase 2A, 5-HT1A receptor, buspirone, synaptic plasticity
- MeSH terms
- Adenosine, Cyclic AMP, Animals, Buspirone, Electric Stimulation, Enzyme Inhibitors, Colforsin, Hippocampus, Male, Synaptic Transmission, Neurons, Piperazines, Receptors, Serotonin, Serotonin Antagonists, Synapses, Theobromine, Thionucleotides, Time Factors, Xanthines, Least-Squares Analysis, Rats, Sprague-Dawley, Serotonin Receptor Agonists, Long-Term Potentiation, Pyramidal Cells, Excitatory Postsynaptic Potentials, Receptors, Serotonin, 5-HT1, Rats, Purinergic P1 Receptor Antagonists, In Vitro Techniques
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