Asymptotic hippocampal long-term potentiation in rats does not preclude additional potentiation at later phases
Abstract
Hippocampal long-term potentiation may serve as an elementary process underlying certain forms of learning and memory in vertebrates. As is the case with behavioural memory, hippocampal long-term potentiation in the CA1 region and in the dentate gyrus exhibits distinct phases. These comprise a short-term early potentiation which lasts one to three hours and is independent of protein synthesis and is characterized in general by the activation of N-methyl-D-aspartate receptors and protein kinases; and a later, longer lasting phase, which can be separated by inhibitors of protein synthesis. Here, we report that the prior induction of long-term potentiation, both in the dentate gyrus in vivo and in the CA1-region in vitro, precludes further long-term but not short-term potentiation by means of a newly delivered conditioning stimulus to a subset of the same activated synapse population during the early stage (approximately 1-3 hours post tetanus). In contrast, a subsequent, long-lasting potentiation can be induced after the establishment of the late phase of potentiation (> 4 h). Thus, the system preserves the capacity for short-term potentiation immediately after potentiation, but the capacity for the induction of longer lasting plastic changes is recovered only after about four hours. Our results demonstrate that, once long-term potentiation has been established, hippocampal neurons do not lose their capacity for functional plasticity during certain phases of the maintenance of long-term potentiation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Additional potentiation can be induced four hours after induction of LTP1.
“Other studies using variable stimulation intensities suggest that additional potentiation can be induced four hours after induction of LTP1 (10, 12).”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [12]
Cites
Inhibition of Postsynaptic PKC or CaMKII Blocks Induction But Not Expression of LTP
Malinow, R., Schulman, H., & Tsien, R. W. (1989) · Science · doi:10.1126/science.2549638 · Cited by 1,325 · see citing works
Impaired Long-Term Potentiation, Spatial Learning, and Hippocampal Development in fyn Mutant Mice
Grant, S. G. N., O’Dell, T. J., Karl, K. A., Stein, P. L., Soriano, P. M., & Kandel, E. R. (1992) · Science · doi:10.1126/science.1361685 · Cited by 1,154 · see citing works
An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation
Malenka, R. C., Kauer, J. A., Perkel, D. J., Mauk, M. D., Kelly, P. T., Nicoll, R. A., & Waxham, M. N. (1989) · Nature · doi:10.1038/340554a0 · Cited by 1,025 · see citing works
Frey, U., Krug, M., Reymann, K. G., & Matthies, H. (1988) · Brain Research · doi:10.1016/0006-8993(88)90008-x · Cited by 806 · see citing works
Self-citationMontarolo, P. G., Goelet, P., Castellucci, V. F., Morgan, J., Kandel, E. R., & Schacher, S. (1986) · Science · doi:10.1126/science.3775383 · Cited by 769 · see citing works
Long-term potentiation in the hippocampus is blocked by tyrosine kinase inhibitors
O’Dell, T. J., Kandel, E. R., & Grant, S. G. N. (1991) · Nature · doi:10.1038/353558a0 · Cited by 521 · see citing works
Krug, M., Lössner, B., & Ott, T. (1984) · Brain Research Bulletin · doi:10.1016/0361-9230(84)90005-4 · Cited by 509 · see citing works
NMDA application potentiates synaptic transmission in the hippocampus
Kauer, J. A., Malenka, R. C., & Nicoll, R. A. (1988) · Nature · doi:10.1038/334250a0 · Cited by 423 · see citing works
Otani, S., Marshall, C. J., Tate, W. P., Goddard, G. V., & Abraham, W. C. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90001-8 · Cited by 274 · see citing works
Alkon, D. L., Amaral, D. G., Bear, M. F., Black, J., Carew, T. J., Cohen, N. J., Disterhoft, J. F., Eichenbaum, H., Golski, S., Gorman, L. K., et al. (1991) · Brain Research Reviews · doi:10.1016/0165-0173(91)90005-s · Cited by 212 · see citing works
Two sensitive periods for the amnesic effect of anisomycin
Grecksch, G., & Matthies, H. (1980) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(80)90145-8 · Cited by 194 · see citing works
Reymann, K. G., Brödemann, R., Kase, H., & Matthies, H. ̈. (1988) · Brain Research · doi:10.1016/0006-8993(88)90274-0 · Cited by 153 · see citing works
Self-citationChanges in protein synthesis accompanying long-term potentiation in the dentate gyrus in vivo
Fazeli, M., Corbet, J., Dunn, M., DOLPHIN, A. C., & Bliss, T. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-04-01346.1993 · Cited by 117 · see citing works
The effects of repeated induction of long-term potentiation in the dentate gyrus
de Jonge, M., & Racine, R. J. (1985) · Brain Research · doi:10.1016/0006-8993(85)91341-1 · Cited by 53 · see citing works
Lössner, B., Schweigert, C., Krug, M., et al. (1990) · PubMed · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Synaptic tagging and long-term potentiation
Frey, U., & Morris, R. G. M. (1997) · Nature · doi:10.1038/385533a0 · Cited by 1,736 · see citing works
BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis
Bramham, C. R., & Messaoudi, E. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.06.003 · Cited by 1,193 · see citing works
Structural and Molecular Remodeling of Dendritic Spine Substructures during Long-Term Potentiation
Bosch, M., Castro, J., Saneyoshi, T., Matsuno, H., Sur, M., & Hayashi, Y. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.021 · Cited by 637 · see citing works
Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation
Frey, U., & Morris, R. G. M. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01189-2 · Cited by 615 · see citing works
Self-citationImpaired Spatial Learning after Saturation of Long-Term Potentiation
Moser, E. I., Krobert, K. A., Moser, M.-B., & Morris, R. G. M. (1998) · Science · doi:10.1126/science.281.5385.2038 · Cited by 505 · 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
Synaptic evidence for the efficacy of spaced learning
Kramár, E. A., Babayan, A. H., Gavin, C. F., Cox, C. D., Jafari, M., Gall, C. M., Rumbaugh, G., & Lynch, G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1120700109 · Cited by 192 · see citing works
Frey, S., & Frey, J. U. (2008) · Progress in brain research · doi:10.1016/s0079-6123(07)00007-6 · Cited by 139 · see citing works
Lynch, G., Kramár, E. A., Babayan, A. H., Rumbaugh, G., & Gall, C. M. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.07.006 · Cited by 97 · see citing works
Relationship between increase in astrocytic GLT-1 glutamate transport and late-LTP
Pita-Almenar, J. D., Zou, S., Colbert, C. M., & Eskin, A. (2012) · Learning & Memory · doi:10.1101/lm.023259.111 · Cited by 52 · see citing works
Cao, G., & Harris, K. M. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00297.2014 · Cited by 41 · see citing works
- Authors
- Frey, U., Schollmeier, K., Reymann, K. G., & Seidenbecher, T.
- Corresponding author
- Frey, U.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 1995-08
- Volume
- 67
- Issue
- 4
- Pages
- 799-807
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2004746599
- Cited by
- 93
- References
- 15
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 4 · 2022: 1 · 2021: 1 · 2020: 2 · 2018: 2 · 2017: 1 · 2016: 4 · 2015: 5 · 2014: 6 · 2013: 2 · 2012: 4
- FWCI
- 1.85
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- long-term potentiation, hippocampus, CA1 region, dentate gyrus, short-term potentiation, synaptic plasticity, tetanic stimulation, protein synthesis, NMDA receptor, protein kinases, memory formation
- MeSH terms
- Animals, Cerebellar Nuclei, Electric Stimulation, Evoked Potentials, Hippocampus, Male, Time Factors, Rats, Wistar, Long-Term Potentiation, Rats
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
