Hebbian modification of a hippocampal population pattern in the rat
Open accessAbstract
1. The study of the physiological role of long-term potentiation (LTP) is often hampered by the challenge of finding a physiological event that can be used to assess synaptic strength. We explored the possibility of utilising a naturally occurring event, the hippocampal sharp wave (SPW), for the assessment of synaptic strength and the induction of LTP in vivo. 2. We used two methods in which hippocampal cells were either recorded intracellularly or extracellularly in vivo. In both cases, a linear association between the magnitude of the SPW and cellular responsiveness was observed. 3. LTP was induced by depolarising cells during SPWs by either direct intracellular current injection or extracellular microstimulation adjacent to the cell body. Both of these approaches led to an increase in the slope of the linear association between SPWs and cellular responsiveness. 4. This change was achieved without a rise in overall cell excitability, implying that the synapses providing input to CA1 cells during sharp waves had undergone potentiation. 5. Our findings show that the Hebbian pairing of cellular activation with spontaneous, naturally occurring synaptic events is capable of inducing LTP.
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?
SW-Rs may conversely promote LTP and spike time-dependent plasticity in hippocampal circuits.
“SW-Rs may conversely promote LTP and spike timedependent plasticity in hippocampal circuits (97,159,241,640,777).”
From About Sleep's Role in Memory (2013) · cites this paper as [640]
Cites
Two-stage model of memory trace formation: A role for “noisy” brain states
Buzsáki, G. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90423-5 · Cited by 1,709 · see citing works
Self-citationFear conditioning induces associative long-term potentiation in the amygdala
Rogan, M. T., Stäubli, U. V., & LeDoux, J. E. (1997) · Nature · doi:10.1038/37601 · Cited by 1,310 · see citing works
Intracellular injections of EGTA block induction of hippocampal long-term potentiation
Lynch, G., Larson, J., Kelso, S., Barrionuevo, G., & Schottler, F. (1983) · Nature · doi:10.1038/305719a0 · Cited by 1,116 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762 · Cited by 3,760 · see citing works
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Self-citationControl of sleep and wakefulness
Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E., & McCarley, R. W. (2012) · Physiological Reviews · doi:10.1152/physrev.00032.2011 · Cited by 1,477 · see citing works
Neural syntax: cell assemblies, synapsembles, and readers
Buzsáki, G. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.023 · Cited by 1,289 · see citing works
Self-citationThe reorganization and reactivation of hippocampal maps predict spatial memory performance
Dupret, D., O'Neill, J., Pleydell-Bouverie, B., & Csicsvari, J. (2010) · Nature Neuroscience · doi:10.1038/nn.2599 · Cited by 769 · see citing works
Ripples in the medial temporal lobe are relevant for human memory consolidation
Axmacher, N., Elger, C. E., & Fell, J. (2008) · Brain · doi:10.1093/brain/awn103 · Cited by 372 · see citing works
Hippocampal ripples and memory consolidation
Girardeau, G., & Zugaro, M. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.02.005 · Cited by 330 · see citing works
Hippocampal CA2 sharp-wave ripples reactivate and promote social memory
Oliva, A., Fernández-Ruiz, A., Leroy, F., & Siegelbaum, S. A. (2020) · Nature · doi:10.1038/s41586-020-2758-y · Cited by 268 · see citing works
Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning
Eschenko, O., Ramadan, W., Mölle, M., Born, J., & Sara, S. J. (2008) · Learning & Memory · doi:10.1101/lm.726008 · Cited by 277 · see citing works
Interaction between neocortical and hippocampal networks via slow oscillations
Sirota, A., & Buzsáki, G. (2005) · Thalamus and Related Systems · doi:10.1017/s1472928807000258 · Cited by 270 · see citing works
Self-citationO'Neill, J., Senior, T., & Csicsvari, J. (2006) · Neuron · doi:10.1016/j.neuron.2005.10.037 · Cited by 281 · see citing works
Assembly-specific disruption of hippocampal replay leads to selective memory deficit
Gridchyn, I., Schoenenberger, P., O’Neill, J., & Csicsvari, J. (2020) · Neuron · doi:10.1016/j.neuron.2020.01.021 · Cited by 178 · see citing works
Memory trace replay: The shaping of memory consolidation by neuromodulation
Atherton, L. A., Dupret, D., & Mellor, J. R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.07.004 · Cited by 180 · see citing works
Hippocampal Sharp Wave/Ripples during Sleep for Consolidation of Associative Memory
Ramadan, W., Eschenko, O., & Sara, S. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006697 · Cited by 173 · see citing works
Hippocampal network oscillations at the interplay between innate anxiety and learned fear
Çalışkan, G., & Stork, O. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5109-z · Cited by 72 · see citing works
From remembering to reconstruction: The transformative neural representation of episodic memory.
Xue, G. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102351 · Cited by 49 · see citing works
Kajiya, R., Miyawaki, H., Nakahara, H., & Mizuseki, K. (2025) · eneuro · doi:10.1523/eneuro.0575-24.2025 · Cited by 4 · see citing works
- Authors
- King, C., Henze, D. A., Leinekugel, X., & Buzsáki, G.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 1999-11
- Volume
- 521
- Issue
- 1
- Pages
- 159-167
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC2269637
- OpenAlex
- W2155113153
- Cited by
- 122
- References
- 3
- Citations by year
- 2025: 4 · 2024: 7 · 2023: 6 · 2022: 4 · 2021: 2 · 2020: 4 · 2019: 6 · 2018: 9 · 2017: 2 · 2016: 3 · 2015: 5 · 2014: 5 · 2013: 9 · 2012: 5
- FWCI
- 1.33
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH054671, MH54671)
- National Institute of Neurological Disorders and Stroke (R01NS034994, NS-34994)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- long-term potentiation, Hebbian learning, synaptic efficacy, CA1 pyramidal neurons, microstimulation, intracellular current injection, hippocampus
- MeSH terms
- Animals, Hippocampus, Membrane Potentials, Memory, Neuronal Plasticity, Synapses, Rats, Sprague-Dawley, Long-Term Potentiation, Pyramidal Cells, 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
