High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat
Open accessAbstract
Population bursts of the CA3 network, which occur during eating, drinking, awake immobility, and slow-wave sleep, produce a large field excitatory postsynaptic potential throughout stratum radiatum of the CA1 field (sharp wave). The CA3 burst sets into motion a short-lived, dynamic interaction between CA1 pyramidal cells and interneurons, the product of which is a 200 Hz oscillatory field potential (ripple) and phase-related discharge of the CA1 network. Although many CA1 pyramidal neurons discharge during the time frame (50–100 msec) of each sharp wave, each wave of a ripple (∼5 msec) reflects the synchronization of more discrete subsets of CA1 neurons. When we used multi-site recordings in freely behaving rats, we observed ripples throughout the longitudinal extent (∼4–5 mm) of the dorsal CA1 region that were coherent for multiple cycles of each ripple. High-frequency ripples were also observed throughout the hippocampal–entorhinal output pathway that were concurrent but less coherent on a cycle-by-cycle basis. Single and multiunit neuronal activity was phase-related to local ripples throughout the hippocampal–entorhinal output pathway. Entorhinal ripples occurred 5–30 msec after the CA1 ripples and were related to the occurrence of an entorhinal sharp wave. Thus, during each hippocampal sharp wave, there is a powerful synchronization among the neuronal networks that connect the hippocampus to the neocortex. We suggest that this population interaction (1) biologically constrains theoretical models of hippocampal function and dysfunction and (2) has the capacity to support an “off-line” memory consolidation process.
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 occur mainly during SWS but also during nonexploratory wakefulness.
“SW-Rs occur mainly during SWS but also during nonexploratory wakefulness (e.g., drinking, grooming, and quiet wakefulness).”
From About Sleep's Role in Memory (2013) · cites this paper as [196]
Cites
Hebb, D. O. (2005) · doi:10.4324/9781410612403 · Cited by 9,825 · see citing works
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
Simple memory: a theory for archicortex
Marr, D. (1971) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1971.0078 · Cited by 2,771 · see citing works
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-citationHippocampal CA1 interneurons: an in vivo intracellular labeling study
Sik, A., Penttonen, M., Ylinen, A., & Buzsaki, G. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06651.1995 · Cited by 669 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
“, high-frequency local field potential oscillations (100– 300 Hz) originating in CA1] to form SW-R events (159, 162, 196, 241, 459, 832, 1342).”
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-citationSelective suppression of hippocampal ripples impairs spatial memory
Girardeau, G., Benchenane, K., Wiener, S. I., Buzsáki, G., & Zugaro, M. B. (2009) · Nature Neuroscience · doi:10.1038/nn.2384 · Cited by 1,560 · 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
Grouping of brain rhythms in corticothalamic systems
Steriade, M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.029 · Cited by 1,296 · see citing works
Coordinated interactions between hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep
Siapas, A. G., & Wilson, M. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80629-7 · Cited by 1,052 · see citing works
Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval
Carr, M. F., Jadhav, S. P., & Frank, L. M. (2011) · Nature Neuroscience · doi:10.1038/nn.2732 · Cited by 958 · see citing works
Pape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · see citing works
Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat
Csicsvari, J., Hirase, H., Czurkó, A., Mamiya, A., & Buzsáki, G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-01-00274.1999 · Cited by 966 · see citing works
Self-citationReplay and Time Compression of Recurring Spike Sequences in the Hippocampus
Nádasdy, Z., Hirase, H., Czurkó, A., Csicsvari, J., & Buzsáki, G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-21-09497.1999 · Cited by 932 · see citing works
Self-citationHippocampal replay of extended experience
Davidson, T. J., Kloosterman, F., & Wilson, M. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.027 · Cited by 806 · see citing works
“During pauses in locomotion and during slow-wave sleep, many place cells are recruited in intermittent population bursts, which are accompanied by ripples in the hippocampal local field potential (Buzsáki et al., 1992; Chrobak and Buzsáki, 1996).”
Learning-dependent increases in sleep spindle density
Gais, S., Mölle, M., Helms, K., & Born, J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06830.2002 · Cited by 859 · see citing works
Buzsáki, G. (2005) · Hippocampus · doi:10.1002/hipo.20113 · Cited by 872 · see citing works
Self-citationAwake replay of remote experiences in the hippocampus
Karlsson, M. P., & Frank, L. M. (2009) · Nature Neuroscience · doi:10.1038/nn.2344 · Cited by 769 · see citing works
GABAergic Cells Are the Major Postsynaptic Targets of Mossy Fibers in the Rat Hippocampus
Acsády, L., Kamondi, A., Sı́k, A., Freund, T., & Buzsáki, G. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03386.1998 · Cited by 741 · see citing works
Self-citationMizuseki, K., Sirota, A., Pastalkova, E., & Buzsáki, G. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.037 · Cited by 718 · see citing works
Self-citationElectrical coupling underlies high-frequency oscillations in the hippocampus in vitro
Draguhn, A., Traub, R. D., Schmitz, D., & Jefferys, J. G. R. (1998) · Nature · doi:10.1038/28184 · Cited by 703 · see citing works
Hippocampal network patterns of activity in the mouse
Buzsáki, G., Buhl, D. L., Harris, K. D., Csicsvari, J., Czéh, B., & Morozov, A. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00669-3 · Cited by 486 · see citing works
Self-citationThe hippocampal sharp wave-ripple in memory retrieval for immediate use and consolidation
Joo, H. R., & Frank, L. M. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0077-1 · Cited by 430 · see citing works
Rewarded Outcomes Enhance Reactivation of Experience in the Hippocampus
Singer, A. C., & Frank, L. M. (2009) · Neuron · doi:10.1016/j.neuron.2009.11.016 · Cited by 385 · see citing works
The Role of Hippocampal Replay in Memory and Planning
Ólafsdóttir, H. F., Bush, D., & Barry, C. (2018) · Current Biology · doi:10.1016/j.cub.2017.10.073 · Cited by 413 · 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
Memory trace reactivation in hippocampal and neocortical neuronal ensembles
Sutherland, G. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00079-9 · Cited by 384 · see citing works
A cortical-hippocampal-cortical loop of information processing during memory consolidation
Rothschild, G., Eban, E., & Frank, L. M. (2017) · Nature Neuroscience · doi:10.1038/nn.4457 · Cited by 387 · see citing works
Neuronal Diversity in GABAergic Long-Range Projections from the Hippocampus
Jinno, S., Klausberger, T., Marton, L. F., Dalezios, Y., Roberts, J. D. B., Fuentealba, P., Bushong, E. A., Henze, D., Buzsáki, G., & Somogyi, P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1847-07.2007 · Cited by 369 · see citing works
Self-citationEffects of early and late nocturnal sleep on priming and spatial memory
Plihal, W., & Born, J. (1999) · Psychophysiology · doi:10.1111/1469-8986.3650571 · Cited by 364 · see citing works
Cannabinoids reveal importance of spike timing coordination in hippocampal function
Robbe, D., Montgomery, S. M., Thome, A., Rueda-Orozco, P. E., McNaughton, B. L., & Buzsaki, G. (2006) · Nature Neuroscience · doi:10.1038/nn1801 · Cited by 333 · see citing works
State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep
Wierzynski, C. M., Lubenov, E. V., Gu, M., & Siapas, A. G. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.011 · Cited by 289 · see citing works
Reactivations of emotional memory in the hippocampus-amygdala system during sleep
Girardeau, G., Inema, I., & Buzsáki, G. (2017) · Nature Neuroscience · doi:10.1038/nn.4637 · Cited by 266 · see citing works
Self-citationPennartz, C. M. A., Lee, E., Verheul, J., Lipa, P., Barnes, C. A., & McNaughton, B. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0575-04.2004 · Cited by 282 · see citing works
New Experiences Enhance Coordinated Neural Activity in the Hippocampus
Cheng, S., & Frank, L. M. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.035 · Cited by 286 · 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-citationConnexin expression in electrically coupled postnatal rat brain neurons
Venance, L., Rozov, A., Blatow, M., Burnashev, N., Feldmeyer, D., & Monyer, H. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.160037097 · Cited by 273 · see citing works
Hippocampal sharp-wave ripples linked to visual episodic recollection in humans
Norman, Y., Yeagle, E. M., Khuvis, S., Harel, M., Mehta, A. D., & Malach, R. (2019) · Science · doi:10.1126/science.aax1030 · Cited by 270 · 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
Use it or lose it: how neurogenesis keeps the brain fit for learning
Shors, T. J., Anderson, M. L., Curlik, D. M., & Nokia, M. S. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.023 · Cited by 190 · see citing works
H2 histamine receptor-phosphorylation of Kv3.2 modulates interneuron fast spiking
Atzori, M., Lau, D., Tansey, E. P., Chow, A., Ozaita, A., Rudy, B., & McBain, C. J. (2000) · Nature Neuroscience · doi:10.1038/77693 · Cited by 109 · see citing works
Dexamethasone blocks sleep induced improvement of declarative memory
Plihal, W., Pietrowsky, R., & Born, J. (1999) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00080-8 · Cited by 90 · see citing works
A Novel Type of GABAergic Interneuron Connecting the Input and the Output Regions of the Hippocampus
Ceranik, K., Bender, R., Geiger, J. R. P., Monyer, H., Jonas, P., Frotscher, M., & Lübke, J. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05380.1997 · Cited by 83 · see citing works
Structural organization of long-range GABAergic projection system of the hippocampus
Jinno, S. (2009) · Frontiers in Neuroanatomy · doi:10.3389/neuro.05.013.2009 · Cited by 75 · see citing works
Yang, M., Logothetis, N. K., & Eschenko, O. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.2107-18.2018 · Cited by 57 · see citing works
Interneuron control of hippocampal oscillations
Allen, K., & Monyer, H. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.08.016 · Cited by 64 · see citing works
Fukuda, T., & Kosaka, T. (2000) · Neuroscience Research · doi:10.1016/s0168-0102(00)00163-2 · Cited by 63 · see citing works
Thalamocortical Oscillations: Local Control of EEG Slow Waves
Timofeev, I., & Chauvette, S. (2011) · Current Topics in Medicinal Chemistry · doi:10.2174/156802611797470376 · Cited by 55 · see citing works
Katona, L., Micklem, B., Borhegyi, Z., Swiejkowski, D. A., Valenti, O., Viney, T. J., Kotzadimitriou, D., Klausberger, T., & Somogyi, P. (2017) · Hippocampus · doi:10.1002/hipo.22696 · Cited by 50 · see citing works
Brain State Dependence of Hippocampal Subthreshold Activity in Awake Mice
Hulse, B. K., Lubenov, E. V., & Siapas, A. G. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.11.084 · Cited by 40 · see citing works
Fast effects of glucocorticoids on memory-related network oscillations in the mouse hippocampus
Weiss, E. K., Krupka, N., Bähner, F., Both, M., & Draguhn, A. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01699.x · Cited by 23 · see citing works
- Authors
- Chrobak, J. J., & Buzsáki, G.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- ORCID
- Chrobak, James J.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1996-05-01
- Volume
- 16
- Issue
- 9
- Pages
- 3056-3066
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6579047
- OpenAlex
- W1612572634
- Cited by
- 587
- References
- 5
- Citations by year
- 2026: 10 · 2025: 17 · 2024: 13 · 2023: 32 · 2022: 16 · 2021: 16 · 2020: 27 · 2019: 16 · 2018: 26 · 2017: 20 · 2016: 20 · 2015: 19 · 2014: 24 · 2013: 28 · 2012: 23
- FWCI
- 9.66
- 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)
- Funders
- National Science Foundation
- Alzheimer's Association
- National Institutes of Health (5p41rr009754-09)
- National Institute of Neurological Disorders and Stroke (R01NS034994, NS-34994)
- National Center for Research Resources (1P41RR-09754)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- hippocampal ripples, sharp-wave ripples, CA1 pyramidal neurons, neuronal synchronization, field excitatory postsynaptic potentials, freely moving rats
- MeSH terms
- Animals, Efferent Pathways, Electrophysiology, Hippocampus, Nerve Net, Oscillometry, Rats, Sprague-Dawley, Entorhinal Cortex, 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