The DOI matches its Crossref record; 15 of the 15 references it cites were found in a registry or an index.
Pyramidal Cell-Interneuron Interactions Underlie Hippocampal Ripple Oscillations
Open accessAbstract
SUMMARY High-frequency ripple oscillations, observed most prominently in the hippocampal CA1 pyramidal layer, are associated with memory consolidation. The cellular and network mechanisms underlying the generation, frequency control, and spatial coherence of the rhythm are poorly understood. Using multisite optogenetic manipulations in freely behaving rodents, we found that depolarization of a small group of nearby pyramidal cells was sufficient to induce high-frequency oscillations, whereas closed-loop silencing of pyramidal cells or activation of parvalbumin-(PV) or somatostatin-immunoreactive interneurons aborted spontaneously occurring ripples. Focal pharmacological blockade of GABAA receptors abolished ripples. Localized PV inter-neuron activation paced ensemble spiking, and simultaneous induction of high-frequency oscillations at multiple locations resulted in a temporally coherent pattern mediated by phase-locked inter-neuron spiking. These results constrain competing models of ripple generation and indicate that temporally precise local interactions between excitatory and inhibitory neurons support ripple generation in the intact hippocampus.
Overview
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
Verification
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.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991) · The Anatomical Record · doi:10.1002/ar.1092310411 · Cited by 2,994 · cited 1×
“Assuming a brain refractive index nout = 1.36 (Binding et al., 2011) and CA1 neuronal density of 105 mm 3 (West et al., 1991), the disk spans up to V = 10 3 mm3 and contains 1–100 somata (depending on h), which may consist of about 80 PYR and 20 INT.”
BackgroundInfluentialReverse replay of behavioural sequences in hippocampal place cells during the awake state
Foster, D. J., & Wilson, M. A. (2006) · Nature · doi:10.1038/nature04587 · Cited by 1,727
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
Self-citationWhittington, M. A., Traub, R. D., & Jefferys, J. G. R. (1995) · Nature · doi:10.1038/373612a0 · Cited by 1,613
Selective 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
Self-citationBrain-state- and cell-type-specific firing of hippocampal interneurons in vivo
Klausberger, T., Magill, P. J., Márton, L. F., Roberts, J. D. B., Cobden, P. M., Buzsáki, G., & Somogyi, P. (2003) · Nature · doi:10.1038/nature01374 · Cited by 1,345
Self-citationForward and reverse hippocampal place-cell sequences during ripples
Diba, K., & Buzsáki, G. (2007) · Nature Neuroscience · doi:10.1038/nn1961 · Cited by 1,205
Self-citationOscillatory 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
Self-citationAwake hippocampal sharp-wave ripples support spatial memory
Jadhav, S. P., Kemere, C., German, P. W., & Frank, L. M. (2012) · Science · doi:10.1126/science.1217230 · Cited by 924
Awake replay of remote experiences in the hippocampus
Karlsson, M. P., & Frank, L. M. (2009) · Nature Neuroscience · doi:10.1038/nn.2344 · Cited by 769 · cited 4×
“The neuronal sequence is often similar to place cell sequences observed during exploration (Foster and Wilson, 2006; Diba and Buzsáki, 2007; Karlsson and Frank, 2009).”
BackgroundInfluential
Research works printed but not linked: 45
- Bähner, 2011, Cellular correlate of assembly formation in oscillating hippocampal networks in vitro, Proc. Natl. Acad. Sci. USA, 108, E607, 10.1073/pnas.1103546108 · DOI
- Binding, 2011, Brain refractive index measured in vivo with high-NA defocus-corrected full-field OCT and consequences for two-photon microscopy, Opt. Express, 19, 4833, 10.1364/OE.19.004833 · DOI · Paper page
- Bragin, 1999, Hippocampal and entorhinal cortex high-frequency oscillations (100--500 Hz) in human epileptic brain and in kainic acid—treated rats with chronic seizures, Epilepsia, 40, 127, 10.1111/j.1528-1157.1999.tb02065.x · DOI · Paper page
- Brunel, 1999, Fast global oscillations in networks of integrate-and-fire neurons with low firing rates, Neural Comput., 11, 1621, 10.1162/089976699300016179 · DOI · Paper page
- Brunel, 2003, What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance, J. Neurophysiol., 90, 415, 10.1152/jn.01095.2002 · DOI · Paper page
- Buhl, 2003, Selective impairment of hippocampal gamma oscillations in connexin-36 knock-out mouse in vivo, J. Neurosci., 23, 1013, 10.1523/JNEUROSCI.23-03-01013.2003 · DOI · Paper page
- Buzsáki, 1986, Hippocampal sharp waves: their origin and significance, Brain Res., 398, 242, 10.1016/0006-8993(86)91483-6 · DOI · Paper page
- Buzsáki, 2012, High frequency oscillations in the intact brain, Prog. Neurobiol., 98, 241, 10.1016/j.pneurobio.2012.02.004 · DOI · Paper page
- Buzsáki, 1983, Cellular bases of hippocampal EEG in the behaving rat, Brain Res., 287, 139, 10.1016/0165-0173(83)90037-1 · DOI · Paper page
- Buzsáki, 1992, High-frequency network oscillation in the hippocampus, Science, 256, 1025, 10.1126/science.1589772 · DOI · Paper page
- Chiovini, 2014, Dendritic spikes induce ripples in parvalbumin interneurons during hippocampal sharp waves, Neuron, 82, 908, 10.1016/j.neuron.2014.04.004 · DOI
- Chrobak, 1996, High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat, J. Neurosci., 16, 3056, 10.1523/JNEUROSCI.16-09-03056.1996 · DOI · Paper page
- Csicsvari, 2000, Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events, Neuron, 28, 585, 10.1016/S0896-6273(00)00135-5 · DOI · Paper page
- Geisler, 2005, Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges, J. Neurophysiol., 94, 4344, 10.1152/jn.00510.2004 · DOI · Paper page
- Gibson, 1999, Two networks of electrically coupled inhibitory neurons in neocortex, Nature, 402, 75, 10.1038/47035 · DOI · Paper page
- Grenier, 2001, Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates, J. Neurophysiol., 86, 1884, 10.1152/jn.2001.86.4.1884 · DOI · Paper page
- Hájos, 2013, Input-output features of anatomically identified CA3 neurons during hippocampal sharp wave/ripple oscillation in vitro, J. Neurosci., 33, 11677, 10.1523/JNEUROSCI.5729-12.2013 · DOI
- Kandel, 1997, Cellular-synaptic generation of sleep spindles, spike-and-wave discharges, and evoked thalamocortical responses in the neocortex of the rat, J. Neurosci., 17, 6783, 10.1523/JNEUROSCI.17-17-06783.1997 · DOI · Paper page
- Karlócai, 2014, Physiological sharp wave-ripples and interictal events in vitro: what’s the difference?, Brain, 137, 463, 10.1093/brain/awt348 · DOI
- Klausberger, 2008, Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations, Science, 321, 53, 10.1126/science.1149381 · DOI · Paper page
- Le Van Quyen, 2008, Cell type-specific firing during ripple oscillations in the hippocampal formation of humans, J. Neurosci., 28, 6104, 10.1523/JNEUROSCI.0437-08.2008 · DOI · Paper page
- Lin, 2009, Characterization of engineered channelrhodopsin variants with improved properties and kinetics, Biophys. J., 96, 1803, 10.1016/j.bpj.2008.11.034 · DOI · Paper page
- Maier, 2003, Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices, J. Physiol., 550, 873, 10.1113/jphysiol.2003.044602 · DOI · Paper page
- Memmesheimer, 2010, Quantitative prediction of intermittent high-frequency oscillations in neural networks with supralinear dendritic interactions, Proc. Natl. Acad. Sci. USA, 107, 11092, 10.1073/pnas.0909615107 · DOI
- Mizuseki, 2011, Hippocampal CA1 pyramidal cells form functionally distinct sublayers, Nat. Neurosci., 14, 1174, 10.1038/nn.2894 · DOI · Paper page
- Nguyen, 2009, Characterizing the dynamic frequency structure of fast oscillations in the rodent hippocampus, Front. Integr. Neurosci., 3, 11, 10.3389/neuro.07.011.2009 · DOI
- Nimmrich, 2005, Induced sharp wave-ripple complexes in the absence of synaptic inhibition in mouse hippocampal slices, J. Physiol., 563, 663, 10.1113/jphysiol.2004.079558 · DOI
- Pais, 2003, Sharp wave-like activity in the hippocampus in vitro in mice lacking the gap junction protein connexin 36, J. Neurophysiol., 89, 2046, 10.1152/jn.00549.2002 · DOI
- Patel, 2013, Local generation and propagation of ripples along the septotemporal axis of the hippocampus, J. Neurosci., 33, 17029, 10.1523/JNEUROSCI.2036-13.2013 · DOI · Paper page
- Ponomarenko, 2004, Multiple GABAA receptor subtypes regulate hippocampal ripple oscillations, Eur. J. Neurosci., 20, 2141, 10.1111/j.1460-9568.2004.03685.x · DOI
- Rácz, 2009, Augmented hippocampal ripple oscillations in mice with reduced fast excitation onto parvalbumin-positive cells, J. Neurosci., 29, 2563, 10.1523/JNEUROSCI.5036-08.2009 · DOI
- Schmitz, 2001, Axo-axonal coupling. a novel mechanism for ultrafast neuronal communication, Neuron, 31, 831, 10.1016/S0896-6273(01)00410-X · DOI · Paper page
- Schomburg, 2012, The spiking component of oscillatory extracellular potentials in the rat hippocampus, J. Neurosci., 32, 11798, 10.1523/JNEUROSCI.0656-12.2012 · DOI · Paper page
- Stark, 2012, Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals, J. Neurophysiol., 108, 349, 10.1152/jn.00153.2012 · DOI
- Stark, 2013, Inhibition-induced theta resonance in cortical circuits, Neuron, 80, 1263, 10.1016/j.neuron.2013.09.033 · DOI · Paper page
- Sullivan, 2011, Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity, J. Neurosci., 31, 8605, 10.1523/JNEUROSCI.0294-11.2011 · DOI · Paper page
- Taxidis, 2012, Modeling sharp wave-ripple complexes through a CA3-CA1 network model with chemical synapses, Hippocampus, 22, 995, 10.1002/hipo.20930 · DOI
- Traub, 2000, A model of high-frequency ripples in the hippocampus based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons, J. Neurosci., 20, 2086, 10.1523/JNEUROSCI.20-06-02086.2000 · DOI
- Traub, 1996, A mechanism for generation of long-range synchronous fast oscillations in the cortex, Nature, 383, 621, 10.1038/383621a0 · DOI · Paper page
- Traub, 2003, GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations, Proc. Natl. Acad. Sci. USA, 100, 11047, 10.1073/pnas.1934854100 · DOI · Paper page
- Traub, 2012, Axonal properties determine somatic firing in a model of in vitro CA1 hippocampal sharp wave/ripples and persistent gamma oscillations, Eur. J. Neurosci., 36, 2650, 10.1111/j.1460-9568.2012.08184.x · DOI
- Viereckel, 2013, Effects of the GABA-uptake blocker NNC-711 on spontaneous sharp wave-ripple complexes in mouse hippocampal slices, Hippocampus, 23, 323, 10.1002/hipo.22104 · DOI
- Wilson, 1994, Reactivation of hippocampal ensemble memories during sleep, Science, 265, 676, 10.1126/science.8036517 · DOI · Paper page
- Wong, 1983, Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region, J. Neurophysiol., 49, 442, 10.1152/jn.1983.49.2.442 · DOI · Paper page
- Ylinen, 1995, Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms, J. Neurosci., 15, 30, 10.1523/JNEUROSCI.15-01-00030.1995 · DOI · Paper page
Cited by
GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits
Tremblay, R., Lee, S., & Rudy, B. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.033 · Cited by 2,033
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
Self-citationHippocampal GABAergic Inhibitory Interneurons
Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889
Long-duration hippocampal sharp wave ripples improve memory
Fernández-Ruiz, A., Oliva, A., Fermino de Oliveira, E., Rocha-Almeida, F., Tingley, D., & Buzsáki, G. (2019) · Science · doi:10.1126/science.aax0758 · Cited by 490
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
Metadata
- Authors
- Stark, E., Roux, L., Eichler, R., Senzai, Y., Royer, S., & Buzsáki, G.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2014-07
- Volume
- 83
- Issue
- 2
- Pages
- 467-480
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2046999866
- Cited by
- 450
- References
- 15
- FWCI
- 16.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 465 d)
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
How to cite
Cite CoChat for the checks on this page, and the paper for its own findings.
- This page
- CoChat. (2026). Citation check: Pyramidal Cell-Interneuron Interactions Underlie Hippocampal Ripple Oscillations. https://app.cochat.ai/papers/10.1016/j.neuron.2014.06.023
- The paper
- Stark, E., Roux, L., Eichler, R., Senzai, Y., Royer, S., & Buzsáki, G. (2014). Pyramidal Cell-Interneuron Interactions Underlie Hippocampal Ripple Oscillations. Neuron. https://doi.org/10.1016/j.neuron.2014.06.023
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.