Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences
Open accessAbstract
Coding what is known and what is new: Do neural activity patterns during sleep reflect the replay of a novel experience or an invariant preexisting dynamic? Grosmark and Buzsáki observed that both familiar and novel aspects of learned information are replayed during synchronous bursts of activity in the hippocampus. Familiarity was encoded by fast-firing less-modifiable neurons that showed rate and sequence correlations that persisted into postlearning sleep. The novel features of an experience were represented by a different set of slowly firing and highly plastic cells. Science , this issue p. 1440
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Sleep replay features a less faithful recapitulation of previous experience compared with wake replay.
“Generally, sleep replay appears to feature a less faithful recapitulation of previous experience compared with wake replay.137,[154][155][156]”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [154]
The indexed passages (labeled Abstract; page unavailable) discuss replay during waking immobility and sleep, and report increased maze-related sequences from pre- to postexperience sleep. Searches for replay fidelity and wake-versus-sleep comparisons found no passage saying that sleep replay recapitulates experience less faithfully than wake replay. (LLM, conf=0.76)
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Cites
Reactivation of hippocampal ensemble memories during sleep
Wilson, M. A., & McNaughton, B. L. (1994) · Science · doi:10.1126/science.8036517 · Cited by 3,118 · 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-citationReverse 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 · 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-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-citationNeuronal Dynamics: From Single Neurons to Networks and Models of Cognition
Gerstner, W., Kistler, W. M., Naud, R., & Paninski, L. (2014) · doi:10.1017/cbo9781107447615 · Cited by 1,515 · see citing works
Memory of sequential experience in the hippocampus during slow wave sleep
Lee, A. K., & Wilson, M. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)01096-6 · Cited by 1,296 · see citing works
Hippocampal place-cell sequences depict future paths to remembered goals
Pfeiffer, B. E., & Foster, D. J. (2013) · Nature · doi:10.1038/nature12112 · Cited by 1,216 · see citing works
Forward and reverse hippocampal place-cell sequences during ripples
Diba, K., & Buzsáki, G. (2007) · Nature Neuroscience · doi:10.1038/nn1961 · Cited by 1,205 · see citing works
Self-citationReplay of neuronal firing sequences in rat hippocampus during sleep following spatial experience
Skaggs, W. E., & McNaughton, B. L. (1996) · Science · doi:10.1126/science.271.5257.1870 · Cited by 1,173 · see citing works
Harris, K. D., Henze, D. A., Csicsvari, J. L., Hirase, H., & Buzsáki, G. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.1.401 · Cited by 1,153 · see citing works
Self-citationNeuromodulation: acetylcholine and memory consolidation
Hasselmo, M. E. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(99)01365-0 · Cited by 809 · see citing works
Hippocampal 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 · cited 4× · see citing works
“First, a spatial Bayesian decoder (2), constructed from the firing-rate vectors of place cells (n = 491 cells) during track running (eight novel exploration sessions), was applied to all candidate ripple events (21) (figs.”
InfluentialThe 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
Kudrimoti, H. S., Barnes, C. A., & McNaughton, B. L. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-10-04090.1999 · Cited by 753 · see citing works
Preplay of future place cell sequences by hippocampal cellular assemblies
Dragoi, G., & Tonegawa, S. (2011) · Nature · doi:10.1038/nature09633 · Cited by 716 · see citing works
Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons
Bittner, K. C., Grienberger, C., Vaidya, S. P., Milstein, A. D., Macklin, J. J., Suh, J., Tonegawa, S., & Magee, J. C. (2015) · Nature Neuroscience · doi:10.1038/nn.4062 · Cited by 540 · see citing works
REM sleep reorganizes hippocampal excitability
Grosmark, A. D., Mizuseki, K., Pastalkova, E., Diba, K., & Buzsáki, G. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.015 · Cited by 344 · see citing works
Self-citationSelective information routing by ventral hippocampal CA1 projection neurons
Ciocchi, S., Passecker, J., Malagon‐Vina, H., Mikuš, N., & Klausberger, T. (2015) · Science · doi:10.1126/science.aaa3245 · Cited by 344 · see citing works
Hippocampal place cells construct reward related sequences through unexplored space
Ólafsdóttir, H. F., Barry, C., Saleem, A. B., Hassabis, D., & Spiers, H. J. (2015) · eLife · doi:10.7554/elife.06063 · Cited by 319 · see citing works
Preconfigured, Skewed Distribution of Firing Rates in the Hippocampus and Entorhinal Cortex
Mizuseki, K., & Buzsáki, G. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.07.039 · Cited by 319 · see citing works
Self-citationReactivation of experience-dependent cell assembly patterns in the hippocampus
O'Neill, J., Senior, T. J., Allen, K., Huxter, J. R., & Csicsvari, J. (2008) · Nature Neuroscience · doi:10.1038/nn2037 · Cited by 318 · 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
Distinct preplay of multiple novel spatial experiences in the rat
Dragoi, G., & Tonegawa, S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1306031110 · Cited by 234 · see citing works
Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons
Mizuseki, K., Royer, S., Diba, K., & Buzsáki, G. (2012) · Hippocampus · doi:10.1002/hipo.22002 · Cited by 221 · see citing works
Self-citationPlace Representation within Hippocampal Networks Is Modified by Long-Term Potentiation
Dragoi, G., Harris, K. D., & Buzsáki, G. (2003) · Neuron · doi:10.1016/s0896-6273(03)00465-3 · Cited by 215 · see citing works
Self-citationHippocampal Replay Captures the Unique Topological Structure of a Novel Environment
Wu, X., & Foster, D. J. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3414-13.2014 · Cited by 201 · see citing works
Trajectory events across hippocampal place cells require previous experience
Silva, D., Feng, T., & Foster, D. J. (2015) · Nature Neuroscience · doi:10.1038/nn.4151 · Cited by 183 · see citing works
Large environments reveal the statistical structure governing hippocampal representations
Rich, P. D., Liaw, H.-P., & Lee, A. K. (2014) · Science · doi:10.1126/science.1255635 · Cited by 177 · see citing works
Homeostatic Maintenance of Neuronal Excitability by Burst Discharges In Vivo
Buzsáki, G. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.9.893 · Cited by 108 · see citing works
Self-citationLarge-scale Recording of Neurons by Movable Silicon Probes in Behaving Rodents
Vandecasteele, M., M., S., Royer, S., Belluscio, M., Berényi, A., Diba, K., Fujisawa, S., Grosmark, A., Mao, D., Mizuseki, K., et al. (2012) · Journal of Visualized Experiments · doi:10.3791/3568 · Cited by 99 · see citing works
Self-citationAn Overview of Bayesian Methods for Neural Spike Train Analysis
Chen, Z. S. (2013) · Computational Intelligence and Neuroscience · doi:10.1155/2013/251905 · Cited by 69 · see citing works
Sloppiness in Spontaneously Active Neuronal Networks
Panas, D., Amin, H., Maccione, A., Muthmann, O., van Rossum, M. C. W., Berdondini, L., & Hennig, M. H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4421-14.2015 · Cited by 51 · see citing works
Large-scale Recording of Neurons by Movable Silicon Probes in Behaving Rodents
Vandecasteele, M., M., S., Royer, S., et al. (2012) · Journal of Visualized Experiments · doi:10.3791/3568-v · Cited by 32 · see citing works
Buzsáki, G. (2015) · Science · doi:10.1126/science.aaa6505 · Cited by 17 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- [1]O’Keefe J Nadel L The Hippocampus as a Cognitive Map Oxford Univ. Press 1978
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Active inference: a process theory
Friston, K., FitzGerald, T., Rigoli, F., Schwartenbeck, P., & Pezzulo, G. (2017) · Neural Computation · doi:10.1162/neco_a_00912 · Cited by 1,156 · see citing works
Navigating cognition: Spatial codes for human thinking
Bellmund, J. L. S., Gärdenfors, P., Moser, E. I., & Doeller, C. F. (2018) · Science · doi:10.1126/science.aat6766 · Cited by 643 · see citing works
Ultrastructural evidence for synaptic scaling across the wake/sleep cycle
de Vivo, L., Bellesi, M., Marshall, W., Bushong, E. A., Ellisman, M. H., Tononi, G., & Cirelli, C. (2017) · Science · doi:10.1126/science.aah5982 · Cited by 574 · see citing works
Human replay spontaneously reorganizes experience
Liu, Y., Dolan, R. J., Kurth-Nelson, Z., & Behrens, T. E. J. (2019) · Cell · doi:10.1016/j.cell.2019.06.012 · Cited by 497 · see citing works
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 · 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
Foster, D. J. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031538 · Cited by 375 · 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
Sleep—A brain-state serving systems memory consolidation
Brodt, S., Inostroza, M., Niethard, N., & Born, J. (2023) · Neuron · doi:10.1016/j.neuron.2023.03.005 · Cited by 343 · see citing works
CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus
Soltesz, I., & Losonczy, A. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0118-0 · Cited by 333 · 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
Cortical circuit activity underlying sleep slow oscillations and spindles
Niethard, N., Ngo, H.-V. V., Ehrlich, I., & Born, J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1805517115 · Cited by 245 · see citing works
Functional and structural underpinnings of neuronal assembly formation in learning
Holtmaat, A., & Caroni, P. (2016) · Nature Neuroscience · doi:10.1038/nn.4418 · Cited by 239 · see citing works
Hippocampal-prefrontal reactivation during learning is stronger in awake compared with sleep states
Tang, W., Shin, J. D., Frank, L. M., & Jadhav, S. P. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2291-17.2017 · Cited by 160 · see citing works
Superficial layers of the medial entorhinal cortex replay independently of the hippocampus
O’Neill, J., Boccara, C. N., Stella, F., Schoenenberger, P., & Csicsvari, J. (2017) · Science · doi:10.1126/science.aag2787 · Cited by 177 · see citing works
Spatial goal coding in the hippocampal formation
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Emergence of preconfigured and plastic time-compressed sequences in early postnatal development
Farooq, U., & Dragoi, G. (2019) · Science · doi:10.1126/science.aav0502 · Cited by 131 · see citing works
Hippocampal reactivation of random trajectories resembling brownian diffusion
Stella, F., Baracskay, P., O’Neill, J., & Csicsvari, J. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.052 · Cited by 107 · see citing works
Reward revaluation biases hippocampal replay content away from the preferred outcome
Carey, A. A., Tanaka, Y., & van der Meer, M. A. A. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0464-6 · Cited by 106 · see citing works
Hippocampal reactivation extends for several hours following novel experience
Giri, B., Miyawaki, H., Mizuseki, K., Cheng, S., & Diba, K. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.1950-18.2018 · Cited by 99 · see citing works
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Self-citationHippocampo-cortical circuits for selective memory encoding, routing, and replay
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Plasticity during sleep is linked to specific regulation of cortical circuit activity
Niethard, N., Burgalossi, A., & Born, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00065 · Cited by 89 · see citing works
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Self-citationHippocampal replay of experience at real-world speeds
Denovellis, E. L., Gillespie, A. K., Coulter, M. E., Sosa, M., Chung, J. E., Eden, U. T., & Frank, L. M. (2021) · eLife · doi:10.7554/elife.64505 · Cited by 89 · see citing works
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Grosmark, A. D., Sparks, F. T., Davis, M. J., & Losonczy, A. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00920-7 · Cited by 71 · see citing works
Self-citationTanni, S., de Cothi, W., & Barry, C. (2022) · Current Biology · doi:10.1016/j.cub.2022.06.046 · Cited by 37 · see citing works
Eckert, M. J., McNaughton, B. L., & Tatsuno, M. (2020) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2019.0655 · Cited by 34 · see citing works
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The two tales of hippocampal sharp-wave ripple content: The rigid and the plastic
Hall, A. F., & Wang, D. V. (2023) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102396 · Cited by 23 · see citing works
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Ohki, T., & Takei, Y. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13844 · Cited by 20 · see citing works
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- Authors
- Grosmark, A. D., & Buzsáki, G.
- Affiliations
- Columbia University Irving Medical Center (US)
- New York University (US)
- Corresponding author
- Buzsáki, György
- Venue
- Science
- Published
- 2016-03-25
- Volume
- 351
- Issue
- 6280
- Pages
- 1440-1443
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC4919122
- OpenAlex
- W2310925872
- Cited by
- 367
- References
- 35
- Citations by year
- 2026: 18 · 2025: 45 · 2024: 42 · 2023: 47 · 2022: 28 · 2021: 34 · 2020: 34 · 2019: 50 · 2018: 27 · 2017: 32 · 2016: 10
- FWCI
- 24.99
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DANDI Archive (cc-by)
- Funders
- NIH (NS075015, MH54671, MH102840)
- Simons Foundation
- G. Harold and Leila Y. Mathers Foundation
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- hippocampal ripples, place cells, memory consolidation, episodic memory, neuronal firing dynamics, pyramidal neurons, neuroplasticity, burst firing, spatial specificity
- MeSH terms
- Action Potentials, Animals, Hippocampus, Learning, Male, Neuronal Plasticity, Sleep, Pyramidal Cells, Maze Learning, Rats, Inbred LEC, Rats
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