Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience
Abstract
Patterns of neuronal activity recorded in CA1 of the hippocampus and in neocortex during waking-behavior, are reactivated during subsequent slow-wave sleep (SWS). It has been suggested that this reactivation may originate in the hippocampal CA3 region, where modifiable excitatory recurrent connections are abundant and where sharp-waves in which the reactivation is most robust, appear to arise. The present experiment investigated whether ensemble firing patterns of granule cells in the fascia dentata (FD), an area 'upstream' from CA3, are also reactivated during sleep. Populations of FD granule cells were recorded from during spatial behavior and during prior and subsequent SWS. firing rate correlations between cell-pairs with overlapping place fields were significantly enhanced during post behavioral sleep compared to pre behavioral sleep. Correlations between cells with non-overlapping place fields or which were silent during maze behavior, were not changed. Thus reactivation of experience-specific correlation states also occurs in granule cells during sleep. Because these cells do not have excitatory interconnections, but form a major input to CA3 pyramidal cells, current models predicted that sleep reactivation would appear first in CA3. There are, however, both extensive polysynaptic excitatory interactions among granule cells and feedback from CA3 pyramidal cells. Granule cells also receive indirect input from neocortical regions known to undergo trace reactivation. Alth…
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?
Reactivation of firing patterns during sleep after performance on spatial tasks was obtained in the dentate gyrus.
“Reactivation of firing patterns during sleep after the performance on spatial tasks was likewise obtained in the dentate gyrus (1065).”
From About Sleep's Role in Memory (2013) · cites this paper as [1065]
Cites
Still being checked.
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
Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network
McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., Lowell, B. B., Fanselow, M. S., Wilson, M. A., & Tonegawa, S. (2007) · Science · doi:10.1126/science.1140263 · Cited by 958 · see citing works
Experience-dependent changes in cerebral activation during human REM sleep
Maquet, P., Laureys, S., Peigneux, P., Fuchs, S., Petiau, C., Phillips, C., Aerts, J., Del Fiore, G., Degueldre, C., Meulemans, T., et al. (2000) · Nature Neuroscience · doi:10.1038/77744 · Cited by 747 · see citing works
The reinterpretation of dreams: An evolutionary hypothesis of the function of dreaming
Revonsuo, A. (2000) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00004015 · Cited by 676 · 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
Ramı́rez-Amaya, V., Vazdarjanova, A. I., Mikhael, D. M., Rosi, S., Worley, P. F., & Barnes, C. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4342-04.2005 · Cited by 364 · see citing works
Self-citationSleeping brain, learning brain. The role of sleep for memory systems
Peigneux, P., Laureys, S., Delbeuck, X., & Maquet, P. (2001) · Neuroreport · doi:10.1097/00001756-200112210-00001 · Cited by 347 · see citing works
Integration of New Neurons into Functional Neural Networks
Ramı́rez-Amaya, V., Marrone, D. F., Gage, F. H., Worley, P. F., & Barnes, C. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2195-06.2006 · Cited by 332 · see citing works
Self-citationThe relationships between memory systems and sleep stages
Rauchs, G., Desgranges, B., Foret, J., & Eustache, F. (2005) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2005.00450.x · Cited by 279 · see citing works
Spatial Representations of Granule Cells and Mossy Cells of the Dentate Gyrus
GoodSmith, D., Chen, X., Wang, C., Kim, S. H., Song, H., Burgalossi, A., Christian, K. M., & Knierim, J. J. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.026 · Cited by 267 · 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
Re-evaluating Circuit Mechanisms Underlying Pattern Separation
Cayco-Gajic, N. A., & Silver, R. A. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.044 · Cited by 220 · see citing works
Senescent synapses and hippocampal circuit dynamics
Burke, S. N., & Barnes, C. A. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2009.12.003 · Cited by 199 · see citing works
Self-citationDisambiguating the similar: The dentate gyrus and pattern separation
Schmidt, B., Marrone, D. F., & Markus, E. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.08.039 · Cited by 198 · see citing works
The content of hippocampal “replay”
Pfeiffer, B. E. (2017) · Hippocampus · doi:10.1002/hipo.22824 · Cited by 172 · see citing works
Hippocampal granule cells opt for early retirement
Alme, C. B., Buzzetti, R. A., Marrone, D. F., Leutgeb, J. K., Chawla, M. K., Schaner, M. J., Bohanick, J. D., Khoboko, T., Leutgeb, S., Moser, E. I., et al. (2010) · Hippocampus · doi:10.1002/hipo.20810 · Cited by 170 · see citing works
Self-citationSpatial Firing Correlates of Physiologically Distinct Cell Types of the Rat Dentate Gyrus
Neunuebel, J. P., & Knierim, J. J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6038-11.2012 · Cited by 163 · see citing works
MEF2 negatively regulates learning-induced structural plasticity and memory formation
Cole, C. J., Mercaldo, V., Restivo, L., Yiu, A. P., Sekeres, M. J., Han, J., Vetere, G., Pekar, T., Ross, P. J., Neve, R. L., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3189 · Cited by 131 · see citing works
Luo, J., Phan, T., Yang, Y., Garelick, M. G., & Storm, D. R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5018-12.2013 · Cited by 121 · see citing works
Sequence Reactivation in the Hippocampus Is Impaired in Aged Rats
Gerrard, J. L., Burke, S. N., McNaughton, B. L., & Barnes, C. A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1265-08.2008 · Cited by 97 · see citing works
Self-citationGoodSmith, D., Lee, H., Neunuebel, J. P., Song, H., & Knierim, J. J. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0940-19.2019 · Cited by 65 · see citing works
Sustained Transcription of the Immediate Early GeneArcin the Dentate Gyrus after Spatial Exploration
Ramı́rez-Amaya, V., Angulo‐Perkins, A., Chawla, M. K., Barnes, C. A., & Rosi, S. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2916-12.2013 · Cited by 63 · see citing works
Self-citationLatent Attractors: A Model for Context-Dependent Place Representations in the Hippocampus
Doboli, S., Minai, A. A., & Best, P. J. (2000) · Neural Computation · doi:10.1162/089976600300015484 · Cited by 55 · see citing works
Off-Line Reprocessing of Recent Memory and its Role in Memory Consolidation: A Progress Report
McNaughton, B. L., Barnes, C. A., Battaglia, F. P., Bower, M. R., Cowen, S. L., Ekstrom, A. D., Gerrard, J. L., Hoffman, K. L., Houston, F. P., Karten, Y. J. G., et al. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198574002.003.0013 · Cited by 53 · see citing works
Self-citationSleep loss disrupts Arc expression in dentate gyrus neurons
Delorme, J. E., Kodoth, V., & Aton, S. J. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.04.006 · Cited by 47 · see citing works
The role of sleep in the consolidation of route learning in humans: A behavioural study
Ferrara, M., Iaria, G., Gennaro, L. D., Guariglia, C., Curcio, G., Tempesta, D., & Bertini, M. (2006) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2006.07.015 · Cited by 48 · see citing works
Neural Activity Patterns Underlying Spatial Coding in the Hippocampus
Sosa, M., Gillespie, A. K., & Frank, L. M. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_462 · Cited by 39 · see citing works
The effects of aging on dentate circuitry and function
Patrylo, P. R., & Williamson, A. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63037-4 · Cited by 38 · see citing works
Porcello, D. M., Ho, C. S., Joho, R. H., & Huguenard, J. R. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00556.2001 · Cited by 38 · see citing works
Dual Coding with STDP in a Spiking Recurrent Neural Network Model of the Hippocampus
Bush, D., Philippides, A. O., Husbands, P., & O’Shea, M. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000839 · Cited by 37 · see citing works
Reactivation of hippocampal ensemble activity patterns in the aging rat.
Gerrard, J. L., Kudrimoti, H., McNaughton, B. L., & Barnes, C. A. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.6.1180 · Cited by 35 · see citing works
Self-citationSleep talking: a viable access to mental processes during sleep
Alfonsi, V., D'Atri, A., Scarpelli, S., Mangiaruga, A., & De Gennaro, L. (2019) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2018.12.001 · Cited by 34 · see citing works
Voegtlin, T., & Verschure, P. F. M. J. (1999) · Reviews in the Neurosciences · doi:10.1515/revneuro.1999.10.3-4.291 · Cited by 31 · see citing works
Chawla, M. K., & Barnes, C. A. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63036-2 · Cited by 30 · see citing works
Self-citationHensbroek, R. A., Kamal, A., Baars, A. M., Verhage, M., & Spruijt, B. M. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00243-7 · Cited by 29 · see citing works
Dissociating the past from the present in the activity of place cells
de Hoz, L., & Wood, E. R. (2006) · Hippocampus · doi:10.1002/hipo.20207 · Cited by 26 · see citing works
Xie, M., Li, C., He, C., Li, Y., Tan, G., Yan, J. Y., Wang, J., & Hu, Z. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.10.002 · Cited by 25 · see citing works
The role of sleep disturbance and inflammation for spatial memory
Piber, D. (2021) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2021.100333 · Cited by 19 · see citing works
Encoding spatial context: a hypothesis on the function of the dentate gyrus-hilus system
Minai, A. A., & Best, P. J. (2002) · International Joint Conference on Neural Networks (IJCNN) · doi:10.1109/ijcnn.1998.682334 · Cited by 14 · see citing works
Gheidi, A., Azzopardi, E., Adams, A., & Marrone, D. F. (2013) · BMC Neuroscience · doi:10.1186/1471-2202-14-100 · Cited by 13 · see citing works
Serotonin modulates infraslow oscillation in the dentate gyrus during non-REM sleepPreprint
Turi, G. F., Teng, S., Chen, X., Lim, E. C., Dias, C., Hu, R., Wang, R., Zhen, F., & Peng, Y. (2024) · eLife · doi:10.7554/elife.100196.4 · Cited by 23 · see citing works
A connectionist model of spatial learning in the rat
Strösslin, T. (2004) · Infoscience (Ecole Polytechnique Fédérale de Lausanne) · doi:10.5075/epfl-thesis-2951 · Cited by 4 · see citing works
Lines, J., Nation, K., & Fellous, J. (2017) · Computational Intelligence and Neuroscience · doi:10.1155/2017/8091780 · Cited by 3 · see citing works
From necessity to sufficiency in memory research: when sleep helps to understand wake experiences
Lacroix, M. M., de Lavilléon, G., & Benchenane, K. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.08.009 · Cited by 2 · see citing works
Serotonin modulates infraslow oscillation in the dentate gyrus during Non-REM sleepPreprint
Turi, G. F., Teng, S., Chen, X., Lim, E. C., Dias, C., Hu, R., Wang, R., Zhen, F., & Peng, Y. (2024) · eLife · doi:10.7554/elife.100196.1 · Cited by 3 · see citing works
Memory reactivation underlies experience-dependent adaptive regulation of sleep
Yu, M., Wang, J., Zhai, Z., Huang, R., Fan, G., Xiaoya, S., Niu, Y., Zhu, H., Chen, J., Jiang, G., et al. (2026) · Science · doi:10.1126/science.aed8630 · Cited by 1 · see citing works
Chapter 4.3 Hippocampal neuronal activity and episodic memory
Wood, E. R., & de Hoz, L. (2008) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(08)00224-5 · Cited by 1 · see citing works
Mnemonic information in the rodent hippocampus during wake and sleep states
Louie, K. (2002) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 1 · see citing works
Serotonin modulates infraslow oscillation in the dentate gyrus during Non-REM sleepPreprint
Turi, G. F., Teng, S., Chen, X., Lim, E. C., Dias, C., Hu, R., Wang, R., Zhen, F., & Peng, Y. (2025) · eLife · doi:10.7554/elife.100196.2 · Cited by 1 · see citing works
The Truth About Mossy Fiber Long-Term Potentiation
Martinez, J. L., Meilandt, W. J., & Thompson, K. J. (2005) · Springer eBooks · doi:10.1007/0-387-25443-9_8
Sleep’s role in the reprocessing and restructuring of memory
Koopman, A. C. M. (2020) · ORCA Online Research @Cardiff (Cardiff University)
The Effects of Repetition and Sequence Length on Hippocampal Memory Trace Reactivation
Sutherland, G. R. (2008) · UA Campus Repository (The University of Arizona)
Serotonin modulates infraslow oscillation in the dentate gyrus during Non-REM sleepPreprint
Turi, G. F., Teng, S., Chen, X., Lim, E. C., Dias, C., Hu, R., Wang, R., Zhen, F., & Peng, Y. (2025) · eLife · doi:10.7554/elife.100196.3 · Cited by 1 · see citing works
Coordinated memory trace reactivation across distributed neural ensembles in the primate neocortex
Hoffman, K. L. (2003) · UA Campus Repository (The University of Arizona)
- Authors
- Shen, J., Kudrimoti, H., McNaughton, B., & Barnes, C.
- Affiliations
- University of Arizona (US)
- Corresponding author
- Shen, Jiemin
- McNaughton, Bruce
- Venue
- Journal of Sleep Research
- Publisher
- Wiley
- Published
- 1998-06
- Volume
- 7
- Issue
- S1
- Pages
- 6-16
- ISSN
- 0962-1105 (ISSN-L)
- 1365-2869
- OpenAlex
- W2068110865
- Cited by
- 61
- References
- 0
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 2 · 2021: 2 · 2020: 1 · 2019: 2 · 2018: 2 · 2017: 4 · 2016: 4 · 2015: 2 · 2013: 4 · 2012: 2
- FWCI
- 1.49
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Sleep Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5k05mh001227-04)
- National Institute of Mental Health (MH-01227, MH 46823)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- sleep-dependent memory consolidation, hippocampal reactivation, dentate gyrus granule cells, slow-wave sleep, place fields, spatial experience, CA3
- MeSH terms
- Animals, Behavior, Animal, Electroencephalography, Hippocampus, Male, Neurons, Sleep Stages, Spatial Behavior, Time Factors, Dentate Gyrus, 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
