Grid cell co-activity patterns during sleep reflect spatial overlap of grid fields during active behaviors
Open accessPublished version of a preprint
Abstract
Continuous-attractor network models of grid formation posit that recurrent connectivity between grid cells controls their patterns of co-activation. Grid cells from a common module exhibit stable offsets in their periodic spatial tuning curves across environments, and this may reflect recurrent connectivity or correlated sensory inputs. Here we explore whether cell–cell relationships predicted by attractor models persist during sleep states in which spatially informative sensory inputs are absent. We recorded ensembles of grid cells in superficial layers of medial entorhinal cortex during active exploratory behaviors and overnight sleep. Per grid cell pair and collectively, and across waking, rapid eye movement sleep and non-rapid eye movement sleep, we found preserved patterns of spike-time correlations that reflected the spatial tuning offsets between these grid cells during active exploration. The preservation of cell–cell relationships across waking and sleep states was not explained by theta oscillations or activity in hippocampal subregion CA1. These results indicate that recurrent connectivity within the grid cell network drives grid cell activity across behavioral states. How grid cells’ geometric firing patterns arise remains unknown. This study shows preserved grid cell co-activity patterns across sleep that reflect grid field overlap during waking, suggesting that grid firing emerges from specific connectivity patterns.
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
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.
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?
There is evidence for hippocampus-independent replay in extrahippocampal sites, e.g., in superficial layers of medial entorhinal cortex and prefrontal cortex.
“There is, however, also evi-dence for hippocampus-independent replay in extrahippocampal sites, e.g., in superficial layers of medial entorhinal cortex and in prefrontal cortex.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [93]
The Discussion reports that superficial-layer medial entorhinal grid cells rarely reactivate in coordination with hippocampal place cells, and the References identify a study of replay independent of the hippocampus in those layers. For medial prefrontal cortex, however, the Discussion describes activity correlated with hippocampal activity during replay, not hippocampus-independent replay. No page numbers are provided in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat
O'Keefe, J., & Dostrovsky, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90358-1 · Cited by 6,151 · see citing works
Microstructure of a spatial map in the entorhinal cortex
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. (2005) · Nature · doi:10.1038/nature03721 · Cited by 4,068 · see citing works
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
Dynamics of pattern formation in lateral-inhibition type neural fields
Амари, Ш.-И. (1977) · Biological Cybernetics · doi:10.1007/bf00337259 · Cited by 2,086 · see citing works
Path integration and the neural basis of the 'cognitive map'
McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., & Moser, M.-B. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1932 · Cited by 2,024 · see citing works
Taube, J., Muller, R., & Ranck, J. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00420.1990 · Cited by 1,809 · see citing works
Coordinated memory replay in the visual cortex and hippocampus during sleep
Ji, D., & Wilson, M. A. (2007) · Nature Neuroscience · doi:10.1038/nn1825 · Cited by 1,669 · see citing works
Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex
Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B. L., Witter, M. P., Moser, M.-B., & Moser, E. I. (2006) · Science · doi:10.1126/science.1125572 · Cited by 1,485 · see citing works
Frequency of gamma oscillations routes flow of information in the hippocampus
Colgin, L. L., Denninger, T., Fyhn, M., Hafting, T., Bonnevie, T., Jensen, O. B., Moser, M., & Moser, E. I. (2009) · Nature · doi:10.1038/nature08573 · Cited by 1,425 · see citing works
Self-citationMemory 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
Representation of Geometric Borders in the Entorhinal Cortex
Solstad, T., Boccara, C. N., Kropff, E., Moser, M.-B., & Moser, E. I. (2008) · Science · doi:10.1126/science.1166466 · Cited by 1,213 · see citing works
Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep
Louie, K., & Wilson, M. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00186-6 · Cited by 1,148 · 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
Replay 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
Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans
Tallon‐Baudry, C., Bertrand, O., Delpuech, C., & Pernier, J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-02-00722.1997 · Cited by 926 · see citing works
Hippocampal sharp waves: Their origin and significance
Buzsáki, G. (1986) · Brain Research · doi:10.1016/0006-8993(86)91483-6 · Cited by 925 · see citing works
Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat
Steward, O., & Scoville, S. A. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901690306 · Cited by 837 · see citing works
Accurate Path Integration in Continuous Attractor Network Models of Grid Cells
Burak, Y., & Fiete, I. R. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000291 · Cited by 779 · see citing works
Self-citationMapping of a non-spatial dimension by the hippocampal-entorhinal circuit
Aronov, D., Nevers, R., & Tank, D. W. (2017) · Nature · doi:10.1038/nature21692 · Cited by 773 · see citing works
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 · 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
Hippocampal remapping and grid realignment in entorhinal cortex
Fyhn, M., Hafting, T., Treves, A., Moser, M.-B., & Moser, E. I. (2007) · Nature · doi:10.1038/nature05601 · Cited by 749 · see citing works
An oscillatory interference model of grid cell firing
Burgess, N., Barry, C., & O'Keefe, J. M. (2007) · Hippocampus · doi:10.1002/hipo.20327 · Cited by 688 · see citing works
Speed cells in the medial entorhinal cortex
Kropff, E., Carmichael, J. E., Moser, M.-B., & Moser, E. I. (2015) · Nature · doi:10.1038/nature14622 · Cited by 668 · see citing works
A Spin Glass Model of Path Integration in Rat Medial Entorhinal Cortex
Fuhs, M. C., & Touretzky, D. S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4353-05.2006 · Cited by 628 · see citing works
Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep
Euston, D. R., Tatsuno, M., & McNaughton, B. L. (2007) · Science · doi:10.1126/science.1148979 · Cited by 586 · see citing works
Gothard, K., Skaggs, W. E., Moore, K. L., & McNaughton, B. L. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-02-00823.1996 · Cited by 488 · see citing works
A map of visual space in the primate entorhinal cortex
Killian, N. J., Jutras, M. J., & Buffalo, E. A. (2012) · Nature · doi:10.1038/nature11587 · Cited by 471 · see citing works
Hippocampus-independent phase precession in entorhinal grid cells
Hafting, T., Fyhn, M., Bonnevie, T., Moser, M., & Moser, E. I. (2008) · Nature · doi:10.1038/nature06957 · Cited by 471 · see citing works
Understanding memory through hippocampal remapping
Colgin, L. L., Moser, E. I., & Moser, M.-B. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.06.008 · Cited by 450 · see citing works
Self-citationWhat Does the Anatomical Organization of the Entorhinal Cortex Tell Us?
Canto, C. B., Wouterlood, F. G., & Witter, M. P. (2008) · Neural Plasticity · doi:10.1155/2008/381243 · Cited by 418 · see citing works
Recurrent inhibitory circuitry as a mechanism for grid formation
Couey, J. J., Witoelar, A., Zhang, S., Zheng, K., Ye, J., Dunn, B. A., Czajkowski, R., Moser, M., Moser, E. I., Roudi, Y., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3310 · Cited by 413 · see citing works
Representation of Three-Dimensional Space in the Hippocampus of Flying Bats
Yartsev, M. M., & Ulanovsky, N. (2013) · Science · doi:10.1126/science.1235338 · Cited by 403 · see citing works
Temporal Interaction between Single Spikes and Complex Spike Bursts in Hippocampal Pyramidal Cells
Harris, K. D., Hirase, H., Leinekugel, X., Henze, D. A., & Buzsáki, G. (2001) · Neuron · doi:10.1016/s0896-6273(01)00447-0 · Cited by 388 · 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
Impaired Spatial Representation in CA1 after Lesion of Direct Input from Entorhinal Cortex
Brun, V. H., Leutgeb, S., Wu, H., Schwarcz, R. M., Witter, M. P., Moser, E. I., & Moser, M. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.034 · Cited by 364 · see citing works
Grid cells require excitatory drive from the hippocampus
Bonnevie, T., Dunn, B. A., Fyhn, M., Hafting, T., Derdikman, D., Kubie, J. L., Roudi, Y., Moser, E. I., & Moser, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3311 · Cited by 341 · see citing works
Grid cells and cortical representation
Moser, E. I., Roudi, Y., Witter, M. P., Kentros, C., Bonhoeffer, T., & Moser, M.-B. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3766 · Cited by 335 · see citing works
Reactivation 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
A Multiplexed, Heterogeneous, and Adaptive Code for Navigation in Medial Entorhinal Cortex
Hardcastle, K., Maheswaranathan, N., Ganguli, S., & Giocomo, L. M. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.025 · Cited by 312 · see citing works
Generation of theta rhythm in medial entorhinal cortex of freely moving rats
Mitchell, S. J., & Ranck, J. B. (1980) · Brain Research · doi:10.1016/0006-8993(80)90006-2 · Cited by 299 · see citing works
Specific evidence of low-dimensional continuous attractor dynamics in grid cells
Yoon, K., Buice, M. A., Barry, C., Hayman, R., Burgess, N., & Fiete, I. R. (2013) · Nature Neuroscience · doi:10.1038/nn.3450 · Cited by 296 · see citing works
Self-citationDuring Running in Place, Grid Cells Integrate Elapsed Time and Distance Run
Kraus, B. J., Brandon, M. P., Robinson, R. J., Connerney, M. A., Hasselmo, M. E., & Eichenbaum, H. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.031 · Cited by 286 · see citing works
Feedback Inhibition Enables Theta-Nested Gamma Oscillations and Grid Firing Fields
Pastoll, H., Solanka, L., van Rossum, M. C. W., & Nolan, M. F. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.032 · Cited by 278 · see citing works
Internally organized mechanisms of the head direction sense
Peyrache, A., Lacroix, M. M., Petersen, P. C., & Buzsáki, G. (2015) · Nature Neuroscience · doi:10.1038/nn.3968 · Cited by 274 · see citing works
Hippocampal place cell assemblies are speed-controlled oscillators
Geisler, C. E., Robbe, D., Zugaro, M., Sirota, A., & Buzsáki, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610121104 · Cited by 273 · see citing works
Spatial Representation along the Proximodistal Axis of CA1
Henriksen, E. J., Colgin, L. L., Barnes, C. A., Witter, M. P., Moser, M., & Moser, E. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.042 · Cited by 260 · see citing works
Self-citationOptogenetic Dissection of Entorhinal-Hippocampal Functional Connectivity
Zhang, S., Ye, J., Miao, C., Tsao, A., Cerniauskas, I., Ledergerber, D., Moser, M., & Moser, E. I. (2013) · Science · doi:10.1126/science.1232627 · Cited by 251 · see citing works
Jadhav, S. P., Rothschild, G., Roumis, D. K., & Frank, L. M. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.010 · Cited by 250 · see citing works
Local and Distant Input Controlling Excitation in Layer II of the Medial Entorhinal Cortex
Fuchs, E. C., Neitz, A., Pinna, R., Melzer, S., Caputi, A., & Monyer, H. (2015) · Neuron · doi:10.1016/j.neuron.2015.11.029 · Cited by 179 · 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
Dordek, Y., Soudry, D., Meir, R., & Derdikman, D. (2016) · eLife · doi:10.7554/elife.10094 · Cited by 175 · see citing works
Coordinated grid and place cell replay during rest
Ólafsdóttir, H. F., Carpenter, F., & Barry, C. (2016) · Nature Neuroscience · doi:10.1038/nn.4291 · Cited by 175 · see citing works
Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro
Dhillon, A., & Jones, R. S. G. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00225-6 · Cited by 171 · see citing works
Grid Cells Use HCN1 Channels for Spatial Scaling
Giocomo, L. M., Hussaini, S. A., Fan, Z., Kandel, E. R., Moser, M., & Moser, E. I. (2011) · Cell · doi:10.1016/j.cell.2011.08.051 · Cited by 158 · see citing works
Navratilova, Z., Giocomo, L. M., Fellous, J., Hasselmo, M. E., & McNaughton, B. L. (2011) · Hippocampus · doi:10.1002/hipo.20939 · Cited by 156 · see citing works
A Map-like Micro-Organization of Grid Cells in the Medial Entorhinal Cortex
Gu, Y., Lewallen, S., Kinkhabwala, A. A., Domnisoru, C., Yoon, K., Gauthier, J. L., Fiete, I., & Tank, D. W. (2018) · Cell · doi:10.1016/j.cell.2018.08.066 · Cited by 134 · see citing works
Self-citationGrid cells: The position code, neural network models of activity, and the problem of learning
Welinder, P., Burak, Y., & Fiete, I. (2008) · Hippocampus · doi:10.1002/hipo.20519 · Cited by 88 · see citing works
Self-citationGrid Cell Responses in 1D Environments Assessed as Slices through a 2D Lattice
Yoon, K., Lewallen, S., Kinkhabwala, A. A., Tank, D. W., & Fiete, I. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.039 · Cited by 81 · see citing works
Self-citationZheng, C., Bieri, K. W., Trettel, S. G., & Colgin, L. L. (2015) · Hippocampus · doi:10.1002/hipo.22415 · Cited by 75 · see citing works
Self-citationGrossberg, S., & Pilly, P. K. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002648 · Cited by 55 · see citing works
Do We Understand the Emergent Dynamics of Grid Cell Activity?: Figure 1.
Burak, Y., & Fiete, I. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2857-06.2006 · Cited by 50 · see citing works
Self-citationReconstruction of the postsubiculum head direction signal from neural ensembles
Johnson, A. C., Seeland, K. D., & Redish, A. D. (2004) · Hippocampus · doi:10.1002/hipo.20033 · Cited by 43 · see citing works
A Model of Grid Cells Based on a Path Integration Mechanism
Guanella, A., & Verschure, P. F. M. J. (2006) · Lecture notes in computer science · doi:10.1007/11840817_77 · Cited by 28 · see citing works
Head direction cells in the postsubiculum do not show replay of prior waking sequences during sleep
Brandon, M. P., Bogaard, A. R., Andrews, C. M., & Hasselmo, M. E. (2011) · Hippocampus · doi:10.1002/hipo.20924 · Cited by 26 · see citing works
Inferring circuit mechanisms from sparse neural recording and global perturbation in grid cells
Widloski, J., Marder, M. P., & Fiete, I. (2018) · eLife · doi:10.7554/elife.33503 · Cited by 21 · see citing works
Self-citationMethodological Caveats in the Detection of Coordinated Replay between Place Cells and Grid Cells
Trimper, J. B., Trettel, S. G., Hwaun, E., & Colgin, L. L. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00057 · Cited by 20 · see citing works
Self-citationCortical microcircuit determination through global perturbation and sparse sampling in grid cellsPreprint
Widloski, J., & Fiete, I. (2015) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/019224 · Cited by 4 · see citing works
Self-citationSmith, H. J. (2013) · Science · doi:10.1126/science.340.6129.123-a · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Perineuronal nets stabilize the grid cell network
Christensen, A. C., Lensjø, K. K., Lepperød, M. E., Dragly, S.-A., Sutterud, H., Blackstad, J. S., Fyhn, M., & Hafting, T. (2021) · Nature Communications · doi:10.1038/s41467-020-20241-w · Cited by 1,865 · see citing works
Toroidal topology of population activity in grid cells
Gardner, R. J., Hermansen, E., Pachitariu, M., Burak, Y., Baas, N. A., Dunn, B. A., Moser, M.-B., & Moser, E. I. (2022) · Nature · doi:10.1038/s41586-021-04268-7 · Cited by 428 · see citing works
Object-vector coding in the medial entorhinal cortex
Høydal, Ø. A., Skytøen, E. R., Andersson, S. O., Moser, M.-B., & Moser, E. I. (2019) · Nature · doi:10.1038/s41586-019-1077-7 · Cited by 366 · 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
A neural-level model of spatial memory and imagery
Bicanski, A., & Burgess, N. (2018) · eLife · doi:10.7554/elife.33752 · Cited by 230 · see citing works
A structured scaffold underlies activity in the hippocampus
Mulders, D., Yim, M. Y., Lee, J. S., Lee, A. K., Taillefumier, T., & Fiete, I. R. (2021) · doi:10.1101/2021.11.20.469406 · Cited by 11 · see citing works
Self-citation
- Authors
- Trettel, S. G., Trimper, J. B., Hwaun, E., Fiete, I. R., & Colgin, L. L.
- Affiliations
- Brown University (US)
- The University of Texas at Austin (US)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Trettel, Sean G.
- Trimper, John B.
- Colgin, Laura Lee
- Venue
- Nature Neuroscience
- Published
- 2019-03-25
- Volume
- 22
- Issue
- 4
- Pages
- 609-617
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC7412059
- OpenAlex
- W2951002351
- Semantic Scholar
- 41426d063e66b8b89ca4a123bde1b219158fb45b
- Cited by
- 108
- References
- 69
- Citations by year
- 2026: 8 · 2025: 23 · 2024: 15 · 2023: 12 · 2022: 10 · 2021: 12 · 2020: 12 · 2019: 11 · 2018: 4 · 2017: 1
- FWCI
- 6.54
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- cc-by-nc-nd
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation (1453756, CAREER)
- Howard Hughes Medical Institute
- Simons Foundation
- Whitehall Foundation
- National Institutes of Health
- Office of Naval Research (N00014, N00014-14-1-0322)
- National Institute of Mental Health (T32MH106454)
- National Institute on Drug Abuse (T32DA018926)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- grid cells, sleep, continuous attractor networks, recurrent connectivity, medial entorhinal cortex, REM sleep, NREM sleep, theta oscillations, hippocampal CA1, spatial navigation
- MeSH terms
- Grid Cells, Action Potentials, Animals, Exploratory Behavior, Male, Models, Neurological, Motor Activity, Sleep, Entorhinal Cortex, Rats, Long-Evans, CA1 Region, Hippocampal, Spatial Processing
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
