Place cells in the hippocampus: Eleven maps for eleven rooms
Open accessAbstract
Significance: The hippocampus is thought to store a large number of experiences that, despite their similarity, can be individually retrieved with minimal interference. Studies have shown that place cells in hippocampal area CA3 form statistically independent representations of pairs of environments. It has remained unclear, however, whether CA3 place cells maintain this independence when the number of environments is increased. We recorded activity from CA3 in 11 environments with nearly identical geometric features. Spatial firing patterns remained uncorrelated across all 55 pairs of environments, with minimal overlap in the populations of active cells. The data suggest that the capacity of the CA3 network is large and speak against extensive recurrence of spatial motifs across experiences.
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Mammalian PCs are notable for their representational flexibility, while other spatial cells exhibit more coherent shifts across environments.
“Mammalian PCs are notable for their representational flexibility10,40,41, while other spatial cells exhibit more coherent shifts across environments42–44.”
From A population code for spatial representation in the zebrafish telencephalon (2024) · cites this paper as [41]
Remapping is thought to underlie the ability of the HPC to store multiple unique representations of similar environments or altered states of the same environment.
“Remapping is thought to underlie the ability of the HPC to store multiple unique representations of similar environments or altered states of the same environment 12 .”
From From cognitive maps to spatial schemas (2023) · cites this paper as [12]
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(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
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
The hippocampus as a cognitive map
Passingham, R. E. (1979) · Neuroscience · doi:10.1016/0306-4522(79)90015-0 · Cited by 5,128 · 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
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
Dynamics of the Hippocampal Ensemble Code for Space
Wilson, M. A., & McNaughton, B. L. (1993) · Science · doi:10.1126/science.8351520 · Cited by 2,350 · see citing works
Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus
Leutgeb, J. K., Leutgeb, S., Moser, M.-B., & Moser, E. I. (2007) · Science · doi:10.1126/science.1135801 · Cited by 1,601 · cited 2× · see citing works
“The hippocampus is thought to embody several mechanisms for preventing such interference, all ensuring that new representations overlap minimally with preexisting ones (2, 4, 5).”
BackgroundMethodSelf-citationThe effects of changes in the environment on the spatial firing of hippocampal complex-spike cells
Muller, R., & Kubie, J. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-07-01951.1987 · Cited by 1,581 · see citing works
Hippocampal synaptic enhancement and information storage within a distributed memory system
McNaughton, B. L., & Morris, R. G. M. (1987) · Trends in Neurosciences · doi:10.1016/0166-2236(87)90011-7 · Cited by 1,304 · see citing works
Computational analysis of the role of the hippocampus in memory
Treves, A., & Rolls, E. T. (1994) · Hippocampus · doi:10.1002/hipo.450040319 · Cited by 1,272 · see citing works
Self-citationGeometric determinants of the place fields of hippocampal neurons
O'Keefe, J., & Burgess, N. (1996) · Nature · doi:10.1038/381425a0 · Cited by 1,166 · see citing works
Path integration and cognitive mapping in a continuous attractor neural network model
Samsonovich, A., & McNaughton, B. L. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-15-05900.1997 · Cited by 989 · see citing works
The log-dynamic brain: how skewed distributions affect network operations
Buzsáki, G., & Mizuseki, K. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3687 · Cited by 964 · see citing works
Deciphering The Hippocampal Polyglot: the Hippocampus as a Path Integration System
McNaughton, B. L., Barnes, C. A., Gerrard, J. L., Gothard, K. M., Jung, M. W., Knierim, J. J., Kudrimoti, H. S., Qin, Y., Skaggs, W. E., Suster, M. S., et al. (1996) · Journal of Experimental Biology · doi:10.1242/jeb.199.1.173 · Cited by 900 · see citing works
Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1
Leutgeb, S., Leutgeb, J. K., Treves, A., Moser, M., & Moser, E. I. (2004) · Science · doi:10.1126/science.1100265 · Cited by 774 · see citing works
Self-citationPreplay 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
The global record of memory in hippocampal neuronal activity
Wood, E. R., Dudchenko, P. A., & Eichenbaum, H. (1999) · Nature · doi:10.1038/17605 · Cited by 707 · see citing works
Treves, A., & Rolls, E. T. (1992) · Hippocampus · doi:10.1002/hipo.450020209 · Cited by 702 · see citing works
Self-citationMarkus, E. J., Qin, Y., Leonard, B. W., Skaggs, W. E., McNaughton, B. L., & Barnes, C. A. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07079.1995 · Cited by 684 · see citing works
Experience‐dependent modifications of hippocampal place cell firing
Bostock, E., Muller, R. U., & Kubie, J. L. (1991) · Hippocampus · doi:10.1002/hipo.450010207 · Cited by 555 · see citing works
A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus
Claiborne, B. J., Amaral, D. G., & Cowan, W. M. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902460403 · Cited by 509 · 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-citationMcKenzie, S., Frank, A. J., Kinsky, N. R., Porter, B., Rivière, P. D., & Eichenbaum, H. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.019 · Cited by 373 · see citing works
Theta-paced flickering between place-cell maps in the hippocampus
Jezek, K., Henriksen, E. J., Treves, A., Moser, E. I., & Moser, M.-B. (2011) · Nature · doi:10.1038/nature10439 · Cited by 359 · see citing works
Self-citationProgressive Transformation of Hippocampal Neuronal Representations in “Morphed” Environments
Leutgeb, J. K., Leutgeb, S., Treves, A., Meyer, R. M., Barnes, C. A., McNaughton, B. L., Moser, M., & Moser, E. I. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.007 · Cited by 357 · see citing works
Self-citationThe firing of hippocampal place cells predicts the future position of freely moving rats
Muller, R., & Kubie, J. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-12-04101.1989 · Cited by 310 · see citing works
Weighting Systems for Linear Functions of Correlated Variables When There is no Dependent Variable
Wilks, S. S. (1938) · Psychometrika · doi:10.1007/bf02287917 · Cited by 275 · 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-citationLarge 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
Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus
Deguchi, Y., Donato, F., Galimberti, I., Cabuy, E., & Caroni, P. (2011) · Nature Neuroscience · doi:10.1038/nn.2768 · Cited by 157 · see citing works
McKenzie, S., Robinson, N. T. M., Herrera, L., Churchill, J. C., & Eichenbaum, H. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0879-13.2013 · Cited by 132 · see citing works
Stable and Rapid Recurrent Processing in Realistic Autoassociative Memories
Battaglia, F. P., & Treves, A. (1998) · Neural Computation · doi:10.1162/089976698300017827 · Cited by 102 · see citing works
Self-citationContext‐specific acquisition of location discrimination by hippocampal place cells
Hayman, R. M. A., Chakraborty, S., Anderson, M. I., & Jeffery, K. J. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03035.x · Cited by 88 · see citing works
Singer, A. C., Karlsson, M. P., Nathe, A. R., Carr, M. F., & Frank, L. M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0926-10.2010 · Cited by 80 · see citing works
Distinct Lineage-Dependent Structural and Functional Organization of the Hippocampus
Xu, H.-T., Han, Z., Gao, P., He, S., Li, Z., Shi, W., Kodish, O., Shao, W., Brown, K. N., Huang, K., et al. (2014) · Cell · doi:10.1016/j.cell.2014.03.067 · Cited by 80 · see citing works
Flagged first, then by citations
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Sorted by citations
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
What Learning Systems do Intelligent Agents Need? Complementary Learning Systems Theory Updated
Kumaran, D., Hassabis, D., & McClelland, J. L. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.05.004 · Cited by 736 · see citing works
Spatial representation in the hippocampal formation: a history
Moser, E. I., Moser, M.-B., & McNaughton, B. L. (2017) · Nature Neuroscience · doi:10.1038/nn.4653 · Cited by 560 · see citing works
Self-citationObject-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
Self-citationTargeted Activation of Hippocampal Place Cells Drives Memory-Guided Spatial Behavior
Robinson, N. T. M., Descamps, L. A. L., Russell, L. E., Buchholz, M. O., Bicknell, B. A., Antonov, G. K., Lau, J. Y. N., Nutbrown, R., Schmidt-Hieber, C., & Häusser, M. (2020) · Cell · doi:10.1016/j.cell.2020.09.061 · Cited by 281 · see citing works
Hippocampal remapping as hidden state inference
Sanders, H., Wilson, M. A., & Gershman, S. J. (2020) · eLife · doi:10.7554/elife.51140 · Cited by 163 · see citing works
Schema cells in the macaque hippocampus
Baraduc, P., Duhamel, J.-R., & Wirth, S. (2019) · Science · doi:10.1126/science.aav5404 · Cited by 123 · see citing works
From cognitive maps to spatial schemas
Farzanfar, D., Spiers, H. J., Moscovitch, M., & Rosenbaum, R. S. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-022-00655-9 · Cited by 115 · see citing works
George, D., Rikhye, R. V., Gothoskar, N., Guntupalli, J. S., Dedieu, A., & Lázaro-Gredilla, M. (2021) · Nature Communications · doi:10.1038/s41467-021-22559-5 · Cited by 109 · see citing works
Post-learning hippocampal replay selectively reinforces spatial memory for highly rewarded locations
Michon, F., Sun, J.-J., Kim, C. Y., Ciliberti, D., & Kloosterman, F. (2019) · Current Biology · doi:10.1016/j.cub.2019.03.048 · Cited by 86 · see citing works
Hippocampal Remapping and Its Entorhinal Origin
Latuske, P., Kornienko, O., Kohler, L., & Allen, K. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00253 · Cited by 102 · see citing works
Manipulating Hippocampal Place Cell Activity by Single-Cell Stimulation in Freely Moving Mice
Diamantaki, M., Coletta, S., Nasr, K., Zeraati, R., Laturnus, S., Berens, P., Preston-Ferrer, P., & Burgalossi, A. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.031 · Cited by 85 · see citing works
How the Brain’s Navigation System Shapes Our Visual Experience
Nau, M., Julian, J. B., & Doeller, C. F. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.06.008 · Cited by 79 · see citing works
Fotowat, H., Lee, C., Jun, J. J., & Maler, L. (2019) · eLife · doi:10.7554/elife.44119 · Cited by 69 · see citing works
Geometric transformation of cognitive maps for generalization across hippocampal-prefrontal circuits
Tang, W., Shin, J. D., & Jadhav, S. P. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112246 · Cited by 59 · see citing works
Tanni, S., de Cothi, W., & Barry, C. (2022) · Current Biology · doi:10.1016/j.cub.2022.06.046 · Cited by 37 · see citing works
The human brain uses spatial schemas to represent segmented environments
Peer, M., & Epstein, R. A. (2021) · Current Biology · doi:10.1016/j.cub.2021.08.012 · Cited by 38 · see citing works
A population code for spatial representation in the zebrafish telencephalon
Yang, C., Mammen, L., Kim, B., Li, M., Robson, D. N., & Li, J. M. (2024) · Nature · doi:10.1038/s41586-024-07867-2 · Cited by 38 · see citing works
“PCs demonstrate the potential for significant remapping across distinct environments Mammalian PCs are notable for their representational flexibility 10,40,41 , while other spatial cells exhibit more coherent shifts across environments 42–44 .”
Boundary vector cells in the goldfish central telencephalon encode spatial information
Cohen, L., Vinepinsky, E., Donchin, O., & Segev, R. (2023) · PLOS Biology · doi:10.1371/journal.pbio.3001747 · Cited by 37 · see citing works
Presotto, A., Fayrer-Hosken, R., Curry, C., & Madden, M. (2019) · Animal Cognition · doi:10.1007/s10071-019-01242-9 · Cited by 33 · see citing works
Schøyen, V., Pettersen, M. B., Holzhausen, K., Fyhn, M., Malthe-Sørenssen, A., & Lepperød, M. E. (2023) · iScience · doi:10.1016/j.isci.2023.108102 · Cited by 26 · see citing works
“While this aligns with experimental findings of global remapping in place cells being completely un-correlated in different environments, 13,58 this method represents a rather strong transformation for multiple reasons.”
MethodThe 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
Circuit mechanisms for disentangled representations and generalization in the hippocampus
Tang, W., Chang, H., Liu, C., Perez-Hernandez, S., Zheng, W. Y., Park, J., Karaba, L. A., Oliva, A., & Fernandez-Ruiz, A. (2026) · Nature Neuroscience · doi:10.1038/s41593-026-02491-x
- Authors
- Alme, C. B., Miao, C., Jezek, K., Treves, A., Moser, E. I., & Moser, M.-B.
- Affiliations
- Norwegian University of Science and Technology (NO)
- Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, 7491 Trondheim, Norway;
- Scuola Internazionale Superiore di Studi Avanzati (IT)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-12-08
- Volume
- 111
- Issue
- 52
- Pages
- 18428-18435
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4284589
- OpenAlex
- W2001783678
- Cited by
- 296
- References
- 36
- Citations by year
- 2026: 20 · 2025: 33 · 2024: 35 · 2023: 28 · 2022: 28 · 2021: 24 · 2020: 20 · 2019: 40 · 2018: 21 · 2017: 18 · 2016: 15 · 2015: 14
- FWCI
- 8.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- SDL (submittedVersion)
- BIBSYS Brage (BIBSYS (Norway)) (submittedVersion)
- NORA - Norwegian Open Research Archives (submittedVersion, other-oa)
- Funders
- EC | European Research Council (ERC) (268598)
- Kavli Foundation (No number)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Keywords
- place cells, hippocampus, CA3, episodic memory, spatial firing patterns, orthogonal representations, memory capacity, spatial maps, rats
- MeSH terms
- Animals, Behavior, Animal, Brain Mapping, Male, Nerve Net, Rats, Long-Evans, Rats, CA3 Region, Hippocampal
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