Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry
Abstract
Place cells in hippocampal area CA1 may receive positional information from the intrahippocampal associative network in area CA3 or directly from the entorhinal cortex. To determine whether direct entorhinal connections support spatial firing and spatial memory, we removed all input from areas CA3 to CA1, thus isolating the CA1 area. Pyramidal cells in the isolated CA1 area developed sharp and stable place fields. Rats with an isolated CA1 area showed normal acquisition of an associative hippocampal-dependent spatial recognition task. Spatial recall was impaired. These results suggest that the hippocampus contains two functionally separable memory circuits: The direct entorhinal-CA1 system is sufficient for recollection-based recognition memory, but recall depends on intact CA3-CA1 connectivity.
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The disynaptic circuit can account for residual hippocampal-dependent memory and high levels of CA1 place cell firing in vivo following surgical or genetic lesions of CA3.
“Moreover, the disynaptic circuit can account for the residual hippocampal-dependent memory and high levels of CA1 place cell firing in vivo following surgical or genetic lesions of CA3 (Brun et al., 2002; Nakashiba et al., 2008).”
From Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop (2010) · cites this paper as Brun et al., 2002
Cites
(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
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376 · see citing works
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
Self-citationA cortical–hippocampal system for declarative memory
Eichenbaum, H. (2000) · Nature reviews. Neuroscience · doi:10.1038/35036213 · Cited by 1,725 · see citing works
Recognition memory: What are the roles of the perirhinal cortex and hippocampus?
Brown, M. W., & Aggleton, J. P. (2001) · Nature reviews. Neuroscience · doi:10.1038/35049064 · Cited by 1,555 · see citing works
McNaughton, B. L., Barnes, C. A., & O'Keefe, J. (1983) · Experimental Brain Research · doi:10.1007/bf00237147 · Cited by 1,071 · 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
Spatial learning with a minislab in the dorsal hippocampus.
Moser, M., Moser, E. I., Forrest, E., Andersen, P. N., & Morris, R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.21.9697 · Cited by 902 · see citing works
Self-citationNeural Networks and Brain Function
Rolls, E. T., & Treves, A. (1997) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198524328.001.0001 · Cited by 885 · see citing works
Critical role of the hippocampus in memory for sequences of events
Fortin, N. J., Agster, K. L., & Eichenbaum, H. B. (2002) · Nature Neuroscience · doi:10.1038/nn834 · Cited by 881 · see citing works
Natural killer cells, viruses and cancer
Cerwenka, A., & Lanier, L. L. (2001) · Nature reviews. Immunology · doi:10.1038/35095564 · Cited by 874 · see citing works
Quirk, G., Muller, R., Kubie, J., & Ranck, J. B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-05-01945.1992 · Cited by 420 · see citing works
McNaughton, B. L., Barnes, C. A., Meltzer, J., & Sutherland, R. J. (1989) · Experimental Brain Research · doi:10.1007/bf00248904 · Cited by 388 · see citing works
What determines the capacity of autoassociative memories in the brain?
Treves, A., & Rolls, E. T. (1991) · Network Computation in Neural Systems · doi:10.1088/0954-898x_2_4_004 · Cited by 354 · see citing works
Yeckel, M. F., & Berger, T. W. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.15.5832 · Cited by 286 · see citing works
Mizumori, S., McNaughton, B. L., Barnes, C. A., & Fox, K. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-11-03915.1989 · Cited by 223 · see citing works
Entorhinal-Hippocampal Interactions Revealed by Real-Time Imaging
Iijima, T., Witter, M. P., Ichikawa, M., Tominaga, T., Kajiwara, R., & Matsumoto, G. (1996) · Science · doi:10.1126/science.272.5265.1176 · Cited by 222 · see citing works
Self-citationInterdependence of Multiple Theta Generators in the Hippocampus: a Partial Coherence Analysis
Kocsis, B., Bragin, A., & Buzsáki, G. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-06200.1999 · Cited by 218 · see citing works
Handelmann, G. E., & Olton, D. S. (1981) · Brain Research · doi:10.1016/0006-8993(81)90183-9 · Cited by 181 · see citing works
Káli, S., & Dayan, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-19-07463.2000 · Cited by 139 · see citing works
Steffenach, H.-A., Sloviter, R. S., Moser, E. I., & Moser, M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.042700999 · Cited by 129 · see citing works
Self-citationNew excitement in cognitive space: between place cells and spatial memory
Moser, E. I., & Paulsen, O. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(01)00279-3 · Cited by 57 · see citing works
Self-citationCortico-hippocampal communication by way of parallel parahippocampal-subicular pathways.
Lavenex (2000) · Pure Amsterdam UMC · doi:10.1002/1098-1063(2000)10:4 · Cited by 1 · see citing works
Self-citation
Flagged first, then by citations
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Sorted by citations
Place Cells, Grid Cells, and the Brain's Spatial Representation System
Moser, E. I., Kropff, E., & Moser, M.-B. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.061307.090723 · Cited by 1,934 · see citing works
Self-citationFrequency 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-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 · see citing works
Spatial representation in the entorhinal cortex
Fyhn, M., Molden, S., Witter, M. P., Moser, E. I., & Moser, M.-B. (2004) · Science · doi:10.1126/science.1099901 · Cited by 1,339 · see citing works
Self-citationThe anatomy of memory: an interactive overview of the parahippocampal–hippocampal network
van Strien, N. M., Cappaert, N. L. M., & Witter, M. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2614 · Cited by 1,041 · see citing works
Self-citationRemembering the past and imagining the future: A neural model of spatial memory and imagery.
Byrne, P., Becker, S., & Burgess, N. (2007) · Psychological Review · doi:10.1037/0033-295x.114.2.340 · Cited by 1,011 · see citing works
Spatial memory, recognition memory, and the hippocampus
Broadbent, N. J., Squire, L. R., & Clark, R. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406344101 · Cited by 985 · see citing works
Nakashiba, T., Cushman, J. D., Pelkey, K. A., Renaudineau, S., Buhl, D. L., McHugh, T. J., Barrera, V. R., Chittajallu, R., Iwamoto, K. S., McBain, C. J., et al. (2012) · Cell · doi:10.1016/j.cell.2012.01.046 · Cited by 805 · 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-citationModes and models of forebrain cholinergic neuromodulation of cognition
Hasselmo, M. E., & Sarter, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.104 · Cited by 733 · see citing works
Temporal Encoding of Place Sequences by Hippocampal Cell Assemblies
Dragoi, G., & Buzsáki, G. (2006) · Neuron · doi:10.1016/j.neuron.2006.02.023 · Cited by 727 · see citing works
Mizuseki, K., Sirota, A., Pastalkova, E., & Buzsáki, G. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.037 · Cited by 718 · see citing works
Differential Control of Learning and Anxiety along the Dorsoventral Axis of the Dentate Gyrus
Kheirbek, M. A., Drew, L. J., Burghardt, N. S., Costantini, D. O., Tannenholz, L., Ahmari, S. E., Zeng, H., Fenton, A. A., & Hen, R. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.038 · Cited by 713 · see citing works
Jessberger, S., Clark, R. E., Broadbent, N. J., Clemenson, G. D., Consiglio, A., Lie, D. C., Squire, L. R., & Gage, F. H. (2009) · Learning & Memory · doi:10.1101/lm.1172609 · Cited by 654 · see citing works
Rhythms of the hippocampal network
Colgin, L. L. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.21 · Cited by 654 · 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
NMDA receptors, place cells and hippocampal spatial memory
Nakazawa, K., McHugh, T. J., Wilson, M. A., & Tonegawa, S. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1385 · Cited by 619 · see citing works
A computational theory of hippocampal function, and empirical tests of the theory
Rolls, E. T., & Kesner, R. P. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.04.005 · Cited by 608 · 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-citationThe mechanisms for pattern completion and pattern separation in the hippocampus
Rolls, E. T. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00074 · Cited by 545 · see citing works
Place Cells, Grid Cells, and MemoryPreprint
Moser, M., Rowland, D. C., & Moser, E. I. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021808 · Cited by 538 · see citing works
Self-citationRudolph, U., & Möhler, H. (2004) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.44.101802.121429 · Cited by 518 · see citing works
Hippocampal CA3 NMDA Receptors Are Crucial for Memory Acquisition of One-Time Experience
Nakazawa, K., Sun, L. D., Quirk, M. C., Rondi‐Reig, L., Wilson, M. A., & Tonegawa, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00165-x · Cited by 506 · see citing works
Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning
Nakashiba, T., Young, J. Z., McHugh, T. J., Buhl, D. L., & Tonegawa, S. (2008) · Science · doi:10.1126/science.1151120 · Cited by 492 · see citing works
Morris, R., Moser, E. I., Riedel, G., Martin, S. J., Sandin, J., Day, M., & O’Carroll, C. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1264 · Cited by 480 · see citing works
Self-citationA Behavioral Role for Dendritic Integration
Nolan, M. F., Malleret, G., Dudman, J. T., Buhl, D. L., Santoro, B., Gibbs, E., Vronskaya, S., Buzsáki, G., Siegelbaum, S. A., Kandel, E. R., et al. (2004) · Cell · doi:10.1016/j.cell.2004.11.020 · Cited by 472 · see citing works
(2013) · Elsevier eBooks · doi:10.1016/c2010-0-65035-8 · Cited by 465 · see citing works
Vazdarjanova, A., & Guzowski, J. F. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0350-04.2004 · Cited by 465 · see citing works
Play it again: reactivation of waking experience and memory
O’Neill, J., Pleydell-Bouverie, B., Dupret, D., & Csicsvari, J. L. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.01.006 · Cited by 448 · see citing works
Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3
Lee, I., Yoganarasimha, D., Rao, G., & Knierim, J. J. (2004) · Nature · doi:10.1038/nature02739 · Cited by 440 · see citing works
A Behavioral Assessment of Hippocampal Function Based on a Subregional Analysis
Kesner, R. P., Lee, I., & Gilbert, P. E. (2004) · Reviews in the Neurosciences · doi:10.1515/revneuro.2004.15.5.333 · Cited by 435 · see citing works
Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance
Montgomery, S. M., & Buzsáki, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701826104 · Cited by 431 · see citing works
What 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
Self-citationA distinct role for norepinephrine in memory retrieval.
Murchison, C. F., Zhang, X.-Y., Zhang, W.-P., Ouyang, M., Lee, A., & Thomas, S. A. (2004) · Cell · doi:10.1016/s0092-8674(04)00259-4 · Cited by 402 · see citing works
Morris, R. G. M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04888.x · Cited by 398 · see citing works
Gamma Oscillations in the Hippocampus
Colgin, L. L., & Moser, E. I. (2010) · Physiology · doi:10.1152/physiol.00021.2010 · Cited by 376 · see citing works
Self-citationRearing on Hind Legs, Environmental Novelty, and the Hippocampal Formation
Lever, C., Burton, S., & O'Keefe, J. M. (2006) · Reviews in the Neurosciences · doi:10.1515/revneuro.2006.17.1-2.111 · Cited by 366 · 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
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-citationEnsemble Dynamics of Hippocampal Regions CA3 and CA1
Guzowski, J. F., Knierim, J. J., & Moser, E. I. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.003 · Cited by 354 · see citing works
Self-citationEntorhinal Cortex Layer III Input to the Hippocampus Is Crucial for Temporal Association Memory
Suh, J., Rivest, A. J., Nakashiba, T., Tominaga, T., & Tonegawa, S. (2011) · Science · doi:10.1126/science.1210125 · Cited by 352 · see citing works
Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory
Remondes, M., & Schuman, E. M. (2004) · Nature · doi:10.1038/nature02965 · Cited by 352 · see citing works
A computational theory of hippocampal function, and tests of the theory: New developments
Kesner, R. P., & Rolls, E. T. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.009 · Cited by 347 · see citing works
Witter, M. P., & Amaral, D. G. (2004) · Elsevier eBooks · doi:10.1016/b978-012547638-6/50022-5 · Cited by 344 · see citing works
Self-citationNeurocognitive aging: prior memories hinder new hippocampal encoding
Wilson, I. A., Gallagher, M., Eichenbaum, H., & Tanila, H. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.10.002 · Cited by 343 · see citing works
Behavioral functions of the CA3 subregion of the hippocampusPreprint
Kesner, R. P. (2007) · Learning & Memory · doi:10.1101/lm.688207 · Cited by 337 · see citing works
Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop
Chevaleyre, V., & Siegelbaum, S. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.013 · Cited by 324 · see citing works
Building hippocampal circuits to learn and remember: Insights into the development of human memory
Lavenex, P., & Lavenex, P. B. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.02.007 · Cited by 309 · see citing works
Adult neurogenesis: integrating theories and separating functions
Aimone, J. B., Deng, W., & Gage, F. H. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.04.003 · Cited by 303 · see citing works
Roozendaal, B., Hahn, E. L., Nathan, S. V., de Quervain, D. J.-F., & McGaugh, J. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2574-04.2004 · Cited by 301 · see citing works
Jarsky, T., Roxin, A., Kath, W. L., & Spruston, N. (2005) · Nature Neuroscience · doi:10.1038/nn1599 · Cited by 301 · see citing works
Hippocampal mechanisms for the context-dependent retrieval of episodes
Hasselmo, M. E., & Eichenbaum, H. (2005) · Neural Networks · doi:10.1016/j.neunet.2005.08.007 · Cited by 298 · see citing works
Astrocytic regulation of glutamate homeostasis in epilepsy
Coulter, D. A., & Eid, T. (2012) · Glia · doi:10.1002/glia.22341 · Cited by 293 · see citing works
Age-Associated Alterations of Hippocampal Place Cells Are Subregion Specific
Wilson, I. A., Ikonen, S., Gallagher, M., Eichenbaum, H., & Tanila, H. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1744-05.2005 · Cited by 278 · see citing works
Gating of hippocampal activity, plasticity, and memory by entorhinal cortex long-range inhibition
Basu, J., Zaremba, J. D., Cheung, S. K., Hitti, F. L., Zemelman, B. V., Losonczy, A., & Siegelbaum, S. A. (2016) · Science · doi:10.1126/science.aaa5694 · Cited by 274 · see citing works
A computational theory of episodic memory formation in the hippocampus
Rolls, E. T. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.03.027 · Cited by 271 · see citing works
Navigating from hippocampus to parietal cortex
Whitlock, J. R., Sutherland, R. J., Witter, M. P., Moser, M.-B., & Moser, E. I. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804216105 · Cited by 267 · see citing works
Self-citationSpatial 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-citationPKMζ Maintains Spatial, Instrumental, and Classically Conditioned Long-Term Memories
Serrano, P., Friedman, E., Kenney, J., Taubenfeld, S., Zimmerman, J. M., Hanna, J., Alberini, C., Kelley, A., Maren, S., Rudy, J., et al. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060318 · Cited by 273 · see citing works
Glutamate-receptor-mediated encoding and retrieval of paired-associate learning
Day, M., Langston, R. F., & Morris, R. (2003) · Nature · doi:10.1038/nature01769 · Cited by 259 · see citing works
Knierim, J. J., Lee, I., & Hargreaves, E. L. (2006) · Hippocampus · doi:10.1002/hipo.20203 · Cited by 259 · see citing works
Daumas, S., Halley, H., Francès, B., & Lassalle, J. (2005) · Learning & Memory · doi:10.1101/lm.81905 · Cited by 259 · see citing works
Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area
Price, C. J., Cauli, B., Kovacs, E. R., Kulik, A., Lambolez, B., Shigemoto, R., & Capogna, M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1135-05.2005 · Cited by 255 · see citing works
The emergence of grid cells: Intelligent design or just adaptation?
Kropff, E., & Treves, A. (2008) · Hippocampus · doi:10.1002/hipo.20520 · Cited by 254 · see citing works
Hippocampal Place Fields Emerge upon Single-Cell Manipulation of Excitability During Behavior
Lee, D., Lin, B., & Lee, A. K. (2012) · Science · doi:10.1126/science.1221489 · Cited by 251 · see citing works
Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning
Rolls, E. T., Stringer, S. M., & Elliot, T. (2006) · Network Computation in Neural Systems · doi:10.1080/09548980601064846 · Cited by 250 · see citing works
The Corticohippocampal Circuit, Synaptic Plasticity, and MemoryPreprint
Basu, J., & Siegelbaum, S. A. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021733 · Cited by 244 · see citing works
Pattern separation, completion, and categorisation in the hippocampus and neocortex
Rolls, E. T. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.07.008 · Cited by 234 · see citing works
Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map
Leutgeb, S., & Leutgeb, J. K. (2007) · Learning & Memory · doi:10.1101/lm.703907 · Cited by 234 · see citing works
An attractor network in the hippocampus: Theory and neurophysiologyPreprint
Rolls, E. T. (2007) · Learning & Memory · doi:10.1101/lm.631207 · Cited by 232 · see citing works
Computational Models of Grid Cells
Giocomo, L. M., Moser, M., & Moser, E. I. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.023 · Cited by 231 · see citing works
Self-citationTheta–gamma coupling in the entorhinal–hippocampal system
Colgin, L. L. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.08.001 · Cited by 226 · see citing works
Bosman, C. A., Lansink, C. S., & Pennartz, C. M. A. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12606 · Cited by 225 · see citing works
Slow and Fast Gamma Rhythms Coordinate Different Spatial Coding Modes in Hippocampal Place Cells
Bieri, K. W., Bobbitt, K. N., & Colgin, L. L. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.013 · Cited by 221 · see citing works
Moser, E. I., & Moser, M. (2008) · Hippocampus · doi:10.1002/hipo.20483 · Cited by 220 · see citing works
Self-citationGrid cell firing patterns signal environmental novelty by expansion
Barry, C., Ginzberg, L. L., O'Keefe, J. M., & Burgess, N. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209918109 · Cited by 219 · see citing works
Rowland, D. C., Roudi, Y., Moser, M., & Moser, E. I. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-013824 · Cited by 219 · see citing works
Self-citationSun, Y., Nguyen, A. Q., Nguyen, J. P., Le, L., Saur, D., Choi, J., Callaway, E. M., & Xu, X. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.02.030 · Cited by 218 · see citing works
A distinct entorhinal cortex to hippocampal CA1 direct circuit for olfactory associative learning
Li, Y., Xu, J., Liu, Y., Zhu, J., Liu, N., Zeng, W., Huang, N., Rasch, M. J., Jiang, H., Gu, X., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4517 · Cited by 210 · see citing works
Hippocampus and remote spatial memory in rats
Clark, R. E., Broadbent, N., & Squire, L. R. (2004) · Hippocampus · doi:10.1002/hipo.20056 · Cited by 209 · see citing works
Fenton, A. A., Kao, H.-Y., Neymotin, S. A., Olypher, A. V., Vayntrub, Y., Lytton, W. W., & Ludvig, N. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2862-08.2008 · Cited by 208 · 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
Dudman, J. T., Tsay, D., & Siegelbaum, S. A. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.020 · Cited by 192 · see citing works
Disambiguating 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
Ji, J.-Z., & Maren, S. (2008) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.794808 · Cited by 195 · see citing works
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Leutgeb, S., Leutgeb, J. K., Moser, M., & Moser, E. I. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.10.002 · Cited by 183 · see citing works
Self-citationZhu, H., Wang, N., Yao, L., Chen, Q., Zhang, R., Qian, J., Hou, Y., Guo, W., Fan, S., Liu, S., et al. (2018) · Cell · doi:10.1016/j.cell.2018.04.014 · Cited by 182 · see citing works
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Adams, M. M., Shi, L., Linville, M. C., Forbes, M. E., Long, A. B., Bennett, C., Newton, I. G., Carter, C. S., Sonntag, W. E., Riddle, D. R., et al. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2008.01.016 · Cited by 170 · see citing works
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Rolls, E. T. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00035 · Cited by 169 · see citing works
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Katz, Y., Menon, V., Nicholson, D. A., Geinisman, Y., Kath, W. L., & Spruston, N. (2009) · Neuron · doi:10.1016/j.neuron.2009.06.023 · Cited by 163 · see citing works
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Lambert, F. R., Jabès, A., Lavenex, P. B., & Lavenex, P. (2012) · Cognitive Psychology · doi:10.1016/j.cogpsych.2012.08.001 · Cited by 162 · see citing works
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Lengyel, M., Szatmáry, Z., & Érdi, P. (2003) · Hippocampus · doi:10.1002/hipo.10116 · Cited by 162 · see citing works
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Zheng, C., Bieri, K. W., Hsiao, Y., & Colgin, L. L. (2016) · Neuron · doi:10.1016/j.neuron.2015.12.005 · Cited by 160 · see citing works
Schmitt, W. B., Deacon, R. M. J., Seeburg, P. H., Rawlins, J. N. P., & Bannerman, D. M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-09-03953.2003 · Cited by 158 · see citing works
Connections of the subiculum of the rat: Topography in relation to columnar and laminar organization
Witter, M. P. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.06.022 · Cited by 155 · see citing works
Self-citation
- Authors
- Brun, V. H., Otnæss, M. K., Molden, S., Steffenach, H.-A., Witter, M. P., Moser, M.-B., & Moser, E. I.
- Affiliations
- Norwegian University of Science and Technology (NO)
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- Corresponding author
- Moser, Edvard I.
- Venue
- Science
- Published
- 2002-06-21
- Volume
- 296
- Issue
- 5576
- Pages
- 2243-2246
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2004974848
- Cited by
- 606
- References
- 24
- Citations by year
- 2026: 13 · 2025: 20 · 2024: 15 · 2023: 17 · 2022: 17 · 2021: 26 · 2020: 20 · 2019: 18 · 2018: 18 · 2017: 26 · 2016: 35 · 2015: 39 · 2014: 33 · 2013: 25 · 2012: 31
- FWCI
- 13.98
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- place cells, entorhinal cortex, hippocampal CA1, spatial memory, recollection
- MeSH terms
- Action Potentials, Animals, Brain Mapping, Denervation, Electrodes, Implanted, Hippocampus, Interneurons, Memory, Nerve Net, Neural Pathways, Mental Recall, Space Perception, Pyramidal Cells, Entorhinal Cortex, Maze Learning, Rats
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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.
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