Dynamics of the Hippocampal Ensemble Code for Space
Abstract
Ensemble recordings of 73 to 148 rat hippocampal neurons were used to predict accurately the animals' movement through their environment, which confirms that the hippocampus transmits an ensemble code for location. In a novel space, the ensemble code was initially less robust but improved rapidly with exploration. During this period, the activity of many inhibitory cells was suppressed, which suggests that new spatial information creates conditions in the hippocampal circuitry that are conducive to the synaptic modification presumed to be involved in learning. Development of a new population code for a novel environment did not substantially alter the code for a familiar one, which suggests that the interference between the two spatial representations was very small. The parallel recording methods outlined here make possible the study of the dynamics of neuronal interactions during unique behavioral events.
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?
Brain representations of space are encoded by pyramidal cell assemblies in the hippocampus during active behavior.
“Brain representations of space are encoded by pyramidal cell assemblies in the hippocampus during active behavior1-3.”
From Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence (2014) · cites this paper as [2]
Firing associations between dCA1 pyramidal cells reorganized to represent each environment.
“Additionally, we confirmed that firing associations between dCA1 pyramidal cells reorganized to represent each environment2,4,5,17(Supplementary Fig. 2a).”
From Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence (2014) · cites this paper as [2]
Cites
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
Distributed hierarchical processing in the primate cerebral cortex
Felleman, D. J., & Van Essen, D. C. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1 · Cited by 7,783 · see citing works
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,460 · see citing works
LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS
Scoville, W. B., & Milner, B. (1957) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.20.1.11 · Cited by 7,322 · 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
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
Zola-Morgan, S., Squire, L., & Amaral, D. (1986) · The Journal of Neuroscience · doi:10.1523/jneurosci.06-10-02950.1986 · Cited by 1,997 · see citing works
Place units in the hippocampus of the freely moving rat
O'Keefe, J. (1976) · Experimental Neurology · doi:10.1016/0014-4886(76)90055-8 · Cited by 1,836 · see citing works
Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats
Ranck, J. B. (1973) · Experimental Neurology · doi:10.1016/0014-4886(73)90290-2 · Cited by 1,322 · 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
Self-citationHigh-frequency network oscillation in the hippocampus
Buzsáki, G., Horváth, Z., Urioste, R., Hetke, J. F., & Wise, K. D. (1992) · Science · doi:10.1126/science.1589772 · Cited by 1,223 · 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
Self-citationMental Rotation of the Neuronal Population Vector
Georgopoulos, A. P., Lurito, J. T., Petrides, M., Schwartz, A. B., & Massey, J. T. (1989) · Science · doi:10.1126/science.2911737 · Cited by 910 · see citing works
Spatial firing patterns of hippocampal complex-spike cells in a fixed environment
Muller, R., Kubie, J., & Ranck, J. B. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-07-01935.1987 · Cited by 898 · see citing works
Single unit activity in the rat hippocampus during a spatial memory task
O'Keefe, J. M., & Speakman, A. (1987) · Experimental Brain Research · doi:10.1007/bf00255230 · Cited by 782 · see citing works
Pavlides, C., & Winson, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02907.1989 · Cited by 684 · see citing works
Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents
McNaughton, B. L., Douglas, R. M., & Goddard, G. V. (1978) · Brain Research · doi:10.1016/0006-8993(78)90030-6 · Cited by 647 · see citing works
Self-citationMcNaughton, B. L., O'Keefe, J. M., & Barnes, C. A. (1983) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(83)90097-3 · Cited by 571 · see citing works
Self-citationAbeles, M., & Goldstein, M. H. (1977) · Proceedings of the IEEE · doi:10.1109/proc.1977.10559 · Cited by 391 · see citing works
Barnes, C. A., McNaughton, B. L., Mizumori, S. J. Y., Leonard, B. W., & Lin, L.-H. (1990) · Progress in brain research · doi:10.1016/s0079-6123(08)61257-1 · Cited by 371 · see citing works
Self-citationFirst occurrence of hippocampal spatial firing in a new environment
Hill, A. J. (1978) · Experimental Neurology · doi:10.1016/0014-4886(78)90058-4 · Cited by 360 · see citing works
Dependence of Cortical Plasticity on Correlated Activity of Single Neurons and on Behavioral Context
Ahissar, E., Vaadia, E., Ahissar, M., Bergman, H., Arieli, A., & Abeles, M. (1992) · Science · doi:10.1126/science.1529342 · Cited by 358 · see citing works
Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition
Wigström, H., & Gustafsson, B. (1983) · Nature · doi:10.1038/301603a0 · Cited by 351 · see citing works
Place cells and silent cells in the hippocampus of freely-behaving rats
Thompson, L. T., & Best, P. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-07-02382.1989 · Cited by 337 · see citing works
Spatial correlates of hippocampal unit activity
Olton, D. S., Branch, M., & Best, P. J. (1978) · Experimental Neurology · doi:10.1016/0014-4886(78)90096-1 · Cited by 316 · see citing works
Characteristics of hippocampal primed burst potentiation in vitro and in the awake rat
Diamond, D. M., Dunwiddie, T., & Rose, G. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-11-04079.1988 · Cited by 214 · see citing works
Representation in the hippocampus: what do hippocampal neurons code?
Eichenbaum, H., & Cohen, N. J. (1988) · Trends in Neurosciences · doi:10.1016/0166-2236(88)90100-2 · Cited by 184 · see citing works
Reflexes involving triceps surae from the ankle joint of the cat
Chambers, W. W., Liu, C. N., McCouch, G. P., & Yu, J. (1973) · Experimental Neurology · doi:10.1016/0014-4886(73)90030-7 · Cited by 138 · see citing works
The recall of events through the learning of associations between their parts
Gardner-Medwin, A. R. (1976) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1976.0084 · Cited by 125 · see citing works
Behavior of units in hippocampal circuit of the rat during learning.
Segal, M., & Olds, J. (1972) · Journal of Neurophysiology · doi:10.1152/jn.1972.35.5.680 · Cited by 114 · see citing works
Mountcastle, V. B., Reitboeck, H. J., Poggio, G. F., & Steinmetz, M. (1991) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(91)90140-u · Cited by 102 · see citing works
Scharfman, H. E., & Sarvey, J. M. (1985) · Brain Research · doi:10.1016/0006-8993(85)91552-5 · Cited by 50 · see citing works
Neural group properties in the rat hippocampus during the theta rhythm
Kuperstein, M., Eichenbaum, H., & VanDeMark, T. (1986) · Experimental Brain Research · doi:10.1007/bf00239532 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
Self-citationMicrostructure 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
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,423 · 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
Self-citationVisual Feature Integration and the Temporal Correlation Hypothesis
Singer, W., & Gray, C. M. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.003011 · Cited by 3,157 · see citing works
Neuronal Synchrony: A Versatile Code for the Definition of Relations?
Singer, W. (1999) · Neuron · doi:10.1016/s0896-6273(00)80821-1 · Cited by 2,581 · see citing works
The human hippocampus and spatial and episodic memory
Burgess, N., Maguire, E. A., & O'Keefe, J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00830-9 · Cited by 2,401 · see citing works
Fully integrated silicon probes for high-density recording of neural activity
Jun, J. J., Steinmetz, N. A., Siegle, J. H., Denman, D. J., Bauza, M., Barbarits, B., Lee, A. K., Anastassiou, C. A., Andrei, A., Aydın, Ç., et al. (2017) · Nature · doi:10.1038/nature24636 · Cited by 2,190 · 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
Self-citationInvariant visual representation by single neurons in the human brain
Quiroga, R. Q., Reddy, L., Kreiman, G., Koch, C., & Fried, I. (2005) · Nature · doi:10.1038/nature03687 · Cited by 1,988 · see citing works
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
The Neuropsychology of Anxiety
Gray, J. A., & McNaughton, N. (2003) · doi:10.1093/acprof:oso/9780198522713.001.0001 · Cited by 1,933 · see citing works
Large-scale recording of neuronal ensembles
Buzsáki, G. (2004) · Nature Neuroscience · doi:10.1038/nn1233 · Cited by 1,875 · see citing works
Memory, navigation and theta rhythm in the hippocampal-entorhinal system
Buzsáki, G., & Moser, E. I. (2013) · Nature Neuroscience · doi:10.1038/nn.3304 · Cited by 1,847 · see citing works
Reverse 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
Self-citationPyramidal neurons: dendritic structure and synaptic integration
Spruston, N. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2286 · Cited by 1,688 · see citing works
Functional organization of the hippocampal longitudinal axis
Strange, B. A., Witter, M. P., Lein, E. S., & Moser, E. I. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3785 · Cited by 1,738 · see citing works
The role of medial prefrontal cortex in memory and decision making
Euston, D. R., Gruber, A. J., & McNaughton, B. L. (2012) · Neuron · doi:10.1016/j.neuron.2012.12.002 · Cited by 1,541 · see citing works
Self-citationLisman, J. E., & Jensen, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.007 · Cited by 1,609 · see citing works
Neural plasticity in the ageing brain
Burke, S. N., & Barnes, C. A. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1809 · Cited by 1,600 · see citing works
Cellular networks underlying human spatial navigation
Ekstrom, A. D., Kahana, M. J., Caplan, J. B., Fields, T. A., Isham, E. A., Newman, E. L., & Fried, I. (2003) · Nature · doi:10.1038/nature01964 · Cited by 1,425 · 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
Self-citationA review of methods for spike sorting: the detection and classification of neural action potentials
Lewicki, M. S. (1998) · Network Computation in Neural Systems · doi:10.1088/0954-898x_9_4_001 · Cited by 1,372 · see citing works
Neural syntax: cell assemblies, synapsembles, and readers
Buzsáki, G. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.023 · Cited by 1,289 · see citing works
Hu, H., Gan, J., & Jonas, P. (2014) · Science · doi:10.1126/science.1255263 · Cited by 1,197 · 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
Synaptic plasticity, memory and the hippocampus: a neural network approach to causality
Neves, G., Cooke, S. F., & Bliss, T. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2303 · Cited by 1,207 · see citing works
The Molecular and Systems Biology of Memory
Kandel, E. R., Dudai, Y., & Mayford, M. R. (2014) · Cell · doi:10.1016/j.cell.2014.03.001 · Cited by 1,134 · 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
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
Self-citationMemory engrams: Recalling the past and imagining the future
Josselyn, S. A., & Tonegawa, S. (2020) · Science · doi:10.1126/science.aaw4325 · Cited by 1,087 · see citing works
Two functional components of the hippocampal memory system
Eichenbaum, H., Otto, T., & Cohen, N. J. (1994) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00035391 · Cited by 1,094 · see citing works
The Hippocampus, Memory, and Place Cells
Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M., & Tanila, H. (1999) · Neuron · doi:10.1016/s0896-6273(00)80773-4 · Cited by 1,064 · see citing works
Visual Place Recognition: A Survey
Lowry, S., Sünderhauf, N., Newman, P., Leonard, J. J., Cox, D., Corke, P., & Milford, M. J. (2016) · IEEE Transactions on Robotics · doi:10.1109/tro.2015.2496823 · Cited by 1,079 · see citing works
Zhang, K. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-02112.1996 · Cited by 1,001 · see citing works
Truccolo, W., Eden, U. T., Fellows, M. R., Donoghue, J. P., & Brown, E. N. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00697.2004 · Cited by 1,063 · see citing works
Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles
Guzowski, J. F., McNaughton, B. L., Barnes, C. A., & Worley, P. F. (1999) · Nature Neuroscience · doi:10.1038/16046 · Cited by 1,035 · see citing works
Self-citationAwake hippocampal sharp-wave ripples support spatial memory
Jadhav, S. P., Kemere, C., German, P. W., & Frank, L. M. (2012) · Science · doi:10.1126/science.1217230 · Cited by 924 · see citing works
Prefrontal phase locking to hippocampal theta oscillations
Siapas, A. G., Lubenov, E. V., & Wilson, M. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.028 · Cited by 1,014 · see citing works
Self-citationIntracellular Features Predicted by Extracellular Recordings in the Hippocampus In Vivo
Henze, D. A., Borhegyi, Z., Csicsvari, J., Mamiya, A., Harris, K. D., & Buzsáki, G. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.1.390 · Cited by 942 · 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
Self-citationThe 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
NeuroGrid: recording action potentials from the surface of the brain
Khodagholy, D., Gelinas, J. N., Thesen, T., Doyle, W., Devinsky, O., Malliaras, G. G., & Buzsáki, G. (2015) · Nature Neuroscience · doi:10.1038/nn.3905 · Cited by 938 · 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
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
Self-citationDeciphering 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
Self-citationSpatial 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
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 · see citing works
“Place cells in the hippocampal formation fire selectively when an animal moves through particular locations (‘‘place fields’’) in the environment (O’Keefe and Dostrovsky, 1971; Wilson and McNaughton, 1993).”
Self-citationTemporal structure in spatially organized neuronal ensembles: a role for interneuronal networks
Buzsáki, G., & Chrobak, J. J. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80012-3 · Cited by 878 · see citing works
Barthó, P., Hirase, H., Monconduit, L., Zugaro, M. B., Harris, K. D., & Buzsáki, G. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01170.2003 · Cited by 888 · see citing works
Organization of cell assemblies in the hippocampus
Harris, K. D., Csicsvari, J., Hirase, H., Dragoi, G., & Buzsáki, G. (2003) · Nature · doi:10.1038/nature01834 · Cited by 869 · see citing works
Buzsáki, G. (2005) · Hippocampus · doi:10.1002/hipo.20113 · Cited by 872 · see citing works
Intracellular dynamics of hippocampal place cells during virtual navigation
Harvey, C. D., Collman, F., Dombeck, D. A., & Tank, D. W. (2009) · Nature · doi:10.1038/nature08499 · Cited by 854 · see citing works
Functional imaging of hippocampal place cells at cellular resolution during virtual navigation
Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L., & Tank, D. W. (2010) · Nature Neuroscience · doi:10.1038/nn.2648 · Cited by 873 · see citing works
Multiple neural spike train data analysis: state-of-the-art and future challenges
Brown, E. N., Kass, R. E., & Mitra, P. P. (2004) · Nature Neuroscience · doi:10.1038/nn1228 · Cited by 857 · see citing works
Building neural representations of habits.
Jog, M. S., Kubota, Y., Connolly, C. I., Hillegaart, V., & Graybiel, A. M. (1999) · Science · doi:10.1126/science.286.5445.1745 · Cited by 834 · see citing works
Dynamical principles in neuroscience
Rabinovich, M. I., Varona, P., Selverston, A. I., & Abarbanel, H. D. I. (2006) · Reviews of Modern Physics · doi:10.1103/revmodphys.78.1213 · Cited by 819 · see citing works
Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade‐off
O'Reilly, R. C., & McClelland, J. L. (1994) · Hippocampus · doi:10.1002/hipo.450040605 · Cited by 914 · see citing works
Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat
Jung, M. W., Wiener, S. I., & McNaughton, B. L. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-12-07347.1994 · Cited by 818 · see citing works
Self-citationQuirk, G. J., Repa, J. C., & LeDoux, J. E. (1995) · Neuron · doi:10.1016/0896-6273(95)90092-6 · Cited by 808 · 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
Self-citationSpike sorting for large, dense electrode arrays
Rossant, C., Kadir, S., Goodman, D. F. M., Schulman, J., Hunter, M. L. D., Saleem, A. B., Grosmark, A., Belluscio, M., Denfield, G. H., Ecker, A. S., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4268 · Cited by 760 · 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
Synchronous oscillations in neuronal systems: Mechanisms and functions
Gray, C. M. (1994) · Journal of Computational Neuroscience · doi:10.1007/bf00962716 · Cited by 787 · see citing works
A simple role for BDNF in learning and memory?
Cunha, C. (2010) · Frontiers in Molecular Neuroscience · doi:10.3389/neuro.02.001.2010 · Cited by 778 · 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
The 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
Finite scale of spatial representation in the hippocampus
Kjelstrup, K. B., Solstad, T., Brun, V. H., Hafting, T., Leutgeb, S., Witter, M. P., Moser, E. I., & Moser, M.-B. (2008) · Science · doi:10.1126/science.1157086 · Cited by 760 · see citing works
Gray, C. M., Maldonado, P., Wilson, M., & McNaughton, B. L. (1995) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(95)00085-2 · Cited by 746 · see citing works
Self-citationZhang, K., Ginzburg, I., McNaughton, B. L., & Sejnowski, T. J. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.2.1017 · Cited by 741 · 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
Chronic, multisite, multielectrode recordings in macaque monkeys
Nicolelis, M. A. L., Dimitrov, D., Carmena, J. M., Crist, R., Lehew, G., Kralik, J. D., & Wise, S. P. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1934665100 · Cited by 740 · see citing works
Trajectory Encoding in the Hippocampus and Entorhinal Cortex
Frank, L. M., Brown, E. N., & Wilson, M. A. (2000) · Neuron · doi:10.1016/s0896-6273(00)00018-0 · Cited by 731 · see citing works
Self-citationImpact of aging on hippocampal function: plasticity, network dynamics, and cognition
Rosenzweig, E. S., & Barnes, C. A. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00126-0 · Cited by 730 · 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
Etienne, A. S., & Jeffery, K. J. (2004) · Hippocampus · doi:10.1002/hipo.10173 · Cited by 726 · see citing works
Mental imagery: In search of a theory
Pylyshyn, Z. W. (2002) · Behavioral and Brain Sciences · doi:10.1017/s0140525x02000043 · Cited by 728 · see citing works
Deisseroth, K., Bito, H., & Tsien, R. W. (1996) · Neuron · doi:10.1016/s0896-6273(00)80026-4 · Cited by 698 · see citing works
Guzowski, J. F., Setlow, B., Wagner, E. K., & McGaugh, J. L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05089.2001 · Cited by 700 · see citing works
Markus, 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
Self-citationNeuronal competition and selection during memory formation
Han, J.-H., Kushner, S. A., Yiu, A. P., Cole, C. J., Matynia, A., Brown, R. A., Neve, R. L., Guzowski, J. F., Silva, A. J., & Josselyn, S. A. (2007) · Science · doi:10.1126/science.1139438 · Cited by 682 · see citing works
Hippocampal synaptic plasticity, spatial memory and anxiety
Bannerman, D. M., Sprengel, R., Sanderson, D. J., McHugh, S. B., Rawlins, J. N. P., Monyer, H., & Seeburg, P. H. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3677 · Cited by 688 · see citing works
Head direction cells recorded in the anterior thalamic nuclei of freely moving rats
Taube, J. S. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00070.1995 · Cited by 688 · see citing works
Witten, I. B., Steinberg, E. E., Lee, S. Y., Davidson, T. J., Zalocusky, K. A., Brodsky, M., Yizhar, O., Cho, S. L., Gong, S., Ramakrishnan, C., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.10.028 · Cited by 680 · see citing works
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644 · see citing works
Quantitative measures of cluster quality for use in extracellular recordings
Schmitzer-Torbert, N. C., Jackson, J. C., Henze, D. A., Harris, K., & Redish, A. D. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.09.066 · Cited by 642 · see citing works
Brain-Machine Interfaces: From Basic Science to Neuroprostheses and Neurorehabilitation
Lebedev, M., & Nicolelis, M. A. L. (2017) · Physiological Reviews · doi:10.1152/physrev.00027.2016 · Cited by 655 · see citing works
Synaptic plasticity in the hippocampus: LTP and LTD
Malenka, R. C. (1994) · Cell · doi:10.1016/0092-8674(94)90517-7 · Cited by 655 · 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
Uhlhaas, P. J., Haenschel, C., Nikolic, D., & Singer, W. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn062 · Cited by 629 · see citing works
Place cells, head direction cells, and the learning of landmark stability
Knierim, J., Kudrimoti, H., & McNaughton, B. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-03-01648.1995 · Cited by 608 · see citing works
Self-citationRole of experience and oscillations in transforming a rate code into a temporal code
Mehta, M. R., Lee, A. K., & Wilson, M. A. (2002) · Nature · doi:10.1038/nature00807 · Cited by 630 · see citing works
Self-citationNMDA 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
Self-citationSpatial 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-citationReliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus
Csicsvari, J., Hirase, H., Czurko, A., & Buzsáki, G. (1998) · Neuron · doi:10.1016/s0896-6273(00)80525-5 · Cited by 606 · see citing works
Shadlen, M. N., & Movshon, J. A. (1999) · Neuron · doi:10.1016/s0896-6273(00)80822-3 · Cited by 606 · 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
Long-Term Depression in Hippocampus
Bear, M. F., & Abraham, W. C. (1996) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.19.030196.002253 · Cited by 601 · see citing works
Brown, E. N., Frank, L. M., Tang, D., Quirk, M. C., & Wilson, M. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07411.1998 · Cited by 575 · see citing works
Self-citation
- Authors
- Wilson, M. A., & McNaughton, B. L.
- Affiliations
- University of Arizona (US)
- Venue
- Science
- Published
- 1993-08-20
- Volume
- 261
- Issue
- 5124
- Pages
- 1055-1058
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W1969769253
- Cited by
- 2,350
- References
- 33
- Citations by year
- 2026: 38 · 2025: 74 · 2024: 84 · 2023: 87 · 2022: 68 · 2021: 59 · 2020: 71 · 2019: 86 · 2018: 82 · 2017: 86 · 2016: 65 · 2015: 62 · 2014: 98 · 2013: 87 · 2012: 72
- FWCI
- 39.09
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH 46823)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- hippocampus, ensemble coding, spatial representation, place cells, rats, exploration, inhibitory interneurons, synaptic plasticity, learning, novel environment, parallel recording, neuronal interactions, location prediction
- MeSH terms
- Animals, Behavior, Animal, Exploratory Behavior, Hippocampus, Interneurons, Male, Memory, Neurons, Rats, Inbred F344, Space Perception, 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