Cited by 2,350Memory and Neural MechanismsNeural dynamics and brain functionNeuroscience and Neuropharmacology Research

The DOI matches its Crossref record; 33 of the 33 references it cites were found in a registry or an index.

Dynamics of the Hippocampal Ensemble Code for Space

Wilson, Matthew A., McNaughton, Bruce L.·1993·Science

Open this paper in CoChat — free account

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

Crossref · 10.1126/science.8351520

Cites

33 of 33 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Untitled work
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010
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
Long‐lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,424
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
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
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
Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus
Zola-Morgan, S., Squire, L., & Amaral, D. (1986) · The Journal of Neuroscience · doi:10.1523/jneurosci.06-10-02950.1986 · Cited by 1,997
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
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
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
Self-citation

Flagged first, then by citations

Show all 33 references

Research works printed but not linked: 13

10.1113/jphysiol.1973.sp010273 · DOI · Paper page
KUPERSTEIN, M, EXPERIMENTAL BRAIN RESEARCH 61: 438 (1986).
Larson, J., Frontiers in Excitatory Amino Acid Research: 411 (1988).
MCNAUGHTON, B. L., EXPERIMENTAL BRAIN RESEARCH 52: 41 (1983).
McNaughton, B. L., Neuroscience and Connectionist Theory: 1 (1990).
O'KEEFE, J, EXPERIMENTAL BRAIN RESEARCH 68: 1 (1987).
RANCK, J.B., EXP NEUROL 41: 461 (1973).
REECE, M, SOC NEUR ABSTR 15: 1250 (1989).
Rolls, E. T., Neural Models of Plasticity: 240 (1989).
Skaggs, W. E., Neural Information Processing Systems 5: 1030 (1993).
Squire, L. R., Neural Models of Plasticity: 208 (1989).
Swanson, L. W., Handbook of Chemical Neuroanatomy 5: CH2 (1987).
WILSON, M.A., SOC NEUR ABSTR 17: 1395 (1991).

Sorted by citations

Items 401–500 of 1,003

Place‐selective firing contributes to the reverse‐order reactivation of CA1 pyramidal cells during sharp waves in open‐field exploration
Csicsvari, J., O'Neill, J., Allen, K. L., & Senior, T. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05684.x · Cited by 150
Clinical applications of penetrating neural interfaces and Utah Electrode Array technologies
Normann, R. A., & Fernandez, E. (2016) · Journal of Neural Engineering · doi:10.1088/1741-2560/13/6/061003 · Cited by 135
Engram neurons: Encoding, consolidation, retrieval, and forgetting of memory
Guskjolen, A. J., & Cembrowski, M. S. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02137-5 · Cited by 161
Neurogenesis in the dentate gyrus: carrying the message or dictating the tone
Piatti, V. C., Ewell, L. A., & Leutgeb, J. K. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00050 · Cited by 160
Top-down control of hippocampal signal-to-noise by prefrontal long-range inhibition
Malik, R., Li, Y., Schamiloglu, S., & Sohal, V. S. (2022) · Cell · doi:10.1016/j.cell.2022.04.001 · Cited by 142
Robotic and neuronal simulation of the hippocampus and rat navigation
Burgess, N., Donnett, J. G., Jeffery, K. J., & O'Keefe, J. M. (1997) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1997.0140 · Cited by 149
Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments
Cohen, J. D., Bolstad, M., & Lee, A. K. (2017) · eLife · doi:10.7554/elife.23040 · Cited by 146
The Involvement of Recurrent Connections in Area CA3 in Establishing the Properties of Place Fields: a Model
Káli, S., & Dayan, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-19-07463.2000 · Cited by 143
Aging in the rat hippocampus is associated with widespread reductions in the number of glutamate decarboxylase‐67 positive interneurons but not interneuron degeneration
Stanley, D. P., & Shetty, A. K. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02318.x · Cited by 143
Cell Groups Reveal Structure of Stimulus Space
Curto, C., & Itskov, V. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000205 · Cited by 135
Nonlinear Population Codes
Shamir, M., & Sompolinsky, H. (2004) · Neural Computation · doi:10.1162/089976604773717559 · Cited by 141
Updating hippocampal representations: CA2 joins the circuit
Jones, M. W., & McHugh, T. J. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.07.007 · Cited by 147
Spatial- and Task-Dependent Neuronal Responses during Real and Virtual Translocation in the Monkey Hippocampal Formation
Matsumura, N., Nishijo, H., Tamura, R., Eifuku, S., Endo, S., & Ono, T. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-06-02381.1999 · Cited by 140
Auditory fear conditioning increases CS‐elicited spike firing in lateral amygdala neurons even after extensive overtraining
Maren, S. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00281.x · Cited by 139
Decoding neuronal firing and modelling neural networks
Abbott, L. F. (1994) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583500003024 · Cited by 134
Place Field Repetition and Purely Local Remapping in a Multicompartment Environment
Spiers, H. J., Hayman, R. M. A., Jovalekic, A., Marozzi, E., & Jeffery, K. J. (2015) · Cerebral Cortex · doi:10.1093/cercor/bht198 · Cited by 138
The hippocampus: hub of brain network communication for memory
Battaglia, F. P., Benchenane, K., Sirota, A., Pennartz, C. M. A., & Wiener, S. I. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.05.008 · Cited by 351
Information-Geometric Measure for Neural Spikes
Nakahara, H., & Амари, Ш.-И. (2002) · Neural Computation · doi:10.1162/08997660260293238 · Cited by 136
Spatially Distributed Local Fields in the Hippocampus Encode Rat Position
Agarwal, G., Stevenson, I. H., Berényi, A., Mizuseki, K., Buzsáki, G., & Sommer, F. T. (2014) · Science · doi:10.1126/science.1250444 · Cited by 131
A Single Brief Burst Induces GluR1-dependent Associative Short-term Potentiation: A Potential Mechanism for Short-term Memory
Erickson, M. A., Maramara, L. A., & Lisman, J. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21375 · Cited by 137
What is remembered? Role of attention on the encoding and retrieval of hippocampal representations
Muzzio, I. A., Kentros, C. G., & Kandel, E. R. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.172445 · Cited by 142
The brain in motion: How ensemble fluidity drives memory-updating and flexibility
Mau, W., Hasselmo, M. E., & Cai, D. J. (2020) · eLife · doi:10.7554/elife.63550 · Cited by 148
Single Neurons in CA1 Hippocampus Encode Trace Interval Duration during Trace Heart Rate (Fear) Conditioning in Rabbit
McEchron, M. D., Tseng, W., & Disterhoft, J. F. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-04-01535.2003 · Cited by 137
Contributions of intrinsic and synaptic activities to the generation of neuronal discharges in in vitro hippocampus
Cohen, I., & Miles, R. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00485.x · Cited by 141
Accurate spike sorting for multi‐unit recordings
Takekawa, T., Isomura, Y., & Fukai, T. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.07068.x · Cited by 136
EEG Sharp Waves and Sparse Ensemble Unit Activity in the Macaque Hippocampus
Skaggs, W. E., McNaughton, B. L., Permenter, M. R., Archibeque, M., Vogt, J. A., Amaral, D. G., & Barnes, C. A. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00401.2007 · Cited by 147
Self-citation
A novel somatosensory spatial navigation system outside the hippocampal formation
Long, X., & Zhang, S. (2021) · Cell Research · doi:10.1038/s41422-020-00448-8 · Cited by 136
Impaired hippocampal place cell dynamics in a mouse model of the 22q11.2 deletion
Zaremba, J. D., Diamantopoulou, A., Danielson, N., Grosmark, A., Kaifosh, P., Bowler, J. C., Liao, Z., Sparks, F. T., Gogos, J. A., & Losonczy, A. (2017) · Nature Neuroscience · doi:10.1038/nn.4634 · Cited by 126
A distributed representation of internal time
Howard, M. W., Shankar, K. H., Aue, W. R., & Criss, A. H. (2015) · Psychological Review · doi:10.1037/a0037840 · Cited by 133
Spatio-temporal electrical stimuli shape behavior of an embodied cortical network in a goal-directed learning task
Bakkum, D. J., Chao, Z. C., & Potter, S. M. (2008) · Journal of Neural Engineering · doi:10.1088/1741-2560/5/3/004 · Cited by 133
Persistence of neuronal representations through time and damage in the hippocampus
Gonzalez, W. G., Zhang, H., Harutyunyan, A., & Lois, C. (2019) · Science · doi:10.1126/science.aav9199 · Cited by 144
Scale-Invariant Memory Representations Emerge from Moiré Interference between Grid Fields That Produce Theta Oscillations: A Computational Model
Blair, H. T., Welday, A. C., & Zhang, K. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4724-06.2007 · Cited by 135
The Statistical Structure of the Hippocampal Code for Space as a Function of Time, Context, and Value
Lee, J. S., Briguglio, J. J., Cohen, J. D., Romani, S., & Lee, A. K. (2020) · Cell · doi:10.1016/j.cell.2020.09.024 · Cited by 139
Phase Precession in Hippocampal Interneurons Showing Strong Functional Coupling to Individual Pyramidal Cells
Maurer, A. P., Cowen, S. L., Burke, S. N., Barnes, C. A., & McNaughton, B. L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2882-06.2006 · Cited by 132
Self-citation
Cortical gamma oscillations: the functional key is activation, not cognition
Merker, B. H. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.01.013 · Cited by 136
Distinct neural circuits for control of movement vs. holding still
Shadmehr, R. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00840.2016 · Cited by 131
Plasticity, Hippocampal Place Cells, and Cognitive Maps
Shapiro, M. L. (2001) · Archives of Neurology · doi:10.1001/archneur.58.6.874 · Cited by 132
Organization of hippocampal cell assemblies based on theta phase precession
Maurer, A. P., Cowen, S. L., Burke, S. N., Barnes, C. A., & McNaughton, B. L. (2006) · Hippocampus · doi:10.1002/hipo.20202 · Cited by 131
Self-citation
Impaired retention of spatial memory after transection of longitudinally oriented axons of hippocampal CA3 pyramidal cells
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 133
Decoding Visual Inputs From Multiple Neurons in the Human Temporal Lobe
Quiroga, R. Q., Reddy, L., Koch, C., & Fried, I. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00125.2007 · Cited by 131
Automatic Sorting for Multi-Neuronal Activity Recorded With Tetrodes in the Presence of Overlapping Spikes
TAKAHASHI, S. Y., Anzai, Y., & Sakurai, Y. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00827.2002 · Cited by 130
Dynamics of Hippocampal Ensemble Activity Realignment: Time versus Space
Redish, A. D., Rosenzweig, E. S., Bohanick, J. D., McNaughton, B. L., & Barnes, C. A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09298.2000 · Cited by 128
Self-citation
Hippocampal Sharp Waves and Reactivation during Awake States Depend on Repeated Sequential Experience
Jackson, J. C., Johnson, A. C., & Redish, A. D. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4118-06.2006 · Cited by 132
The Neural Substrates of Infant Sleep in Rats
Karlsson, K. Æ., Gall, A. J., Mohns, E. J., Seelke, A. M. H., & BLUMBERG, M. S. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030143 · Cited by 130
Ceramic-Based Multisite Electrode Arrays for Chronic Single-Neuron Recording
Moxon, K. A., Leiser, S., Gerhardt, G. A., Barbee, K. A., & Chapin, J. K. (2004) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2003.821037 · Cited by 129
A simple neural network model of the hippocampus suggesting its pathfinding role in episodic memory retrievalPreprint
Samsonovich, A. V., & Ascoli, G. A. (2005) · Learning & Memory · doi:10.1101/lm.85205 · Cited by 127
Stress-induced alternative splicing of acetylcholinesterase results in enhanced fear memory and long-term potentiation
Nijholt, I., Farchi, N., Kye, M., Sklan, E. H., Shoham, S., Verbeure, B., Owen, D., Hochner, B., Spiess, J., Soreq, H., et al. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001446 · Cited by 126
Hippocampal place codes are gated by behavioral engagement
Pettit, N. L., Yuan, X. C., & Harvey, C. D. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01050-4 · Cited by 122
Human medial temporal lobe neurons respond preferentially to personally relevant images
Viskontas, I. V., Quiroga, R. Q., & Fried, I. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902319106 · Cited by 127
Sequence learning and the role of the hippocampus in rodent navigation
Foster, D. J., & Knierim, J. J. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.12.005 · Cited by 132
On How the Dentate Gyrus Contributes to Memory Discrimination
van Dijk, M. T., & Fenton, A. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.04.018 · Cited by 133
Parametric Population Representation of Retinal Location: Neuronal Interaction Dynamics in Cat Primary Visual Cortex
Jancke, D., Erlhagen, W., Dinse, H. R., Akhavan, A. C., Giese, M. A., Steinhage, A., & Schöner, G. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-09016.1999 · Cited by 125
Encoding of Head Direction by Hippocampal Place Cells in Bats
Rubin, A., Yartsev, M. M., & Ulanovsky, N. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5393-12.2014 · Cited by 125
Sequential-Context-Dependent Hippocampal Activity Is Not Necessary to Learn Sequences with Repeated Elements
Bower, M. R., Euston, D. R., & McNaughton, B. L. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2901-04.2005 · Cited by 120
Self-citation
Grid cell hexagonal patterns formed by fast self‐organized learning within entorhinal cortex
Mhatre, H., Anatoli Gorchetchnikov, A., & Grossberg, S. (2010) · Hippocampus · doi:10.1002/hipo.20901 · Cited by 126
Network dynamics of hippocampal cell‐assemblies resemble multiple spatial maps within single tasks
Jackson, J. C., & Redish, A. D. (2007) · Hippocampus · doi:10.1002/hipo.20359 · Cited by 126
Stress-induced alterations in hippocampal plasticity, place cells, and spatial memory
Kim, J. J., Lee, H. J., Welday, A. C., Song, E., Cho, J., Sharp, P. E., Jung, M. W., & Blair, H. T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708644104 · Cited by 126
Absent or Low Rate of Adult Neurogenesis in the Hippocampus of Bats (Chiroptera)
Amrein, I., Dechmann, D. K. N., Winter, Y., & Lipp, H. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000455 · Cited by 126
Brain Aging: Impaired Coding of Novel Environmental Cues
Tanila, H., Sipilä, P., Shapiro, M., & Eichenbaum, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-13-05167.1997 · Cited by 123
Reconceiving the hippocampal map as a topological template
Dabaghian, Y. A., Brandt, V. L., & Frank, L. M. (2014) · eLife · doi:10.7554/elife.03476 · Cited by 121
The form and function of hippocampal context representations
Smith, D. M., & Bulkin, D. A. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.01.005 · Cited by 136
Signatures of rapid plasticity in hippocampal CA1 representations during novel experiences
Priestley, J. B., Bowler, J. C., Rolotti, S. V., Fusi, S., & Losonczy, A. (2022) · Neuron · doi:10.1016/j.neuron.2022.03.026 · Cited by 122
Parallel Instabilities of Long-Term Potentiation, Place Cells, and Learning Caused by Decreased Protein Kinase A Activity
Rotenberg, A., Abel, T. G., Hawkins, R. D., Kandel, E. R., & Muller, R. U. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08096.2000 · Cited by 123
Mechanisms Responsible for Cognitive Impairment in EpilepsyPreprint
Lenck‐Santini, P., & Scott, R. C. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a022772 · Cited by 123
Indicators and criteria of consciousness in animals and intelligent machines: an inside-out approach
Pennartz, C. M. A., Farisco, M., & Evers, K. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00025 · Cited by 121
Rapid and Continuous Modulation of Hippocampal Network State during Exploration of New Places
Kemere, C. T., Carr, M. F., Karlsson, M. P., & Frank, L. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073114 · Cited by 126
Is there a geometric module for spatial orientation? Insights from a rodent navigation model.
Sheynikhovich, D., Chavarriaga, R., Strösslin, T., Arleo, A., & Wulfram Gerstner, B. (2009) · Psychological Review · doi:10.1037/a0016170 · Cited by 126
Dynamics and Computation of Continuous Attractors
Wu, S., Hamaguchi, K., & Amari, S.-I. (2008) · Neural Computation · doi:10.1162/neco.2008.10-06-378 · Cited by 121
Machine Psychology: Autonomous Behavior, Perceptual Categorization and Conditioning in a Brain-based Device
Krichmar, J. L. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.8.818 · Cited by 121
The hippocampal rate code: anatomy, physiology and theory
Ahmed, O. J., & Mehta, M. R. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.01.009 · Cited by 127
An artificial neural network analogue of learning in autism
Cohen, I. L. (1994) · Biological Psychiatry · doi:10.1016/0006-3223(94)90057-4 · Cited by 119
Dentate Gyrus and CA1 Ensemble Activity during Spatial Reference Frame Shifts in the Presence and Absence of Visual Input
Gothard, K. M., Hoffman, K. L., Battaglia, F. P., & McNaughton, B. L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07284.2001 · Cited by 120
Self-citation
Impaired Hippocampal Ripple-Associated Replay in a Mouse Model of Schizophrenia
Suh, J., Foster, D. J., Davoudi, H., Wilson, M. A., & Tonegawa, S. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.014 · Cited by 117
Self-citation
Coherent Coding of Spatial Position Mediated by Theta Oscillations in the Hippocampus and Prefrontal Cortex
Zielinski, M. C., Shin, J. D., & Jadhav, S. P. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0106-19.2019 · Cited by 127
Role of intercellular interactions in heterosynaptic long-term depression
Scanziani, M., Malenka, R. C., & Nicoll, R. A. (1996) · Nature · doi:10.1038/380446a0 · Cited by 119
Multielectrode recordings: the next steps
Nicolelis, M. A. L., & Ribeiro, S. T. G. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00374-4 · Cited by 119
Hippocampal Pyramidal Cell–Interneuron Spike Transmission Is Frequency Dependent and Responsible for Place Modulation of Interneuron Discharge
Marshall, L., Henze, D. A., Hirase, H., Leinekugel, X., Dragoi, G., & Buzsáki, G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-02-j0001.2002 · Cited by 118
Hippocampal CA1 Circuitry Dynamically Gates Direct Cortical Inputs Preferentially at Theta Frequencies
Ang, C. W., Carlson, G. C., & Coulter, D. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2992-05.2005 · Cited by 116
Correlation between hippocampal BDNF mRNA expression and memory performance in senescent rats
Schaaf, M. J. M., Workel, J. O., Lesscher, H. M. B., Vreugdenhil, E., Oitzl, M. S., & de Kloet, E. R. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02855-4 · Cited by 124
REVIEW ■ : Multiple Representations of Space in the Brain
Gross, C. G., & Graziano, M. S. A. (1995) · The Neuroscientist · doi:10.1177/107385849500100107 · Cited by 118
Modular Realignment of Entorhinal Grid Cell Activity as a Basis for Hippocampal Remapping
Monaco, J. D., & Abbott, L. F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1433-11.2011 · Cited by 116
Neural Mechanisms for Encoding Binocular Disparity: Receptive Field Position Versus Phase
Anzai, A., Ohzawa, I., & Freeman, R. D. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.2.874 · Cited by 117
On Decoding the Responses of a Population of Neurons from Short Time Windows
Panzeri, S., Treves, A., Schultz, S. R., & Rolls, E. T. (1999) · Neural Computation · doi:10.1162/089976699300016142 · Cited by 117
Excitotoxic Septal Lesions Result in Spatial Memory Deficits and Altered Flexibility of Hippocampal Single-Unit Representations
Leutgeb, S., & Mizumori, S. J. Y. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-15-06661.1999 · Cited by 116
Induction of Hebbian and Non-Hebbian Mossy Fiber Long-Term Potentiation by Distinct Patterns of High-Frequency Stimulation
Urban, N. N., & Barrionuevo, G. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-13-04293.1996 · Cited by 118
Hippocampal output area CA1 broadcasts a generalized novelty signal during an object-place recognition task
Larkin, M. C., Lykken, C., Tye, L. D., Wickelgren, J. G., & Frank, L. M. (2014) · Hippocampus · doi:10.1002/hipo.22268 · Cited by 110
Multiscale representation of very large environments in the hippocampus of flying bats
Eliav, T., Maimon, S. R., Aljadeff, J., Tsodyks, M. V., Ginosar, G., Las, L., & Ulanovsky, N. (2021) · Science · doi:10.1126/science.abg4020 · Cited by 118
Novel Environments Enhance the Induction and Maintenance of Long-Term Potentiation in the Dentate Gyrus
Davis, C. D., Jones, F. L., & Derrick, B. E. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4970-03.2004 · Cited by 118
Outwardly Rectifying Tonically Active GABA A Receptors in Pyramidal Cells Modulate Neuronal Offset, Not Gain
Pavlov, I., Savtchenko, L. P., Kullmann, D. M., Semyanov, A. V., & Walker, M. C. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2747-09.2009 · Cited by 117
Local Feedback Inhibition Tightly Controls Rapid Formation of Hippocampal Place Fields
Rolotti, S. V., Ahmed, M. S., Szoboszlay, M., Geiller, T., Negrean, A., Blockus, H., Gonzalez, K. C., Sparks, F. T., Canales, A. S. S., Tuttman, A. L., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.12.003 · Cited by 115
Rapid Activation of Plasticity-Associated Gene Transcription in Hippocampal Neurons Provides a Mechanism for Encoding of One-Trial Experience
Miyashita, T., Kubík, Š., Haghighi, N., Steward, O., & Guzowski, J. F. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4588-08.2009 · Cited by 118
A multiscale dynamic routing circuit for forming size- and position-invariant object representations
Olshausen, B. A., Anderson, C. H., & Essen, D. C. V. (1995) · Journal of Computational Neuroscience · doi:10.1007/bf00962707 · Cited by 119
Network and intrinsic cellular mechanisms underlying theta phase precession of hippocampal neurons
Maurer, A. P., & McNaughton, B. L. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.05.002 · Cited by 112
Self-citation
MULTIMODAL SENSORY INTEGRATION AND CONCURRENT NAVIGATION STRATEGIES FOR SPATIAL COGNITION IN REAL AND ARTIFICIAL ORGANISMS
Arleo, A., & Rondi‐Reig, L. (2007) · Journal of Integrative Neuroscience · doi:10.1142/s0219635207001593 · Cited by 131
Subcircuits of Deep and Superficial CA1 Place Cells Support Efficient Spatial Coding across Heterogeneous Environments
Sharif, F., Tayebi, B., Buzsáki, G., Royer, S., & Fernandez-Ruiz, A. (2021) · Neuron · doi:10.1016/j.neuron.2020.10.034 · Cited by 111
Tetrode technology: advances in implantable hardware, neuroimaging, and data analysis techniques
Jog, M., Connolly, C. I., Kubota, Y., Iyengar, D. R., Garrido, L., Harlan, R., & Graybiel, A. M. (2002) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(02)00092-4 · Cited by 109
Representation of Objects in Space by Two Classes of Hippocampal Pyramidal Cells
Rivard, B., Li, Y., Lenck‐Santini, P., Poucet, B., & Muller, R. U. (2004) · The Journal of General Physiology · doi:10.1085/jgp.200409015 · Cited by 111
Synaptic plasticity, place cells and spatial memory: study with second generation knockouts
Wilson, M. A., & Tonegawa, S. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01023-5 · Cited by 111
Self-citation
Thinking About Brain Cell Assemblies
Eichenbaum, H. (1993) · Science · doi:10.1126/science.8351525 · Cited by 111
Human Hippocampal CA1 Involvement during Allocentric Encoding of Spatial Information
Suthana, N., Ekstrom, A. D., Moshirvaziri, S., Knowlton, B. J., & Bookheimer, S. Y. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0621-09.2009 · Cited by 119

Authors: Wilson, M. A., & McNaughton, B. L.
Affiliations: University of Arizona (US)
ORCID: Wilson, Matthew A.
McNaughton, Bruce L.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 1993-08-20
Volume: 261
Issue: 5124
Pages: 1055-1058
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.8351520
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

Dynamics of the Hippocampal Ensemble Code for Space

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks