Do hippocampal pyramidal cells respond to nonspatial stimuli?
Open accessAbstract
There are currently a number of theories of rodent hippocampal function. They fall into two major groups that differ in the role they impute to space in hippocampal information processing. On one hand, the cognitive map theory sees space as crucial and central, with other types of nonspatial information embedded in a primary spatial framework. On the other hand, most other theories see the function of the hippocampal formation as broader, treating all types of information as equivalent and concentrating on the processes carried out irrespective of the specific material being represented, stored, and manipulated. One crucial difference, therefore, is the extent to which theories see hippocampal pyramidal cells as representing nonspatial information independently of a spatial framework. Studies have reported the existence of single hippocampal unit responses to nonspatial stimuli, both to simple sensory inputs as well as to more complex stimuli such as objects, conspecifics, rewards, and time, and these findings been interpreted as evidence in favor of a broader hippocampal function. Alternatively, these nonspatial responses might actually be feature-in-place signals where the spatial nature of the response has been masked by the fact that the objects or features were only presented in one location or one spatial context. In this article, we argue that when tested in multiple locations, the hippocampal response to nonspatial stimuli is almost invariably dependent on the animal’s location. Looked at collectively, the data provide strong support for the cognitive map theory.
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The observation that CA1 pyramidal cell activity is systematically biased by the animal's location supports the view that space is a fundamental dimension encoded within the hippocampal cognitive map.
“This observation supports the view that space is a fundamental dimension encoded within the hippocampal cognitive map23,80.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [80]
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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
Self-citationMemory 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
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
Self-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
Packard, M. G., & McGaugh, J. L. (1996) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.0007 · Cited by 1,505 · see citing works
Episodic-like memory during cache recovery by scrub jays
Clayton, N. S., & Dickinson, A. (1998) · Nature · doi:10.1038/26216 · Cited by 1,464 · see citing works
Internally Generated Cell Assembly Sequences in the Rat Hippocampus
Pastalkova, E., Itskov, V., Amarasingham, A., & Buzsáki, G. (2008) · Science · doi:10.1126/science.1159775 · Cited by 1,301 · 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
Hippocampal ‘time cells’ bridge the gap in memory for discontiguous events
MacDonald, C. J., Lepage, K. Q., Eden, U. T., & Eichenbaum, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.012 · Cited by 1,193 · see citing works
Long-term dynamics of CA1 hippocampal place codes
Ziv, Y., Burns, L. D., Cocker, E. D., Hamel, E. O., Ghosh, K. K., Kitch, L. J., Gamal, A. E., & Schnitzer, M. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3329 · Cited by 1,155 · see citing works
What Is a Cognitive Map? Organizing Knowledge for Flexible Behavior
Behrens, T. E. J., Muller, T. H., Whittington, J. C. R., Mark, S., Baram, A. B., Stachenfeld, K. L., & Kurth-Nelson, Z. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.002 · Cited by 1,055 · see citing works
The hippocampal CA2 region is essential for social memory
Hitti, F. L., & Siegelbaum, S. A. (2014) · Nature · doi:10.1038/nature13028 · Cited by 976 · 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
The hippocampal memory indexing theory.
Teyler, T. J., & DiScenna, P. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.2.147 · Cited by 871 · 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
Mapping of a non-spatial dimension by the hippocampal-entorhinal circuit
Aronov, D., Nevers, R., & Tank, D. W. (2017) · Nature · doi:10.1038/nature21692 · Cited by 773 · see citing works
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
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
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
Can We Reconcile the Declarative Memory and Spatial Navigation Views on Hippocampal Function?
Eichenbaum, H., & Cohen, N. J. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.032 · Cited by 615 · 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
Assessing rodent hippocampal involvement in the novel object recognition task. A review
Cohen, S. J., & Stackman, R. W. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.08.002 · Cited by 595 · see citing works
Hippocampal “Time Cells”: Time versus Path Integration
Kraus, B. J., Robinson, R. J., White, J. A., Eichenbaum, H., & Hasselmo, M. E. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.015 · Cited by 526 · see citing works
Whishaw, I. Q., & Vanderwolf, C. H. (1973) · Behavioral Biology · doi:10.1016/s0091-6773(73)80041-0 · Cited by 508 · see citing works
Accumulation of Hippocampal Place Fields at the Goal Location in an Annular Watermaze Task
Hollup, S., Molden, S., Donnett, J. G., Moser, M., & Moser, E. I. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01635.2001 · Cited by 490 · see citing works
Integrating time from experience in the lateral entorhinal cortex
Tsao, A., Sugar, J., Lu, L., Wang, C., Knierim, J. J., Moser, M.-B., & Moser, E. I. (2018) · Nature · doi:10.1038/s41586-018-0459-6 · Cited by 490 · see citing works
Gothard, K., Skaggs, W. E., Moore, K. L., & McNaughton, B. L. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-02-00823.1996 · Cited by 488 · see citing works
Précis of O'Keefe & Nadel's The hippocampus as a cognitive map
O'Keefe, J., & Nadel, L. (1979) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00063949 · Cited by 486 · see citing works
Self-citationInterleaving brain systems for episodic and recognition memory.
Aggleton, J., & Brown, M. W. (2006) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.08.003 · Cited by 465 · see citing works
Space and Time: The Hippocampus as a Sequence Generator
Buzsáki, G., & Tingley, D. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.07.006 · Cited by 461 · see citing works
Coordination of entorhinal–hippocampal ensemble activity during associative learning
Igarashi, K. M., Lu, L., Colgin, L. L., Moser, M., & Moser, E. I. (2014) · Nature · doi:10.1038/nature13162 · Cited by 435 · see citing works
Hippocampus, time, and memory.
Meck, W. H., Church, R. M., & Olton, D. S. (2013) · Behavioral Neuroscience · doi:10.1037/a0034188 · Cited by 416 · see citing works
Rhinal cortex lesions and object recognition in rats.
Mumby, D. G., & Pinel, J. P. J. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.1.11 · Cited by 412 · see citing works
Spatial and behavioral correlates of hippocampal neuronal activity
Wiener, S. I., Paul, C., & Eichenbaum, H. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02737.1989 · Cited by 397 · see citing works
Gradual changes in hippocampal activity support remembering the order of events
Manns, J. R., Howard, M. W., & Eichenbaum, H. (2007) · Neuron · doi:10.1016/j.neuron.2007.08.017 · Cited by 397 · see citing works
A Dedicated Population for Reward Coding in the Hippocampus
Gauthier, J. L., & Tank, D. W. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.008 · Cited by 394 · see citing works
Configural association theory and the hippocampal formation: An appraisal and reconfiguration
Rudy, J. W., & Sutherland, R. J. (1995) · Hippocampus · doi:10.1002/hipo.450050502 · Cited by 379 · see citing works
Eichenbaum, H., Kuperstein, M., Fagan, A., & Nagode, J. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-03-00716.1987 · Cited by 378 · see citing works
Context and conditioning: A place for space
Nadel, L., & Willner, J. (1980) · Physiological Psychology · doi:10.3758/bf03332853 · Cited by 373 · see citing works
Robust Conjunctive Item–Place Coding by Hippocampal Neurons Parallels Learning What Happens Where
Komorowski, R. W., Manns, J. R., & Eichenbaum, H. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1378-09.2009 · Cited by 372 · see citing works
Neuronal code for extended time in the hippocampus
Mankin, E. A., Sparks, F. T., Slayyeh, B., Sutherland, R. J., Leutgeb, S., & Leutgeb, J. K. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214107109 · Cited by 371 · see citing works
Rhinal cortex lesions and object recognition in rats.
Mumby, D. G., & Pinel, J. P. J. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.1.11 · Cited by 348 · see citing works
Selective information routing by ventral hippocampal CA1 projection neurons
Ciocchi, S., Passecker, J., Malagon‐Vina, H., Mikuš, N., & Klausberger, T. (2015) · Science · doi:10.1126/science.aaa3245 · Cited by 344 · see citing works
Vectorial representation of spatial goals in the hippocampus of bats
Sarel, A., Finkelstein, A., Las, L., & Ulanovsky, N. (2017) · Science · doi:10.1126/science.aak9589 · Cited by 340 · see citing works
How vision and movement combine in the hippocampal place code
Chen, G., King, J. A., Burgess, N., & O'Keefe, J. M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1215834110 · Cited by 338 · see citing works
Self-citationHeterogeneous Modulation of Place Cell Firing by Changes in Context
Anderson, M. I., & Jeffery, K. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-26-08827.2003 · Cited by 328 · see citing works
Sustained activation of hippocampal pyramidal cells by ‘space clamping’ in a running wheel
Czurkó, A., Hirase, H., Csicsvari, J. L., & Buzsáki, G. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00446.x · Cited by 326 · see citing works
Krechevsky, I. (1932) · Psychological Review · doi:10.1037/h0073500 · Cited by 325 · see citing works
Hippocampus, time, and memory.
Meck, W. H., Church, R. M., & Olton, D. S. (1984) · Behavioral Neuroscience · doi:10.1037/0735-7044.98.1.3 · Cited by 319 · see citing works
Distinct hippocampal time cell sequences represent odor memories in immobilized rats
MacDonald, C. J., Carrow, S., Place, R., & Eichenbaum, H. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1537-13.2013 · Cited by 312 · see citing works
Episodic-like Memory in the Rat
Babb, S. J., & Crystal, J. D. (2006) · Current Biology · doi:10.1016/j.cub.2006.05.025 · Cited by 308 · see citing works
Vaccari, C., Lolait, S. J., & Ostrowski, N. L. (1998) · Endocrinology · doi:10.1210/endo.139.12.6382 · Cited by 308 · see citing works
Moita, M. A. P., Rosis, S., Zhou, Y., LeDoux, J. E., & Blair, H. T. (2003) · Neuron · doi:10.1016/s0896-6273(03)00033-3 · Cited by 295 · see citing works
The Hippocampus and Memory for “What,” “Where,” and “When”
Ergorul, C., & Eichenbaum, H. (2004) · Learning & Memory · doi:10.1101/lm.73304 · Cited by 294 · see citing works
During Running in Place, Grid Cells Integrate Elapsed Time and Distance Run
Kraus, B. J., Brandon, M. P., Robinson, R. J., Connerney, M. A., Hasselmo, M. E., & Eichenbaum, H. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.031 · Cited by 293 · see citing works
Sublayer-Specific Coding Dynamics during Spatial Navigation and Learning in Hippocampal Area CA1
Danielson, N. B., Zaremba, J. D., Kaifosh, P., Bowler, J., Ladow, M., & Losonczy, A. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.020 · Cited by 288 · see citing works
Social place-cells in the bat hippocampus
Omer, D. B., Maimon, S. R., Las, L., & Ulanovsky, N. (2018) · Science · doi:10.1126/science.aao3474 · Cited by 280 · see citing works
Hippocampal CA2 activity patterns change over time to a larger extent than between spatial contexts
Mankin, E. A., Diehl, G. W., Sparks, F. T., Leutgeb, S., & Leutgeb, J. K. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.001 · Cited by 279 · see citing works
Hippocampal ensemble dynamics timestamp events in long-term memory
Rubin, A., Geva, N., Sheintuch, L., & Ziv, Y. (2015) · eLife · doi:10.7554/elife.12247 · Cited by 266 · see citing works
Spatial representations of self and other in the hippocampus
Danjo, T., Toyoizumi, T., & Fujisawa, S. (2018) · Science · doi:10.1126/science.aao3898 · Cited by 257 · see citing works
The hippocampus and contextual memory retrieval in Pavlovian conditioning
Maren, S., & Holt, W. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00188-6 · Cited by 256 · see citing works
Hippocampal place cells: stereotypy and plasticity
Breese, C., Hampson, R., & Deadwyler, S. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-04-01097.1989 · Cited by 255 · see citing works
Wistar rats show episodic-like memory for unique experiences
KARTTEKE, E., DESOUZASILVA, M., HUSTON, J., & DERE, E. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.10.002 · Cited by 250 · see citing works
Integrated memory for objects, places, and temporal order: Evidence for episodic-like memory in mice
Dere, E., Huston, J. P., & De Souza Silva, M. A. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.07.002 · Cited by 243 · see citing works
Chiba, A. A., Kesner, R. P., & Reynolds, A. M. (1994) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(05)80065-2 · Cited by 241 · see citing works
A cognitive map for object memory in the hippocampusPreprint
Manns, J. R., & Eichenbaum, H. (2009) · Learning & Memory · doi:10.1101/lm.1484509 · Cited by 240 · see citing works
Goal-Related Activity in Hippocampal Place Cells
Hok, V., Lenck‐Santini, P., Roux, S., Save, É., Muller, R. U., & Poucet, B. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2864-06.2007 · Cited by 232 · see citing works
Grid cells and theta as oscillatory interference: Electrophysiological data from freely moving rats
Jeewajee, A., Barry, C., O'Keefe, J., & Burgess, N. (2008) · Hippocampus · doi:10.1002/hipo.20510 · Cited by 212 · see citing works
Self-citationHippocampal Neurons Responding to First-Time Dislocation of a Target Object
Fyhn, M., Molden, S., Hollup, S., Moser, M., & Moser, E. I. (2002) · Neuron · doi:10.1016/s0896-6273(02)00784-5 · Cited by 202 · see citing works
Dudchenko, P. A., Wood, E. R., & Eichenbaum, H. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-08-02964.2000 · Cited by 198 · see citing works
Social and novel contexts modify hippocampal CA2 representations of space
Alexander, G. M., Farris, S., Pirone, J. R., Zheng, C., Colgin, L. L., & Dudek, S. M. (2016) · Nature Communications · doi:10.1038/ncomms10300 · Cited by 191 · see citing works
Lee, I., Griffin, A. L., Zilli, E. A., Eichenbaum, H., & Hasselmo, M. E. (2006) · Neuron · doi:10.1016/j.neuron.2006.06.033 · Cited by 190 · see citing works
Ventral Hippocampal Neurons Are Shaped by Experience to Represent Behaviorally Relevant Contexts
Komorowski, R. W., Garcia, C., Wilson, A., Hattori, S., Howard, M. W., & Eichenbaum, H. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5458-12.2013 · Cited by 188 · see citing works
Time cells in hippocampal area CA3
Salz, D. M., Tiganj, Z., Khasnabish, S., Kohley, A., Sheehan, D., Howard, M. W., & Eichenbaum, H. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0087-16.2016 · Cited by 183 · see citing works
Discrimination of what, when, and where: Implications for episodic-like memory in rats
Babb, S. J., & Crystal, J. D. (2005) · Learning and Motivation · doi:10.1016/j.lmot.2005.02.009 · Cited by 181 · see citing works
Internally Recurring Hippocampal Sequences as a Population Template of Spatiotemporal Information
Villette, V., Malvache, A., Tressard, T., Dupuy, N., & Cossart, R. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.052 · Cited by 165 · see citing works
Hippocampal CA1 Place Cells Encode Intended Destination on a Maze with Multiple Choice Points
Ainge, J. A., Tamošiūnaitė, M., Wörgötter, F., & Dudchenko, P. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2011-07.2007 · Cited by 164 · see citing works
Retrograde and anterograde object recognition in rats with hippocampal lesions
Gaskin, S., Tremblay, A., & Mumby, D. G. (2003) · Hippocampus · doi:10.1002/hipo.10154 · Cited by 160 · see citing works
Evidence for remembering when events occurred in a rodent model of episodic memory
Zhou, W., & Crystal, J. D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904360106 · Cited by 152 · see citing works
Task-Dependent Representations in Rat Hippocampal Place Neurons
Kobayashi, T., Nishijo, H., Fukuda, M., Bureš, J., & Ono, T. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.2.597 · Cited by 151 · see citing works
Nonspatial Sequence Coding in CA1 Neurons
Allen, T. A., Salz, D. M., McKenzie, S., & Fortin, N. J. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2874-15.2016 · Cited by 149 · see citing works
Otto, T., Schottler, F., Staubli, U. V., Eichenbaum, H., & LYNCH, G. S. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.1.111 · Cited by 137 · see citing works
Learned interaction of visual and idiothetic cues in the control of place field orientation
Jeffery, K. J., & O'Keefe, J. M. (1999) · Experimental Brain Research · doi:10.1007/s002210050785 · Cited by 137 · see citing works
Self-citationDiscrimination of what, when, and where is not based on time of day
Babb, S. J., & Crystal, J. D. (2006) · Learning & Behavior · doi:10.3758/bf03193188 · Cited by 136 · see citing works
Place cells in the ventral hippocampus of rats
Poucet, B., Thinus‐Blanc, C., & Muller, R. U. (1994) · Neuroreport · doi:10.1097/00001756-199410270-00014 · Cited by 135 · see citing works
Hippocampal neurons represent events as transferable units of experience
Sun, C., Yang, W., Martin, J., & Tonegawa, S. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0614-x · Cited by 135 · 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
Sharp, P. E. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:4 · Cited by 125 · see citing works
Hippocampal Unit Activity during Classical Aversive and Appetitive Conditioning
Segal, M., Disterhoft, J. F., & Olds, J. (1972) · Science · doi:10.1126/science.175.4023.792 · Cited by 124 · see citing works
Recalibration of path integration in hippocampal place cells
Jayakumar, R. P., Madhav, M. S., Savelli, F., Blair, H. T., Cowan, N. J., & Knierim, J. J. (2019) · Nature · doi:10.1038/s41586-019-0939-3 · Cited by 113 · see citing works
Place cells on a maze encode routes rather than destinations
Grieves, R. M., Wood, E. R., & Dudchenko, P. A. (2016) · eLife · doi:10.7554/elife.15986 · Cited by 106 · see citing works
Mair, R. G., Burk, J. A., & Porter, M. C. (1998) · Behavioral Neuroscience · doi:10.1037//0735-7044.112.4.772 · Cited by 102 · see citing works
Zinyuk, L. E., Kubík, Š., Kaminsky, Y., Fenton, A. A., & Bureš, J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3771 · Cited by 102 · see citing works
Little and often: Ingestive behavior patterns following hippocampal lesions in rats.
Clifton, P. G., Vickers, S. P., & Somerville, E. M. (1998) · Behavioral Neuroscience · doi:10.1037//0735-7044.112.3.502 · Cited by 100 · see citing works
The Hippocampal CA2 Ensemble Is Sensitive to Contextual Change
Wintzer, M. E., Boehringer, R., Polygalov, D., & McHugh, T. J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2563-13.2014 · Cited by 98 · see citing works
Speakman, A., & O'Keefe, J. M. (1990) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1990.tb00445.x · Cited by 96 · see citing works
Self-citationMair, R. G., Burk, J. A., & Porter, M. C. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.4.772 · Cited by 95 · see citing works
Hippocampus, time, and memory—A retrospective analysis.
Meck, W. H., Church, R. M., & Matell, M. S. (2013) · Behavioral Neuroscience · doi:10.1037/a0034201 · Cited by 92 · see citing works
Little and often: Ingestive behavior patterns following hippocampal lesions in rats.
Clifton, P. G., Vickers, S. P., & Somerville, E. M. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.3.502 · Cited by 92 · see citing works
Insensitivity of place cells to the value of spatial goals in a two-choice flexible navigation task
Duvelle, É., Grieves, R. M., Hok, V., Poucet, B., Arleo, A., Jeffery, K. J., & Save, É. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1578-18.2018 · Cited by 91 · see citing works
Neuronal Responses to Conspecifics in the Ventral CA1
Rao, R. P., von Heimendahl, M., Bahr, V., & Brecht, M. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.081 · Cited by 85 · see citing works
Hippocampal neurons inhibit meal onset
Henderson, Y. O., Smith, G. P., & Parent, M. B. (2012) · Hippocampus · doi:10.1002/hipo.22062 · Cited by 83 · see citing works
Itskov, P. M., Vinnik, E., & Diamond, M. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016462 · Cited by 78 · see citing works
Hippocampal Neural Correlates for Values of Experienced Events
Lee, H., Ghim, J.-W., Kim, H., Lee, D., & Jung, M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2806-12.2012 · Cited by 77 · see citing works
Kobayashi, T., Tran, A. H., Nishijo, H., Ono, T., & Matsumoto, G. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00700-5 · Cited by 77 · see citing works
Place field assembly distribution encodes preferred locations
Mamad, O., Stumpp, L., McNamara, H. M., Ramakrishnan, C., Deisseroth, K., Reilly, R. B., & Tsanov, M. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2002365 · Cited by 73 · see citing works
Sakurai, Y. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00509-2 · Cited by 70 · see citing works
Prefrontal Cortex Focally Modulates Hippocampal Place Cell Firing Patterns
Hok, V., Chah, E., Save, É., & Poucet, B. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3427-12.2013 · Cited by 69 · see citing works
Remembering to eat: hippocampal regulation of meal onset
Parent, M. B., Darling, J. N., & Henderson, Y. O. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00496.2013 · Cited by 66 · see citing works
Weak and Nondiscriminative Responses to Conspecifics in the Rat Hippocampus
von Heimendahl, M., Rao, R. P., & Brecht, M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3812-11.2012 · Cited by 63 · see citing works
The Spatial Prepositions in English, Vector Grammar, and the Cognitive Map Theory
O'Keefe, J. M. (1996) · The MIT Press eBooks · doi:10.7551/mitpress/4107.003.0009 · Cited by 62 · see citing works
Self-citationMembrane potential dynamics underlying context-dependent sensory responses in the hippocampus
Zhao, X., Wang, Y., Spruston, N., & Magee, J. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0646-2 · Cited by 61 · see citing works
Kaut, K. P., & Bunsey, M. D. (2001) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.1.3.270 · Cited by 55 · see citing works
The Integration of Goal-Directed Signals onto Spatial Maps of Hippocampal Place Cells
Aoki, Y., Igata, H., Ikegaya, Y., & Sasaki, T. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.002 · Cited by 54 · see citing works
Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task
Itskov, P. M., Vinnik, E., Honey, C., Schnupp, J. W. H., & Diamond, M. E. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00404.2011 · Cited by 51 · see citing works
Interaction of Taste and Place Coding in the Hippocampus
Herzog, L. E., Pascual, L. M., Scott, S. J., Mathieson, E., Katz, D. B., & Jadhav, S. P. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2478-18.2019 · Cited by 48 · see citing works
Navigating Through Time: A Spatial Navigation Perspective on How the Brain May Encode Time
Issa, J. B., Tocker, G., Hasselmo, M. E., Heys, J. G., & Dombeck, D. A. (2020) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-101419-011117 · Cited by 46 · see citing works
Ainge, J. A., Tamošiūnaitė, M., Wörgötter, F., & Dudchenko, P. A. (2011) · Hippocampus · doi:10.1002/hipo.20919 · Cited by 45 · see citing works
Behavioral correlates of the distributed coding of spatial context
Anderson, M. I., Killing, S. E. A., Morris, C., O'Donoghue, A., Onyiagha, D., Stevenson, R., Verriotis, M., & Jeffery, K. J. (2006) · Hippocampus · doi:10.1002/hipo.20206 · Cited by 44 · see citing works
Siegel, J. J., Neunuebel, J. P., & Knierim, J. J. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00731.2007 · Cited by 39 · see citing works
Hippocampal CA1 activity correlated with the distance to the goal and navigation performance
Spiers, H. J., Ólafsdóttir, H. F., & Lever, C. (2017) · Hippocampus · doi:10.1002/hipo.22813 · Cited by 38 · see citing works
Hippocampal neural activity reflects the economy of choices during goal‐directed navigation
Tryon, V. L., Penner, M. R., Heide, S. W., King, H. O., Larkin, J. D., & Mizumori, S. J. Y. (2017) · Hippocampus · doi:10.1002/hipo.22720 · Cited by 37 · see citing works
Kaut, K. P., Bunsey, M. D., & Riccio, D. C. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.2.304 · Cited by 35 · see citing works
Internal representation of hippocampal neuronal population spans a time-distance continuum
Haimerl, C., Angulo‐García, D., Villette, V., Reichinnek, S., Torcini, A., Cossart, R., & Malvache, A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1718518116 · Cited by 30 · see citing works
Suzuki, T., Kodama, S., Hoshino, C., Izumi, T., & Miyakawa, H. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06324.x · Cited by 29 · see citing works
Neural Signals Related to Outcome Evaluation Are Stronger in CA1 than CA3
Lee, S.-H., Huh, N., Lee, J. W., Ghim, J.-W., Lee, I., & Jung, M. W. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00040 · Cited by 29 · see citing works
Shan, K. Q., Lubenov, E. V., Papadopoulou, M., & Siapas, A. G. (2016) · eLife · doi:10.7554/elife.14321 · Cited by 27 · see citing works
Vector Grammar, Places, and the Functional Role of the Spatial Prepositions in English
O’Keefe, J. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199260195.003.0004 · Cited by 27 · see citing works
Self-citationZynyuk, L., Huxter, J. R., Muller, R. U., & Fox, S. E. (2011) · Hippocampus · doi:10.1002/hipo.20977 · Cited by 24 · see citing works
Rhinal cortex lesions impair simultaneous olfactory discrimination learning in rats.
Otto, T., & Garruto, D. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.5.1146 · Cited by 18 · see citing works
Cole, E., Ziadé, J., Simundic, A., & Mumby, D. G. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112450 · Cited by 16 · see citing works
A TEST OF THE TIME ESTIMATION HYPOTHESIS OF PLACE CELL GOAL-RELATED ACTIVITY
Hok, V., Lenck‐Santini, P., Save, É., Gaussier, P., Banquet, J. P., & Poucet, B. (2007) · Journal of Integrative Neuroscience · doi:10.1142/s0219635207001611 · Cited by 12 · see citing works
Spatial navigation on the radial maze with trial-unique intramaze cues and restricted extramaze cues
Babb, S. J., & Crystal, J. D. (2003) · Behavioural Processes · doi:10.1016/s0376-6357(03)00125-6 · Cited by 11 · see citing works
Impaired hippocampal activity at the goal zone on the place preference task in a DISC1 mouse model
Hayashi, Y., Sawa, A., & Hikida, T. (2015) · Neuroscience Research · doi:10.1016/j.neures.2015.10.005 · Cited by 11 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [11]Cohen NJ, Eichenbaum H. Memory, Amnesisa and the Hippocampal System. Cambridge, MA: MIT Press, 1993.
- [81]O’Keefe J. Hippocampal neurophysiology in the behaving animal. In: The Hippocampus Book, edited by Andersen P, Morris R, Amaral D, Bliss T., O’Keefe J. New York: Oxford University Press, 2007, p. 471– 544.
Cited by
Sorted by citations
Spatial goal coding in the hippocampal formation
Nyberg, N., Duvelle, É., Barry, C., & Spiers, H. J. (2022) · Neuron · doi:10.1016/j.neuron.2021.12.012 · Cited by 141 · see citing works
Neurophysiology of Remembering
Buzsáki, G., McKenzie, S., & Davachi, L. (2022) · Annual Review of Psychology · doi:10.1146/annurev-psych-021721-110002 · Cited by 84 · see citing works
Place and behavioral modulation of hippocampal neurons during immobility
Sartorato, N., Zouridis, I. S., Narantsatsralt, U.-U., Blanco-Hernández, E., & Burgalossi, A. (2026) · Nature Communications · doi:10.1038/s41467-026-75492-w · Cited by 1 · 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
- O’Keefe, J., & Krupic, J.
- Affiliations
- Sainsbury Wellcome Centre and Department of Cell and Developmental Biology, University College London, London, United Kingdom
- University of Cambridge (GB)
- ORCID
- Krupic, Julija
- Venue
- Physiological Reviews
- Publisher
- American Physiological Society
- Published
- 2021-07-01
- Volume
- 101
- Issue
- 3
- Pages
- 1427-1456
- ISSN
- 0031-9333 (ISSN-L)
- 1522-1210
- PMC
- PMC8490123
- OpenAlex
- W3132482678
- Cited by
- 93
- References
- 136
- Citations by year
- 2026: 11 · 2025: 24 · 2024: 21 · 2023: 11 · 2022: 18 · 2021: 8
- FWCI
- 2.12
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Physiological Reviews (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Apollo
- Funders
- Wellcome Trust (203020/Z/16/Z, 090843/F/09/Z)
- Gatsby Charitable Foundation (GAT3361)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- hippocampal pyramidal neurons, hippocampal function, spatial representation, single-unit responses, location dependence, rodent hippocampus, object recognition, reward, time
- MeSH terms
- Place Cells, Animals, Hippocampus, Memory, Pyramidal Cells
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.
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