Study of CA1 place cell activity and exploratory behavior following spatial and nonspatial changes in the environment
Abstract
Changes in the spatial arrangement or identity of objects inside a familiar environment induce reexploration. The present study looks at modifications of place cell activity during such renewed exploration. Hungry rats foraged for food in a cylinder with a salient cue card attached to the wall and with two distinct objects at fixed positions on the floor relative to each other and to the cue card. Once a set of CA1 place cells was recorded in this standard configuration, additional sessions were done after two kinds of manipulation. In the first, the two objects were rotated as a rigid set 90 degrees counterclockwise around the cylinder center while leaving the cue card in place; this was considered a spatial change. The effects of rotating the objects were different for fields near the objects (near fields) and fields far from the objects (far fields). Object rotation altered most near fields in complex ways, including remapping and cessation of firing. Near fields that remained intact after object rotation underwent unpredictable rotations that frequently departed considerably from the expected value of 90 degrees CCW. In contrast, the only change induced in far fields was a reduction of discharge rate on day 1, but not day 2, exposures of the rat to the rotated objects. The effects on both near and far fields were reversed when the objects were returned to their standard position. In the second manipulation, substitution of one of the two familiar objects with a novel object, a nonspatial change, had no detectable effect on place cell activity, regardless of field location. The sensitivity of hippocampal place cells to spatial changes but not to nonspatial changes is in agreement with earlier results showing that hippocampal lesions abolish reexploration after spatial but not after nonspatial object manipulations. The fact that reexploration is accompanied by place cell changes after spatial but not nonspatial changes reinforces the role that the hippocampus is believed to play in navigational computing and is perfectly compatible with the idea that another brain structure, likely perirhinal cortex, is responsible for object recognition.
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?
When the location of two objects was rotated, the CA1 firing pattern remapped, suggesting that the CA1 coordinated the altered spatial information.
“Electrophysiological recordings of the hippocampal CA1 cells have shown that when the location of two objects was rotated, the CA1 firing pattern remapped, suggesting that the CA1 coordinated the altered spatial information (Lenck-Santini et al., 2005).”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Lenck-Santini et al., 2005
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
Place navigation impaired in rats with hippocampal lesions
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982) · Nature · doi:10.1038/297681a0 · Cited by 6,340 · 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
Spatial localization does not require the presence of local cues
Morris, R. G. M. (1981) · Learning and Motivation · doi:10.1016/0023-9690(81)90020-5 · Cited by 2,699 · see citing works
The Hippocampus as a Cognitive Map
Ranck, J. B. (1979) · American Journal of Psychiatry · doi:10.1176/ajp.136.10.1353 · Cited by 2,373 · see citing works
Dynamics of the Hippocampal Ensemble Code for Space
Wilson, M. A., & McNaughton, B. L. (1993) · Science · doi:10.1126/science.8351520 · Cited by 2,350 · see citing works
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
The 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
Self-citationRecognition memory: What are the roles of the perirhinal cortex and hippocampus?
Brown, M. W., & Aggleton, J. P. (2001) · Nature reviews. Neuroscience · doi:10.1038/35049064 · Cited by 1,555 · see citing works
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
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
Self-citationA triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum.
McDonald, R. J., & White, N. M. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.1.3 · Cited by 885 · see citing works
Impaired Recognition Memory in Rats after Damage to the Hippocampus
Clark, R. E., Zola, S. M., & Squire, L. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-23-08853.2000 · Cited by 740 · 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
Impaired Hippocampal Representation of Space in CA1-Specific NMDAR1 Knockout Mice
McHugh, T. J., Blum, K. I., Tsien, J. Z., Tonegawa, S., & Wilson, M. A. (1996) · Cell · doi:10.1016/s0092-8674(00)81828-0 · Cited by 593 · 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
Packard, M. G., & McGaugh, J. L. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.3.439 · Cited by 555 · see citing works
Packard, M. G., & McGaugh, J. L. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.3.439 · Cited by 528 · 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
Abolition of Long-Term Stability of New Hippocampal Place Cell Maps by NMDA Receptor Blockade
Kentros, C., Hargreaves, E., Hawkins, R. D., Kandel, E. R., Shapiro, M., & Muller, R. V. (1998) · Science · doi:10.1126/science.280.5372.2121 · Cited by 484 · see citing works
Self-citationOn the delay-dependent involvement of the hippocampus in object recognition memory
HAMMOND, R. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.03.005 · Cited by 476 · see citing works
Different Contributions of the Hippocampus and Perirhinal Cortex to Recognition Memory
Wan, H., Aggleton, J. P., & Brown, M. W. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-03-01142.1999 · Cited by 449 · see citing works
Spatial memory and radial arm maze performance of rats
Olton, D. S., Collison, C., & Werz, M. A. (1977) · Learning and Motivation · doi:10.1016/0023-9690(77)90054-6 · Cited by 400 · see citing works
Skaggs, W. E., & McNaughton, B. L. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08455.1998 · Cited by 287 · see citing works
A Double Dissociation between Hippocampal Subfields
Lee, I., Rao, G., & Knierim, J. J. (2004) · Neuron · doi:10.1016/j.neuron.2004.05.010 · Cited by 236 · see citing works
Rotenberg, A., Mayford, M. R., Hawkins, R. D., Kandel, E. R., & Muller, R. U. (1996) · Cell · doi:10.1016/s0092-8674(00)81829-2 · Cited by 234 · see citing works
Self-citationFailure of Centrally Placed Objects to Control the Firing Fields of Hippocampal Place Cells
Cressant, A., Muller, R. U., & Poucet, B. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02531.1997 · Cited by 210 · see citing works
Self-citationDiscordance of spatial representation in ensembles of hippocampal place cells
Tanila, H., Shapiro, M. L., & Eichenbaum, H. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:6 · Cited by 195 · see citing works
Knierim, J. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-14-06254.2002 · Cited by 193 · see citing works
A driveable bundle of microwires for collecting single-unit data from freely-moving rats
Kubie, J. L. (1984) · Physiology & Behavior · doi:10.1016/0031-9384(84)90080-5 · Cited by 191 · see citing works
Cho, Y. H., Giese, K. P., Tanila, H., Silva, A. J., & Eichenbaum, H. (1998) · Science · doi:10.1126/science.279.5352.867 · Cited by 189 · see citing works
Spatial firing correlates of neurons in the hippocampal formation of freely moving rats
Muller, R. U., Kubie, J., Bostock, E., Taube, J. S., & Quirk, G. (1991) · doi:10.1093/oso/9780198542841.003.0017 · Cited by 173 · see citing works
Self-citationA study of exploratory behavior as an index of spatial knowledge in hamsters
Poucet, B., Chapuis, N., Durup, M., & Thinus‐Blanc, C. (1986) · Animal Learning & Behavior · doi:10.3758/bf03200043 · Cited by 162 · see citing works
Self-citationRetrograde 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
A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum.
McDonald, R., & White, N. (1993) · Behavioral Neuroscience · doi:10.1037/a0034883 · Cited by 146 · see citing works
Hetherington, P. A., & Shapiro, M. L. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.1.20 · Cited by 143 · see citing works
Blocking in the spatial domain.
Rodrigo, T., Chamizo, V. D., McLaren, I. P. L., & Mackintosh, N. J. (1997) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.23.1.110 · Cited by 141 · see citing works
Galani, R., Weiss, I. C., Cassel, J., & Kelche, C. R. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00197-6 · Cited by 135 · see citing works
Preserved performance in a hippocampal‐dependent spatial task despite complete place cell remapping
Jeffery, K. J., Gilbert, A., Burton, S., & Strudwick, A. (2003) · Hippocampus · doi:10.1002/hipo.10047 · Cited by 134 · see citing works
Sharp, P. E. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:4 · Cited by 125 · see citing works
The hippocampus and long-term object memory in the rat
Vnek, N., & Rothblat, L. A. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02780.1996 · Cited by 113 · see citing works
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 · see citing works
Self-citationSave, É., Buhot, M.-C., Foreman, N., & Thinus‐Blanc, C. (1992) · Behavioural Brain Research · doi:10.1016/s0166-4328(05)80118-4 · Cited by 106 · see citing works
Relationships between Place Cell Firing Fields and Navigational Decisions by Rats
Lenck‐Santini, P., Muller, R. U., Save, É., & Poucet, B. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-20-09035.2002 · Cited by 104 · see citing works
Self-citationEvidence for a relationship between place‐cell spatial firing and spatial memory performance
Lenck‐Santini, P., Save, É., & Poucet, B. (2001) · Hippocampus · doi:10.1002/hipo.1052 · Cited by 98 · see citing works
Self-citationConjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli
Fenton, A. A., Csizmadia, G., & Muller, R. U. (2000) · The Journal of General Physiology · doi:10.1085/jgp.116.2.191 · Cited by 96 · see citing works
Self-citationA study of spatial parameters encoded during exploration in hamsters.
Thinus‐Blanc, C., Bouzouba, L., Chaix, K., et al. (1987) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.13.4.418 · Cited by 87 · see citing works
Stupien, G., Florian, C., & Roullet, P. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(03)00022-4 · Cited by 81 · see citing works
Muscarinic Blockade Slows and Degrades the Location-Specific Firing of Hippocampal Pyramidal Cells
Brazhnik, E. S., Muller, R. U., & Fox, S. E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-02-00611.2003 · Cited by 78 · see citing works
Self-citationBlocking in the spatial domain.
Rodrigo, T., Chamizo, V. D., McLaren, I. P. L., et al. (1997) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.23.1.110 · Cited by 74 · see citing works
A Neural Systems Analysis of Adaptive Navigation
Mizumori, S. J. Y., Cooper, B. G., Leutgeb, S., & Pratt, W. E. (2000) · Molecular Neurobiology · doi:10.1385/mn:21:1-2:057 · Cited by 71 · see citing works
Brown, J. E., & Skaggs, W. E. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.4.1605 · Cited by 40 · see citing works
Spatial problem solving by rats: Exploration and cognitive maps
Ellen, P., Parko, E. M., Wages, C., et al. (1982) · Learning and Motivation · doi:10.1016/0023-9690(82)90030-3 · Cited by 36 · see citing works
The Neural Correlates of Navigation: Do Head Direction and Place Cells Guide Spatial Behavior?
Muir, G. M., & Taube, J. S. (2002) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582302238339 · Cited by 34 · see citing works
Huxter, J. R., Thorpe, C. M., Martin, G. M., & Harley, C. W. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00194-2 · Cited by 19 · see citing works
Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways.
Lavenex (2000) · Pure Amsterdam UMC · doi:10.1002/1098-1063(2000)10:4 · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
<i>Spatial Cognition and the Brain</i>
Burgess, N. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1440.002 · Cited by 614 · 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
The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation
Finnie, P. S. B., & Nader, K. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.008 · Cited by 189 · see citing works
Chao, O. Y., de Souza Silva, M. A., Yang, Y.-M., & Huston, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.007 · Cited by 158 · see citing works
Knierim, J. J., & Hamilton, D. A. (2011) · Physiological Reviews · doi:10.1152/physrev.00021.2010 · Cited by 148 · see citing works
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 · see citing works
Larkin, M. C., Lykken, C., Tye, L. D., Wickelgren, J. G., & Frank, L. M. (2014) · Hippocampus · doi:10.1002/hipo.22268 · Cited by 110 · see citing works
Barbosa, F. F., de Oliveira Pontes, I. M., Ribeiro, S., Ribeiro, A. M., & Silva, R. H. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.022 · Cited by 71 · see citing works
c-Fos expression correlates with performance on novel object and novel place recognition tests
Mendez, M., Arias, N., Uceda, S., & Arias, J. L. (2015) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2015.07.004 · Cited by 54 · see citing works
- Authors
- Lenck-Santini, P.-P., Rivard, B., Muller, R. U., & Poucet, B.
- Affiliations
- University of Bristol (GB)
- SUNY Downstate Health Sciences University (US)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Poucet, B.
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2005
- Volume
- 15
- Issue
- 3
- Pages
- 356-369
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W2109182337
- Cited by
- 81
- References
- 58
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 2 · 2023: 2 · 2022: 3 · 2021: 2 · 2020: 5 · 2019: 1 · 2018: 2 · 2017: 1 · 2016: 3 · 2015: 4 · 2014: 7 · 2013: 6 · 2012: 3
- FWCI
- 2.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- HAL AMU (submittedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Funders
- National Institutes of Health (5r01ns037150-04)
- National Institute of Neurological Disorders and Stroke (NS 20686, NS37150, R01NS020686)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- place cells, hippocampal CA1, re-exploration, spatial change, object rotation, remapping, perirhinal cortex, object recognition, spatial memory
- MeSH terms
- Action Potentials, Animals, Exploratory Behavior, Hippocampus, Male, Neurons, Neuropsychological Tests, Orientation, Photic Stimulation, Space Perception, Rats, Long-Evans, 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
