Differential roles of the dorsal hippocampal regions in the acquisition of spatial and temporal aspects of episodic-like memory

Barbosa, Flávio Freitas; de Oliveira Pontes, Isabella Maria; Ribeiro, Sidarta; Ribeiro, Alessandra Mussi; Silva, Regina Helena

doi:10.1016/j.bbr.2012.04.022

Cited by 71Memory and Neural MechanismsMemory Processes and InfluencesNeurogenesis and neuroplasticity mechanisms

Differential roles of the dorsal hippocampal regions in the acquisition of spatial and temporal aspects of episodic-like memory

Open access

Barbosa, Flávio Freitas, de Oliveira Pontes, Isabella Maria, Ribeiro, Sidarta, Ribeiro, Alessandra Mussi, Silva, Regina Helena·2012·Behavioural Brain Research

DOI 10.1016/j.bbr.2012.04.022

Open this paper in CoChat — free account

Abstract

Episodic memory refers to the recollection of what, where and when an event occurred. Computational models suggest that the dentate gyrus (DG) and the CA3 hippocampal subregions are involved in pattern separation and the rapid acquisition of episodes, while CA1 is involved in the formation of a temporal context. Most of the studies performed to test this hypothesis failed to simultaneously address the aspects of episodic memory. Recently, a new task of object recognition was validated in rats. In the first sample trial, the rat is exposed to four copies of an object. In second sample, the rat is exposed to four copies of a different object. In the test trial, two copies of each of the previous objects are presented. One copy of the object used in sample trial one is located in a different place, and it is expected to be the most explored. Our goal was to evaluate whether the pharmacological inactivation of the dorsal DG/CA3 and CA1 subregions could differentially impair the acquisition of the task. Inactivation of the DG/CA3 subregions impaired the spatial discrimination, while the temporal discrimination was preserved. Rats treated with muscimol in CA1 explored all the objects equally well, irrespective of place or presentation time. Our results are consistent with computational models that postulate a role for DG/CA3 in rapid encoding and in spatial pattern separation, and a role for CA1 in the in the formation of the temporal context of events and as well as in detecting spatial novelty.

Integrity signals

Registry

Crossref · 10.1016/j.bbr.2012.04.022

Cites

44 of 44 references verified0 citation errors · 0 not checkable

Statistics

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

Claims the paper makes

We couldn’t retrieve this paper’s full text, 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?

Inactivation of the CA3/dentate gyrus spared the when component but not the where component.
“inactivation of the CA3/dentate gyrus spared the when component, but not the where component”
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 Barbosa et al., 2012
Pharmacological muscimol microinjections into the hippocampal CA1 area disrupted the where and when components.
“Pharmacological muscimol microinjections into the hippocampal CA1area disrupted the where and when components”
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 Barbosa et al., 2012

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
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
Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory
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
Episodic memory: from mind to brain
Tulving, E. (2002) · Annual Review of Psychology · doi:10.1146/annurev.psych.53.100901.135114 · Cited by 4,950 · see citing works
Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus
Leutgeb, J. K., Leutgeb, S., Moser, M.-B., & Moser, E. I. (2007) · Science · doi:10.1126/science.1135801 · Cited by 1,601 · see citing works
Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach
Norman, K. A., & O'Reilly, R. C. (2003) · Psychological Review · doi:10.1037/0033-295x.110.4.611 · Cited by 1,312 · see citing works
Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts
Mumby, D. G., Gaskin, S., Glenn, M. J., Schramek, T. E., & Lehmann, H. (2002) · Learning & Memory · doi:10.1101/lm.41302 · Cited by 714 · see citing works
Can animals recall the past and plan for the future?
Clayton, N. S., Bussey, T. J., & Dickinson, A. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1180 · Cited by 658 · see citing works
Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1
Gilbert, P. E., Kesner, R. P., & Lee, I. (2001) · Hippocampus · doi:10.1002/hipo.1077 · Cited by 641 · 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
Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition
Dix, S. L., & Aggleton, J. P. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00079-5 · Cited by 598 · see citing works
Object recognition memory: Neurobiological mechanisms of encoding, consolidation and retrieval
Winters, B. D., Saksida, L. M., & Bussey, T. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.04.004 · Cited by 574 · see citing works
Loss of Recent Memory After Bilateral Hippocampal Lesions
Scoville, W. B., & Milner, B. A. (2000) · Journal of Neuropsychiatry · doi:10.1176/jnp.12.1.103-a · Cited by 546 · see citing works
Episodic memory and common sense: how far apart?
Tulving, E. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2001.0937 · Cited by 536 · 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
Hippocampal Inactivation Disrupts the Acquisition and Contextual Encoding of Fear Extinction
Corcoran, K., Desmond, T., Frey, K., & Maren, S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2246-05.2005 · Cited by 390 · see citing works
Hippocampal and neocortical contributions to memory: advances in the complementary learning systems framework
O'Reilly, R. C., & Norman, K. A. (2002) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(02)02005-3 · Cited by 351 · see citing works
Evolution of declarative memory
Manns, J. R., & Eichenbaum, H. (2006) · Hippocampus · doi:10.1002/hipo.20205 · Cited by 345 · see citing works
A computational theory of episodic memory formation in the hippocampus
Rolls, E. T. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.03.027 · Cited by 271 · see citing works
The role of hippocampal subregions in detecting spatial novelty
Lee, I., Hunsaker, M. R., & Kesner, R. P. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.145 · Cited by 270 · see citing works
Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours
Forwood, S., Winters, B. D., & Bussey, T. J. (2004) · Hippocampus · doi:10.1002/hipo.20059 · Cited by 259 · see citing works
Encoding, consolidation, and retrieval of contextual memory: Differential involvement of dorsal CA3 and CA1 hippocampal subregionsPreprint
Daumas, S., Halley, H., Francès, B., & Lassalle, J. (2005) · Learning & Memory · doi:10.1101/lm.81905 · Cited by 259 · see citing works
Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat
Bussey, T. J., Duck, J., Muir, J. L., & Aggleton, J. P. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00155-8 · Cited by 252 · see citing works
The role of the dentate gyrus, CA3a,b, and CA3c for detecting spatial and environmental novelty
Hunsaker, M. R., Rosenberg, J. S., & Kesner, R. P. (2008) · Hippocampus · doi:10.1002/hipo.20464 · Cited by 252 · 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
Episodic-like memory in mice: Simultaneous assessment of object, place and temporal order memory
Dere, E., Huston, J. P., & Silva, M. A. D. S. (2005) · Brain Research Protocols · doi:10.1016/j.brainresprot.2005.08.001 · Cited by 242 · see citing works
Glutamate Receptors in Perirhinal Cortex Mediate Encoding, Retrieval, and Consolidation of Object Recognition Memory
Winters, B. D., & Bussey, T. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0480-05.2005 · Cited by 214 · see citing works
Reversible Inactivation of the Hippocampal Mossy Fiber Synapses in Mice Impairs Spatial Learning, but neither Consolidation nor Memory Retrieval, in the Morris Navigation Task
Lassalle, J., Bataille, T., & Halley, H. (2000) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1999.3931 · Cited by 213 · see citing works
The case for episodic memory in animals
Dere, E., KARTTEKE, E., Huston, J. P., & DESOUZASILVA, M. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.09.005 · Cited by 202 · see citing works
Imaging the spread of reversible brain inactivations using fluorescent muscimol
Allen, T. A., Narayanan, N. S., Kholodar-Smith, D. B., Zhao, Y., Laubach, M., & Brown, T. H. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2008.01.033 · Cited by 187 · see citing works
Distinct contributions of the hippocampus and medial prefrontal cortex to the “what–where–when” components of episodic-like memory in mice
DeVito, L. M., & Eichenbaum, H. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.09.014 · Cited by 164 · see citing works
Muscimol Diffusion after Intracerebral Microinjections: A Reevaluation Based on Electrophysiological and Autoradiographic Quantifications
Edeline, J., Hars, B., Hennevin, E., & Cotillon, N. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4035 · Cited by 157 · see citing works
Role of CA3 and CA1 subregions of the dorsal hippocampus on temporal processing of objects
Hoge, J., & Kesner, R. P. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.04.013 · Cited by 156 · see citing works
Context- but not familiarity-dependent forms of object recognition are impaired following excitotoxic hippocampal lesions in rats.
Good, M. A., Barnes, P., Staal, V., McGregor, A., & Honey, R. C. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.1.218 · Cited by 134 · see citing works
Evaluating the differential roles of the dorsal dentate gyrus, dorsal CA3, and dorsal CA1 during a temporal ordering for spatial locations task
Hunsaker, M. R., & Kesner, R. P. (2008) · Hippocampus · doi:10.1002/hipo.20455 · Cited by 133 · see citing works
The temporal attributes of episodic memory
Kesner, R. P., & Hunsaker, M. R. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.029 · Cited by 102 · see citing works
Electrolytic lesions of dorsal CA3 impair episodic-like memory in rats
Li, J., & Chao, Y.-S. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.06.006 · Cited by 97 · see citing works
Involvement of the hippocampal CA3-region in acquisition and in memory consolidation of spatial but not in object information in mice
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
Study of CA1 place cell activity and exploratory behavior following spatial and nonspatial changes in the environment
Lenck-Santini, P.-P., Rivard, B., Muller, R. U., & Poucet, B. (2005) · Hippocampus · doi:10.1002/hipo.20060 · Cited by 81 · see citing works
Pharmacological Manipulation of Neuronal Ensemble Activity by Reverse Microdialysis in Freely Moving Rats: A Comparative Study of the Effects of Tetrodotoxin, Lidocaine, and Muscimol
van Duuren, E., Plasse, G., van der Blom, R., Joosten, R. N. J. M. A., Mulder, A. B., Pennartz, C. M. A., & Feenstra, M. G. P. (2007) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.124784 · Cited by 78 · see citing works
Dorsal hippocampal N-methyl-d-aspartate receptors underlie spatial working memory performance during non-matching to place testing on the T-maze
McHugh, S. B., Niewoehner, B., Rawlins, J. N. P., & Bannerman, D. M. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.07.021 · Cited by 72 · see citing works
Activation of metabotropic glutamate receptor type 2/3 supports the involvement of the hippocampal mossy fiber pathway on contextual fear memory consolidationPreprint
Daumas, S., Ceccom, J., Halley, H., Francès, B., & Lassalle, J. (2009) · Learning & Memory · doi:10.1101/lm.1418309 · Cited by 47 · see citing works
Extending possible applications of an episodic-like memory task in rats
Barbosa, F. F., Pontes, I. M. D. O., Ribeiro, A. M., & Silva, R. H. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.11.028 · Cited by 23 · see citing works
Self-citation

Flagged first, then by citations

Sorted by citations

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
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
Episodic Memory in Nonhuman Animals
Templer, V. L., & Hampton, R. R. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.016 · Cited by 94 · see citing works
CA1 hippocampal network activity changes during sleep-dependent memory consolidation
Ognjanovski, N., Maruyama, D., Lashner, N., Zochowski, M., & Aton, S. J. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00061 · Cited by 81 · see citing works
Differential cortical c-Fos and Zif-268 expression after object and spatial memory processing in a standard or episodic-like object recognition task
Barbosa, F. F., Santos, J. R., Meurer, Y. S. R., Macêdo, P. T., Ferreira, L. M. S., Pontes, I. M. O., Ribeiro, A. M., & Silva, R. H. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00112 · Cited by 79 · 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
Voluntary exercise followed by chronic stress strikingly increases mature adult-born hippocampal neurons and prevents stress-induced deficits in’ what-when-where’ memory
Castilla-Ortega, E., Rosell-Valle, C., Pedraza, C., Rodríguez de Fonseca, F., Estivill-Torrús, G., & Santín, L. J. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.12.001 · Cited by 41 · see citing works
Interaction between the medial prefrontal cortex and hippocampal CA1 area is essential for episodic-like memory in rats
Chao, O. Y., Nikolaus, S., Lira Brandão, M., Huston, J. P., & de Souza Silva, M. A. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.03.019 · Cited by 38 · see citing works
CA1 inactivation impairs episodic-like memory in rats
Drieskens, D. C., Neves, L. R., Pugliane, K. C., de Souza, I. B. M. B., Lima, Á. D. C., Salvadori, M. G. D. S. S., Ribeiro, A. M., Silva, R. H., & Barbosa, F. F. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.08.008 · Cited by 31 · see citing works
Self-citation
Two distinct ways to form long-term object recognition memory during sleep and wakefulness
Sawangjit, A., Harkotte, M., Oyanedel, C. N., Niethard, N., Born, J., & Inostroza, M. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2203165119 · Cited by 28 · see citing works

Connectional Specification of Regenerating Entorhinal Projection Neuron Classes Cannot Be Overridden by Altered Target Availability in Postnatal Organotypic Slice Co-culture
Li, D., Field, P., & Raisman, G. (1996) · Experimental Neurology · doi:10.1006/exnr.1996.0186 · Cited by 21 · see citing works
Effect of the infusion of the GABA-A receptor agonist, muscimol, on the role of the entorhinal cortex, amygdala, and hippocampus in memory processes
Jersalinsky, D., Quillfeldt, J. A., Walz, R., da Silva, R. C., Silva, M. B. E., Bianchin, M. M., Schmitz, P. K., Zanatta, M. S., Ruschel, A. C., Paczko, N., et al. (1994) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(05)80066-4 · Cited by 33 · see citing works
Self-citation
Entorhinal cortex of the rat: Organization of intrinsic connections
Dolorfo, C. L., & Amaral, D. G. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980817)398:1 · Cited by 268 · see citing works
The expression of a fucosyl-ganglioside in the molecular layer of the dentate gyrus following entorhinal cortical lesions
Suchy, S. F., Schwarting, G. A., Lehco, B., et al. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90347-v · Cited by 7 · see citing works
Loss of synapses in the entorhinal‐dentate gyrus pathway following repeated induction of electroshock seizures in the rat
Cardoso, A., Assunção, M., Andrade, J. P., Pereira, P. A., Madeira, M. D., Paula‐Barbosa, M. M., & Lukoyanov, N. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21474 · Cited by 31 · see citing works

Authors: Barbosa, F. F., de Oliveira Pontes, I. M., Ribeiro, S., Ribeiro, A. M., & Silva, R. H.
Affiliations: Universidade Federal do Rio Grande do Norte (BR)
Corresponding author: Silva, Regina Helena
ORCID: Barbosa, Flávio Freitas
Ribeiro, Sidarta
Ribeiro, Alessandra Mussi
Silva, Regina Helena
Venue: Behavioural Brain Research
Publisher: Elsevier BV
Published: 2012-06
Volume: 232
Issue: 1
Pages: 269-277
ISSN: 0166-4328 (ISSN-L)
DOI: 10.1016/j.bbr.2012.04.022
OpenAlex: W2033499925
Cited by: 71
References: 44
Citations by year: 2026: 3 · 2024: 3 · 2023: 3 · 2022: 12 · 2021: 6 · 2020: 5 · 2019: 3 · 2018: 8 · 2017: 5 · 2016: 2 · 2015: 7 · 2014: 8 · 2013: 6
FWCI: 3.44
Type: journal article
Language: en
Open access: green
repositorio.ufrn.br
Licence: other-oa
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Behavioural Brain Research (publishedVersion)
PubMed (publishedVersion)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
Americanae (AECID Library) (submittedVersion, other-oa)
Funders: Fundação de Apoio à Pesquisa do Rio Grande do Norte
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Conselho Nacional de Desenvolvimento Científico e Tecnológico
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: episodic-like memory, dorsal hippocampus, dentate gyrus, CA3, CA1, spatial discrimination, temporal discrimination, object recognition memory, muscimol inactivation, pattern separation, temporal context, rats
MeSH terms: Analysis of Variance, Animals, Behavior, Animal, Data Interpretation, Statistical, Exploratory Behavior, Hippocampus, Injections, Male, Muscimol, Space Perception, Stereotaxic Techniques, Time Perception, Rats, Wistar, GABA Agonists, Rats, Long-Evans, Rats, CA1 Region, Hippocampal, CA3 Region, Hippocampal, Memory, Episodic

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

Differential roles of the dorsal hippocampal regions in the acquisition of spatial and temporal aspects of episodic-like memory

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks