Memory reconsolidation allows the consolidation of a concomitant weak learning through a synaptic tagging and capture mechanism
Abstract
Motivated by the synaptic tagging and capture (STC) hypothesis, it was recently shown that a weak learning, only able to produce short-term memory (STM), can succeed in establishing long-term memory (LTM) with a concomitant, stronger experience. This is consistent with the capture, by the first-tagged event, of the so-called plasticity-related proteins (PRPs) provided by the second one. Here, we describe how a concomitant session of reactivation/reconsolidation of a stronger, contextual fear conditioning (CFC) memory, allowed LTM to result from a weak spatial object recognition (wSOR) training. Consistent with an STC process, the effect was observed only during a critical time window and was dependent on the CFC reconsolidation-related protein synthesis. Retrieval by itself (without reconsolidation) did not have the same promoting effect. We also found that the inactivation of the NMDA receptor by AP5 prevented wSOR training to receive this support of CFC reconsolidation (supposedly through the production of PRPs), which may be the equivalent of blocking the setting of a learning tag in the dorsal CA1 region for that task. Furthermore, either a Water Maze reconsolidation, or a CFC extinction session, allowed the formation of wSOR-LTM. These results suggest for the first time that a reconsolidation session can promote the consolidation of a concomitant weak learning through a probable STC mechanism. These findings allow new insights concerning the influence of reconsolidation in the acquisition of memories of otherwise unrelated events during daily life situations.
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Pre-sample AP5 microinjections into the hippocampus impaired performance on OPP.
“Pre-sample AP5 microinjections into the hippocampus impaired performance on OPP”
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 Cassini et al., 2013
Cites
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
Synaptic Plasticity and Memory: An Evaluation of the Hypothesis
Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.649 · Cited by 2,794 · see citing works
Synaptic tagging and long-term potentiation
Frey, U., & Morris, R. G. M. (1997) · Nature · doi:10.1038/385533a0 · Cited by 1,736 · see citing works
Mechanisms of emotional arousal and lasting declarative memory.
Cahill, L., & McGaugh, J. L. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01214-9 · Cited by 1,575 · see citing works
Brown, R., & Kulik, J. (1977) · Cognition · doi:10.1016/0010-0277(77)90018-x · Cited by 1,373 · see citing works
Memory Reconsolidation and Extinction Have Distinct Temporal and Biochemical Signatures
Suzuki, A., Josselyn, S. A., Frankland, P. W., Masushige, S., Silva, A. J., & Kida, S. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5491-03.2004 · Cited by 1,127 · see citing works
Making memories last: the synaptic tagging and capture hypothesis
Redondo, R. L., & Morris, R. G. M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2963 · Cited by 792 · see citing works
Molecular mechanisms of memory reconsolidation
Tronson, N. C., & Taylor, J. R. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2090 · Cited by 783 · see citing works
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644 · see citing works
Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation
Frey, U., & Morris, R. G. M. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01189-2 · Cited by 615 · see citing works
Moncada, D., & Viola, H. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1083-07.2007 · Cited by 370 · see citing works
Immediate-Early Genes and Synaptic Function
Lanahan, A. A., & Worley, P. F. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3836 · Cited by 344 · see citing works
Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD
Sajikumar, S. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.03.003 · Cited by 341 · see citing works
Cellular and systems mechanisms of memory strength as a constraint on auditory fear reconsolidation
Wang, S., Alvares, L. D. O., & Nader, K. (2009) · Nature Neuroscience · doi:10.1038/nn.2350 · Cited by 305 · see citing works
Behavioral tagging is a general mechanism of long-term memory formation
Ballarini, F., Moncada, D., Martinez, M. C., Alen, N., & Viola, H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907078106 · Cited by 301 · see citing works
Memory formation, consolidation and transformation
Nadel, L., Hupbach, A., Gómez, R. L., & Newman-Smith, K. C. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.001 · Cited by 295 · see citing works
Wang, S.-H., Redondo, R. L., & Morris, R. G. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008638107 · Cited by 251 · see citing works
Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP
Frey, U., & Morris, R. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(98)00040-9 · Cited by 242 · see citing works
Retrieval per se is not sufficient to trigger reconsolidation of human fear memory
Sevenster, D., Beckers, T., & Kindt, M. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.01.009 · Cited by 238 · see citing works
Redondo, R. L., Okuno, H., Spooner, P. A., Frenguelli, B. G., Bito, H., & Morris, R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3140-09.2010 · Cited by 186 · see citing works
Moncada, D., Ballarini, F., Martinez, M. C., Frey, J. U., & Viola, H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104495108 · Cited by 171 · see citing works
Bustos, S. G., Maldonado, H., & Molina, V. A. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.75 · Cited by 168 · see citing works
Networks of neurons, networks of genes: An integrated view of memory consolidation
Miyashita, T., Kubík, Š., Lewandowski, G. A., & Guzowski, J. F. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.08.012 · Cited by 158 · see citing works
Opposite action of hippocampal CB1 receptors in memory reconsolidation and extinction
de Oliveira Alvares, L., Pasqualini Genro, B., Diehl, F., Molina, V. A., & Quillfeldt, J. A. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.05.005 · Cited by 143 · see citing works
Self-citationSuzuki, A., Mukawa, T., Tsukagoshi, A., Frankland, P. W., & Kida, S. (2008) · Learning & Memory · doi:10.1101/lm.888808 · Cited by 141 · see citing works
Frey, S., & Frey, J. U. (2008) · Progress in brain research · doi:10.1016/s0079-6123(07)00007-6 · Cited by 139 · see citing works
TrkB as a Potential Synaptic and Behavioral Tag
Lü, Y., Ji, Y., Ganesan, S., Schloesser, R. J., Martinowich, K., Sun, M., Mei, F., Chao, M. V., & Lu, B. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2707-11.2011 · Cited by 130 · see citing works
Sajikumar, S., & Körte, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016849108 · Cited by 126 · see citing works
Behavioral tagging of extinction learning
Myskiw, J. D. C., Benetti, F., & Izquierdo, I. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220875110 · Cited by 124 · see citing works
Retrieval induces hippocampal-dependent reconsolidation of spatial memoryPreprint
Rossato, J. I., Bevilaqua, L. R., Medina, J. H., Izquierdo, I., & Cammarota, M. (2006) · Learning & Memory · doi:10.1101/lm.315206 · Cited by 123 · see citing works
Alvares, L. D. O., Crestani, A. P., Cassini, L. F., Haubrich, J., Santana, F., & Quillfeldt, J. A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.04.005 · Cited by 105 · see citing works
Self-citationBehavioural memory reconsolidation of food and fear memories
Flavell, C. R., Barber, D. J., & Lee, J. L. C. (2011) · Nature Communications · doi:10.1038/ncomms1515 · Cited by 104 · see citing works
Bustos, S. G., Giachero, M., Maldonado, H., & Molina, V. A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.215 · Cited by 87 · see citing works
Young, J. Z., Isiegas, C., Abel, T. G., & Nguyen, P. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04707.x · Cited by 85 · see citing works
Barco, Á., de Armentia, M. L., & Alarcón, J. M. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.01.002 · Cited by 77 · see citing works
Almaguer‐Melian, W., Bergado, J. A., Fuentes, N. P., Alberti‐Amador, E., Mercerón‐Martínez, D., & Frey, J. U. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114198109 · Cited by 70 · see citing works
Periodically reactivated context memory retains its precision and dependence on the hippocampus
Alvares, L. D. O., Einarsson, E. Ö., Santana, F., Crestani, A. P., Haubrich, J., Cassini, L. F., Nader, K., & Quillfeldt, J. A. (2011) · Hippocampus · doi:10.1002/hipo.20983 · Cited by 67 · see citing works
Self-citationStress response recruits the hippocampal endocannabinoid system for the modulation of fear memoryPreprint
Alvares, L. D. O., Engelke, D. S., Diehl, F., Scheffer-Teixeira, R., Haubrich, J., Cassini, L. F., Molina, V. A., & Quillfeldt, J. A. (2010) · Learning & Memory · doi:10.1101/lm.1721010 · Cited by 61 · see citing works
Self-citationRetrieval induces reconsolidation of fear extinction memory
Rossato, J. I., Bevilaqua, L. R., Izquierdo, I., Medina, J. H., & Cammarota, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016254107 · Cited by 48 · see citing works
Retroactive hyperamnesia and other emotional effects on memory.
Stratton, G. M. (1919) · Psychological Review · doi:10.1037/h0074902 · Cited by 19 · see citing works
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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
Abnormal sleep spindles, memory consolidation, and schizophrenia
Manoach, D. S., & Stickgold, R. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050718-095754 · Cited by 157 · see citing works
Evidence of VTA and LC control of protein synthesis required for the behavioral tagging process
Moncada, D. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.06.003 · Cited by 50 · see citing works
- Authors
- Cassini, L. F., Sierra, R. O., Haubrich, J., Crestani, A. P., Santana, F., de Oliveira Alvares, L., & Quillfeldt, J. A.
- Affiliations
- Universidade Federal do Rio Grande do Sul (BR)
- Psychobiology and Neurocomputation Laboratory Biophysics Department Institute of Biosciences 91.501‐970
- ORCID
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2013-07-08
- Volume
- 23
- Issue
- 10
- Pages
- 931-941
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W1524250518
- Cited by
- 36
- References
- 40
- Citations by year
- 2025: 4 · 2024: 5 · 2023: 1 · 2022: 2 · 2021: 1 · 2020: 2 · 2019: 3 · 2018: 3 · 2017: 1 · 2016: 7 · 2015: 3 · 2014: 4
- FWCI
- 2.55
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- memory reconsolidation, synaptic tagging and capture, weak learning, long-term memory consolidation, contextual fear conditioning, NMDA receptor, AP5, protein synthesis, dorsal CA1, memory reactivation, memory extinction, water maze
- MeSH terms
- Animals, Behavior, Animal, Conditioning, Psychological, Extinction, Psychological, Fear, Learning, Male, Memory, Memory, Short-Term, Valine, Receptors, N-Methyl-D-Aspartate, Rats, Wistar, Maze Learning, Recognition, Psychology, Rats, CA1 Region, Hippocampal, Memory, Long-Term
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