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Memory Retrieval and the Passage of Time: From Reconsolidation and Strengthening to Extinction
Open accessAbstract
An established memory can be made transiently labile if retrieved or reactivated. Over time, it becomes again resistant to disruption and this process that renders the memory stable is termed reconsolidation. The reasons why a memory becomes labile after retrieval and reconsolidates still remains debated. Here, using inhibitory avoidance learning in rats, we provide evidence that retrievals of a young memory, which are accompanied by its reconsolidation, result in memory strengthening and contribute to its overall consolidation. This function associated to reconsolidation is temporally limited. With the passage of time, the stored memory undergoes important changes, as revealed by the behavioral outcomes of its retrieval. Over time, without explicit retrievals, memory first strengthens and becomes refractory to both retrieval-dependent interference and strengthening. At later times, the same retrievals that lead to reconsolidation of a young memory extinguish an older memory. We conclude that the storage of information is very dynamic and that its temporal evolution regulates behavioral outcomes. These results are important for potential clinical applications.
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“Similarly, older and stronger memories may require additional retrieval procedures for updating to take place (e.g. [135,136]), as do individual differences such as exposure to chronic stress and high trait anxiety [130,137].”
From Multiple memory systems, multiple time points: How science can inform treatment to control the expression of unwanted emotional memories (2018) · cites this paper as [135]
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“…is unique in that it provides an opportunity to erase (Agren et al., 2012; Clem and Huganir, 2010; Monfils, Cowansage, Klann, and LeDoux, 2009; Rao-Ruiz et al., 2011; Schiller et al., 2010) or modify (Chen et al., 2011; Inda, Muravieva, and Alberini, 2011; Lee, 2008; 2010) the existing memory.”
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“…using aversive Pavlovian conditioning paradigms utilizing both cued (Nader et al., 2000a) and contextual fear (Debiec et al., 2002; Lee, 2008), as well as conditioned taste aversion (CTA) (Garcia-Delatorre et al., 2010) and inhibitory avoidance (Boccia et al., 2005, 2011; Inda et al., 2011).”
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Self-citationAddiction: a drug-induced disorder of memory reconsolidation
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BackgroundSelf-citationTranslational Approaches Targeting Reconsolidation
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“Evidence now suggests that the reconsolidation process is involved in modification of established memories (Hupbach et al., 2007; Lukowiak et al., 2007; Lee, 2008, 2010; Inda et al., 2011).”
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“Of particular clinical interest is reconsolidation, the process by which memories can be made labile at the time of their reactivation [22, 23], and is therefore increasingly being used as a treatment target.”
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“Single trial CFC is known to produce a robust, longlasting memory, however subsequent training has been shown to strengthen the memory and prevent random association of shock with re-exposure [6-10].”
BackgroundFunction and mechanisms of memory destabilization and reconsolidation after retrieval
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Mindfulness-Based Stress Reduction, Fear Conditioning, and The Uncinate Fasciculus: A Pilot Study
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“First, we analyzed whether strengthening of the original memory by repeated labilization-reconsolidations maintained the memory available for longer periods of time [12].”
BackgroundInfluentialPropofol-induced deep sedation reduces emotional episodic memory reconsolidation in humans
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“Recent evidence suggests that retrieving a young memory multiple times over several days can lead to a strengthening of the memory trace (Inda et al. 2011).”
BackgroundInfluentialOn the transition from reconsolidation to extinction of contextual fear memories
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Steinmetz, A. B., Johnson, S. A., Iannitelli, D. E., Pollonini, G., & Alberini, C. M. (2016) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2016.04.006 · Cited by 49
“Given that memory retrieval (via testing) early following training can lead to memory strengthening through reconsolidation (Inda et al., 2011), a second group of young adult and aged rats underwent cannula implant, IA training, and IGF-2 or vehicle injections, but were tested for memory retention only once, at 14 day…”
BackgroundSelf-citationEspejo, P. J., Ortiz, V., Martijena, I. D., & Molina, V. A. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.06.033 · Cited by 51
Zou, G.-J., Chen, Z.-R., Wang, X., Cui, Y.-H., Li, F., Li, C.-Q., Wang, L.-F., & Huang, F. (2024) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2024.176759 · Cited by 51
Finsterwald, C., Steinmetz, A. B., Travaglia, A., & Alberini, C. M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0771-15.2015 · Cited by 50
“…or a deficit in memory retrieval or expression, we administered a reminder footshock (RS) in a different context that had no associations with the dark compartment, a procedure known to reinstate decreased threat memory responses such as that observed in extinction training (Inda et al., 2011).”
MethodSelf-citationUnderstanding the dynamic and destiny of memories
Alvares, L. D. O., & Monte, F. H. D. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.009 · Cited by 51
“Other studies using similar experimental designs have drawn the same conclusion by demonstrating that reactivation-induced reconsolidation strengthens the original memory trace (De Oliveira Alvares et al., 2013; Forcato et al., 2014; Inda et al., 2011).”
BackgroundResultAlaghband, Y., & Marshall, J. F. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2793-y · Cited by 47
“Despite the limitation that reconsolidation interference and enhanced extinction can both diminish reinstatement, primed reinstatement remains a useful means by which memories that undergo extinction can be distinguished from memories that are diminished by other processes (Brown et al. 2008; Fricks-Gleason and Marsha…”
InfluentialCorcoran, K. A., Leaderbrand, K., & Radulović, J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3338-13.2013 · Cited by 46
“These molecular and cellular alterations relevant for memory retrieval may impact retrieval-dependent processes that also change over time, such as fear extinction (Inda et al., 2011).”
BackgroundGluR2 endocytosis-dependent protein degradation in the amygdala mediates memory updating
Ferrara, N. C., Jarome, T. J., Cullen, P. K., Orsi, S. A., Kwapis, J. L., Trask, S., Pullins, S. E., & Helmstetter, F. J. (2019) · Scientific Reports · doi:10.1038/s41598-019-41526-1 · Cited by 47
Effects of learning experience on forgetting rates of item and associative memoriesPreprint
Yang, J., Zhan, L., Wang, Y., Du, X., Zhou, W., Ning, X., Sun, Q. Y., & Moscovitch, M. (2016) · Learning & Memory · doi:10.1101/lm.041210.115 · Cited by 51
Extinction learning, which consists of the inhibition of retrieval, can be learned without retrieval
Myskiw, J. D. C., Furini, C. R. G., Schmidt, B. E., Ferreira, F. F., & Izquierdo, I. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1423465112 · Cited by 48
“Almeida-Corrêa S, Amaral OB (2014) Memory labilization in reconsolidation and extinction: Evidence for a common plasticity system? J Physiol Paris 108(4-6):292–306.”
BackgroundEnhancing a declarative memory in humans: The effect of clonazepam on reconsolidation
Rodríguez, M. L. C., Campos, J., Forcato, C., Leiguarda, R., Maldonado, H., Molina, V. A., & Pedreira, M. E. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.059 · Cited by 41
“One of the functionalities proposed suggests that the labilizationereconsolidation process strengthens the original memory (Alberini, 2007; Inda et al., 2011).”
Fabbri, R., Furini, C. R. G., Passani, M. B., Provensi, G., Baldi, E., Bucherelli, C., Izquierdo, I., Myskiw, J. D. C., & Blandina, P. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1604841113 · Cited by 44
“De novo protein synthesis in the hippocampus at training is critical for the consolidation of IA memory (8, 35, 40), and local infusion of anisomycin around that time thwarts memory trace formation (35, 41).”
BackgroundNeuroscience of learning and memory for addiction medicine
Torregrossa, M. M., & Taylor, J. R. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.07.006 · Cited by 43
Contextual Information Drives the Reconsolidation-Dependent Updating of Retrieved Fear Memories
Jarome, T. J., Ferrara, N. C., Kwapis, J. L., & Helmstetter, F. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.161 · Cited by 51
NLGN1 and NLGN2 in the prefrontal cortex: their role in memory consolidation and strengthening
Katzman, A. C., & Alberini, C. M. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.12.003 · Cited by 43
Self-citationWells, A. M., Xie, X., Higginbotham, J. A., Arguello, A. A., Healey, K. L., Blanton, M. A., & Fuchs, R. A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.217 · Cited by 41
“The number of extinction training sessions was uniform to control for memory age, a strong predictor of a memory’s sensitivity to destabilization (Suzuki et al, 2004; Inda et al, 2011), at the time of memory reactivation.”
BackgroundThe curriculum prerequisite network: Modeling the curriculum as a complex system
Aldrich, P. R. (2015) · Biochemistry and Molecular Biology Education · doi:10.1002/bmb.20861 · Cited by 57
“The more steps there are separating two courses, the more opportunity there is for a student to forget material learned in the earlier course, unless there are opportunities later in the curriculum for reinforcement [47, 48].”
BackgroundHu, J., Baussi, O., Levine, A. T., Chen, Y., & Schacher, S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1358-11.2011 · Cited by 39
“DOI:10.1523/JNEUROSCI.1358-11.2011 Copyright © 2011 the authors 0270-6474/11/318841-10$15.00/0 Alberini, 2011; Inda et al., 2011) and suggest that activation of new and old molecular pathways by additional stimuli in neurons already expressing synaptic plasticity contribute to the enhancement of…”
BackgroundInfluentialSurís, A., Smith, J. C., Powell, C. M., & North, C. S. (2013) · Annals of Clinical Psychiatry · doi:10.1177/104012371302500106 · Cited by 40
Mystery of the memory engram: History, current knowledge, and unanswered questions
Lopez, M. R., Wasberg, S. M., Gagliardi, C. M., Normandin, M. E., & Muzzio, I. A. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105574 · Cited by 44
Divergent recruitment of developmentally defined neuronal ensembles supports memory dynamics
Kveim, V. A., Salm, L., Ulmer, T., Lahr, M., Kandler, S., Imhof, F., & Donato, F. (2024) · Science · doi:10.1126/science.adk0997 · Cited by 39
Krawczyk, M. C., Fernández, R. S., Pedreira, M. E., & Boccia, M. M. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.12.011 · Cited by 45
Potentiating mGluR5 function with a positive allosteric modulator enhances adaptive learningPreprint
Xu, J., Zhu, Y., Kraniotis, S., He, Q., Marshall, J. J., Nomura, T., Stauffer, S. R., Lindsley, C. W., Conn, P. J., & Contractor, A. (2013) · Learning & Memory · doi:10.1101/lm.031666.113 · Cited by 39
“triggers a reconsolidation process during which the memory becomes labile and susceptible to modifications (Nader et al. 2000; Sara 2000; Alberini 2005; Inda et al. 2011).”
Huynh, T. N., Santini, E., & Klann, E. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0878-14.2014 · Cited by 39
“It should be noted that there is evidence for reconsolidation as a memory-strengthening mechanism (Lee, 2008; Inda et al., 2011).”
Background
Metadata
- Authors
- Inda, M. C., Muravieva, E. V., & Alberini, C. M.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Corresponding author
- Alberini, Cristina M.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-02-02
- Volume
- 31
- Issue
- 5
- Pages
- 1635-1643
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3069643
- OpenAlex
- W2013517273
- Cited by
- 261
- References
- 57
- Citations by year
- 2026: 7 · 2025: 9 · 2024: 17 · 2023: 6 · 2022: 10 · 2021: 8 · 2020: 14 · 2019: 9 · 2018: 18 · 2017: 19 · 2016: 26 · 2015: 27 · 2014: 28 · 2013: 29 · 2012: 24
- FWCI
- 14.61
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH074736)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- memory reconsolidation, memory retrieval, memory enhancement, memory extinction, passive avoidance, memory consolidation, temporal dynamics of memory
- MeSH terms
- Animals, Avoidance Learning, Cycloheximide, Extinction, Psychological, Inhibition, Psychological, Injections, Intraperitoneal, Male, Memory, Neuropsychological Tests, Protein Synthesis Inhibitors, Mental Recall, Retention, Psychology, Time Factors, Protein Biosynthesis, Rats, Long-Evans, Rats
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