Memory Retrieval and the Passage of Time: From Reconsolidation and Strengthening to Extinction
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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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Older and stronger memories may require additional retrieval procedures for updating to take place, as do individual differences such as exposure to chronic stress and high trait anxiety.
“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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Fukushima, H., Zhang, Y., Archbold, G., Ishikawa, R., Nader, K., & Kida, S. (2014) · eLife · doi:10.7554/elife.02736 · Cited by 97 · see citing works
“Retrieval has been thought to have a role in enhancing memory that requires activation of gene expression and signal transduction pathways such as mTOR (Gordon, 1981; Nader et al., 2000; Nader and Hardt, 2009; Inda et al., 2011; Pedroso et al., 2013).”
BackgroundThy1-Expressing Neurons in the Basolateral Amygdala May Mediate Fear Inhibition
Jasnow, A. M., Ehrlich, D., Choi, D. C., Dabrowska, J., Bowers, M. E., McCullough, K. M., Rainnie, D. G., & Ressler, K. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5539-12.2013 · Cited by 92 · see citing works
“In the present study, mice were exposed to 15 CS tones over a period of 22 min, which is beyond what has been reported to initiate reconsolidation, but does initiate extinction (Pedreira and Maldonado, 2003; Suzuki et al., 2004; Bredy and Barad, 2008; PérezCuesta and Maldonado, 2009; Kirtley and Thomas, 2010; Inda et…”
BackgroundThe neurocircuitry of remote cued fear memory
Bergstrom, H. C. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.028 · Cited by 92 · see citing works
Repeated Labilization-Reconsolidation Processes Strengthen Declarative Memory in Humans
Forcato, C., Rodríguez, M. L. C., & Pedreira, M. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023305 · Cited by 90 · see citing works
“[28] tested whether reconsolidation mediates memory strengthening and its interaction with the passage of time.”
BackgroundResultInfluentialMeyer, F., & Louilot, A. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00118 · Cited by 84 · see citing works
“…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).”
MethodMechanisms of memory enhancement
Stern, S. A., & Alberini, C. M. (2012) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1196 · Cited by 86 · see citing works
Self-citationAddiction: a drug-induced disorder of memory reconsolidation
Tronson, N. C., & Taylor, J. R. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.01.022 · Cited by 83 · see citing works
“This suggests that enhancement of reconsolidation, like the enhancement of consolidation, may lead to strengthened memory [37,53,54,55 ].”
BackgroundSpacing Repetitions Over Long Timescales: A Review and a Reconsolidation Explanation
Smith, C., & Scarf, D. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.00962 · Cited by 79 · see citing works
“Researchers have determined two functions for memory reconsolidation: altering an existing memory trace in response to new experiences and strengthening a memory (Lee, 2008; Alberini, 2011; Inda et al., 2011).”
BackgroundStrengthening a consolidated memory: The key role of the reconsolidation process
Forcato, C., Fernández, R. S., & Pedreira, M. E. (2014) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2014.09.001 · Cited by 72 · see citing works
“We considered that older memories could not be reactivated (Suzuki et al., 2004; Inda et al., 2011).”
BackgroundInfluentialMotor Skills Are Strengthened through Reconsolidation
Wymbs, N. F., Bastian, A. J., & Celnik, P. A. (2016) · Current Biology · doi:10.1016/j.cub.2015.11.066 · Cited by 69 · see citing works
Alberini, C. M., Johnson, S. A., & Ye, X. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-386892-3.00005-6 · Cited by 69 · see citing works
Self-citationCholinergic blockade frees fear extinction from its contextual dependency
Zelikowsky, M., Hast, T. A., Bennett, R. Z., Merjanian, M., Nocera, N. A., Ponnusamy, R., & Fanselow, M. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.08.006 · Cited by 71 · see citing works
Enhancement of Memories by Systemic Administration of Insulin-Like Growth Factor II
Stern, S. A., Kohtz, A. S., Pollonini, G., & Alberini, C. M. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.69 · Cited by 68 · see citing works
“Memory strength can be modulated not only around the initial phase of training but also by targeting retrieval or reactivation and the postretrieval process known as reconsolidation (Chen et al, 2011; Frenkel et al, 2005; Inda et al, 2011; Tronson and Taylor, 2007).”
BackgroundSelf-citationTranslational Approaches Targeting Reconsolidation
Kroes, M. C. W., Schiller, D., LeDoux, J. E., & Phelps, E. A. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_5008 · Cited by 63 · see citing works
“This could indicate that propranolol blocked the enhancement of memory that can result from reactivation (Inda et al. 2011).”
BackgroundBreaking boundaries: optimizing reconsolidation-based interventions for strong and old memoriesPreprint
Elsey, J. W. B., & Kindt, M. (2017) · Learning & Memory · doi:10.1101/lm.044156.116 · Cited by 67 · see citing works
“These findings were corroborated in a later study by the same research group (Inda et al. 2011).”
ResultPedraza, L. K., Sierra, R. O., Boos, F. Z., Haubrich, J., Quillfeldt, J. A., & Alvares, L. D. O. (2015) · Hippocampus · doi:10.1002/hipo.22527 · Cited by 62 · see citing works
“Further studies have shown that this reactivation effect is mediated by the reconsolidation process (Inda et al., 2011; de Oliveira Alvares et al., 2013).”
BackgroundBiased reporting of past self-injurious thoughts and behaviors: A literature review
Klimes‐Dougan, B., Mirza, S. A., Babkin, E., & Lanning, C. (2022) · Journal of Affective Disorders · doi:10.1016/j.jad.2022.04.073 · Cited by 61 · see citing works
Modulating reconsolidation: a link to causal systems-level dynamics of human memories
Sandrini, M., Cohen, L. G., & Censor, N. (2015) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.06.002 · Cited by 63 · see citing works
Winters, B. D., Tucci, M. C., Jacklin, D. L., Reid, J. M., & Newsome, J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2968-11.2011 · Cited by 61 · see citing works
“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).”
BackgroundDalton, B., Bartholdy, S., Campbell, I. C., & Schmidt, U. H. (2018) · Current Neuropharmacology · doi:10.2174/1570159x16666180108111532 · Cited by 61 · see citing works
“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.”
BackgroundCorcoran, K. A., Frick, B. J., Radulović, J., & Kay, L. M. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.11.019 · Cited by 60 · see citing works
The role of test expectancy in the build-up of proactive interference in long-term memory.
Weinstein, Y., Gilmore, A. W., Szpunar, K. K., & McDermott, K. B. (2014) · Journal of Experimental Psychology Learning Memory and Cognition · doi:10.1037/a0036164 · Cited by 59 · see citing works
Treanor, M., Brown, L. A., Rissman, J., & Craske, M. G. (2017) · Perspectives on Psychological Science · doi:10.1177/1745691616664725 · Cited by 58 · see citing works
Memory reconsolidation understood and misunderstood
Ecker, B. (2015) · International Journal of Neuropsychotherapy · doi:10.12744/ijnpt.2015.0002-0046 · Cited by 60 · see citing works
Neuromodulation and neurofeedback treatments in eating disorders and obesity
Dalton, B., Campbell, I. C., & Schmidt, U. H. (2017) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000361 · Cited by 58 · see citing works
Genome-wide analysis of H4K5 acetylation associated with fear memory in mice
Park, C., Rehrauer, H., & Mansuy, I. M. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-539 · Cited by 56 · see citing works
“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
Kida, S. (2020) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.96.008 · Cited by 55 · see citing works
Reconsolidation and the regulation of plasticity: moving beyond memory
Bonin, R. P., & Koninck, Y. D. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.04.007 · Cited by 51 · see citing works
Da Silva, W. C., Cardoso, G., Bonini, J. S., Benetti, F., & Izquierdo, I. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1302356110 · Cited by 52 · see citing works
“The present findings attest to the long-lasting nature of reconsolidation effects (17).”
Mindfulness-Based Stress Reduction, Fear Conditioning, and The Uncinate Fasciculus: A Pilot Study
Hölzel, B. K., Brunsch, V., Gard, T., Greve, D. N., Koch, K., Sorg, C., Lazar, S. W., & Milad, M. R. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00124 · Cited by 55 · see citing works
Forcato, C., Fernández, R. S., & Pedreira, M. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061688 · Cited by 50 · see citing works
“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
Galarza-Vallejo, A., Kroes, M. C. W., Rey, E., Acedo, M. V., Moratti, S., Fernández, G., & Strange, B. A. (2019) · Science Advances · doi:10.1126/sciadv.aav3801 · Cited by 51 · see citing works
Jarome, T. J., Kwapis, J. L., Werner, C. T., Parsons, R. G., Gafford, G. M., & Helmstetter, F. J. (2012) · Learning & Memory · doi:10.1101/lm.024901.111 · Cited by 51 · see citing works
“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
Cassini, L. F., Flavell, C. R., Amaral, O. B., & Lee, J. L. C. (2017) · Learning & Memory · doi:10.1101/lm.045724.117 · Cited by 47 · see citing works
Insulin-like growth factor 2 rescues aging-related memory loss in rats
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 50 · see citing works
“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 49 · see citing works
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 48 · see citing works
Finsterwald, C., Steinmetz, A. B., Travaglia, A., & Alberini, C. M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0771-15.2015 · Cited by 48 · see citing works
“…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 47 · see citing works
“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 · see citing works
“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 · see citing works
“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 46 · see citing works
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 47 · see citing works
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 45 · see citing works
“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 · see citing works
“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 · see citing works
“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 · see citing works
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 43 · see citing works
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 42 · see citing works
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 · see citing works
“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 41 · see citing works
“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 · see citing works
“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 · see citing works
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 39 · see citing works
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 37 · see citing works
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 40 · see citing works
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 · see citing works
“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 38 · see citing works
“It should be noted that there is evidence for reconsolidation as a memory-strengthening mechanism (Lee, 2008; Inda et al., 2011).”
Background
- 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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