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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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Citations
Cites
Memory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250
The organization of recent and remote memories
Frankland, P. W., & Bontempi, B. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1607 · Cited by 2,138
Memory consolidation, retrograde amnesia and the hippocampal complex
Nadel, L., & Moscovitch, M. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80010-4 · Cited by 1,924
Context, time, and memory retrieval in the interference paradigms of Pavlovian learning
Bouton, M. E. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.114.1.80 · Cited by 1,896
The Neurobiology of Consolidations, Or, How Stable is the Engram?
Dudai, Y. (2004) · Annual Review of Psychology · doi:10.1146/annurev.psych.55.090902.142050 · Cited by 1,671
Neural Mechanisms of Extinction Learning and Retrieval
Quirk, G. J., & Mueller, D. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301555 · Cited by 1,645
Protein synthesis and memory: A review.
Davis, H. P., & Squire, L. R. (1984) · Psychological Bulletin · doi:10.1037/0033-2909.96.3.518 · Cited by 1,505
Preventing the return of fear in humans using reconsolidation update mechanisms
Schiller, D., Monfils, M.-H., Raio, C. M., Johnson, D. C., LeDoux, J. E., & Phelps, E. A. (2010) · Nature · doi:10.1038/nature08637 · Cited by 1,248
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
Incubation of cocaine craving after withdrawal
Grimm, J. W., Hope, B. T., Wise, R. A., & Shaham, Y. (2001) · Nature · doi:10.1038/35084134 · Cited by 1,031
Dependence on REM Sleep of Overnight Improvement of a Perceptual Skill
Karni, A., Tanne, D., Rubenstein, B. S., Askenasy, J. J. M., & Sagi, D. (1994) · Science · doi:10.1126/science.8036518 · Cited by 1,002
Transcription Factors in Long-Term Memory and Synaptic Plasticity
Alberini, C. M. (2009) · Physiological Reviews · doi:10.1152/physrev.00017.2008 · Cited by 991
Self-citationRetrieval and reconsolidation: Toward a neurobiology of remembering
Sara, S. J. (2000) · Learning & Memory · doi:10.1101/lm.7.2.73 · Cited by 919
Beyond extinction: erasing human fear responses and preventing the return of fear
Kindt, M., Soeter, M., & Vervliet, B. (2009) · Nature Neuroscience · doi:10.1038/nn.2271 · Cited by 826
Molecular mechanisms of memory reconsolidation
Tronson, N. C., & Taylor, J. R. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2090 · Cited by 810
Cellular and Systems Reconsolidation in the Hippocampus
Dębiec, J., LeDoux, J. E., & Nader, K. (2002) · Neuron · doi:10.1016/s0896-6273(02)01001-2 · Cited by 772
Awake replay of remote experiences in the hippocampus
Karlsson, M. P., & Frank, L. M. (2009) · Nature Neuroscience · doi:10.1038/nn.2344 · Cited by 769
The cognitive neuroscience of remote episodic, semantic and spatial memory
Moscovitch, M., Nadel, L., Winocur, G., Gilboa, A., & Rosenbaum, R. S. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.03.013 · Cited by 711
The labile nature of consolidation theory
Nader, K., Schafe, G. E., & LeDoux, J. E. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044580 · Cited by 613
Alberini, C. M. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2004.11.001 · Cited by 594
Self-citationSleep-dependent memory consolidation and reconsolidation
Stickgold, R., & Walker, M. P. (2007) · Sleep Medicine · doi:10.1016/j.sleep.2007.03.011 · Cited by 567
Memory and Brain Systems: 1969–2009
Squire, L. R. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3575-09.2009 · Cited by 550
Reconsolidation of episodic memories: A subtle reminder triggers integration of new information
Hupbach, A., Gomez, R., Hardt, O., & Nadel, L. (2007) · Learning & Memory · doi:10.1101/lm.365707 · Cited by 544
Stability of retrieved memory: Inverse correlation with trace dominance
Eisenberg, M., Kobilo, T., Berman, D. E., & Dudai, Y. (2003) · Science · doi:10.1126/science.1086881 · Cited by 518
Reconsolidation: maintaining memory relevance
Lee, J. L. C. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.05.002 · Cited by 516
Psychobiology of active and inactive memory.
Lewis, D. J. (1979) · Psychological Bulletin · doi:10.1037/0033-2909.86.5.1054 · Cited by 501
Rites of Passage of the Engram
Dudai, Y., & Eisenberg, M. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.003 · Cited by 476
Temporally graded requirement for protein synthesis following memory reactivation
Milekic, M. H., & Alberini, C. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00976-5 · Cited by 455
Self-citationThe consolidation of new but not reactivated memory requires hippocampal C/EBPβ
Taubenfeld, S. M., Milekic, M. H., Monti, B., & Alberini, C. M. (2001) · Nature Neuroscience · doi:10.1038/90520 · Cited by 426
Self-citationA critical role for IGF-II in memory consolidation and enhancement
Chen, D. Y., Stern, S. A., García‐Osta, A., Saunier-Rebori, B., Pollonini, G., Bambah-Mukku, D., Blitzer, R. D., & Alberini, C. M. (2011) · Nature · doi:10.1038/nature09667 · Cited by 421
Self-citationMemory reconsolidation mediates the strengthening of memories by additional learning
Lee, J. L. C. (2008) · Nature Neuroscience · doi:10.1038/nn.2205 · Cited by 420
Protein Synthesis Subserves Reconsolidation or Extinction Depending on Reminder Duration
Pedreira, M. E., & Maldonado, H. (2003) · Neuron · doi:10.1016/s0896-6273(03)00352-0 · Cited by 406
Reconsolidation: the advantage of being refocused
Dudai, Y. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.03.010 · Cited by 357
Morris, R. G. M., Inglis, J., Ainge, J. A., Olverman, H. J., Tulloch, J., Dudai, Y., & Kelly, P. A. T. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.012 · Cited by 342
The neuroscience of remote memory
Squire, L. R., & Bayley, P. J. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.02.006 · Cited by 329
Stability of recent and remote contextual fear memory
Frankland, P. W., Ding, H.-K., Takahashi, E., Suzuki, A., Kida, S., & Silva, A. J. (2006) · Learning & Memory · doi:10.1101/lm.183406 · Cited by 259
A theory of the incubation of anxiety/fear responses
Eysenck, H. J. (1968) · Behaviour Research and Therapy · doi:10.1016/0005-7967(68)90064-8 · Cited by 237
Persistent Disruption of an Established Morphine Conditioned Place Preference
Milekic, M. H., Brown, S. D., Castellini, C., & Alberini, C. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4818-05.2006 · Cited by 218
Self-citationReconsolidation of fresh, remote, and extinguished fear memory in medaka: old fears don't die
Eisenberg, M., & Dudai, Y. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03818.x · Cited by 214
The role of protein synthesis during the labile phases of memory: Revisiting the skepticism
Alberini, C. M. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.08.007 · Cited by 185
Self-citationBustos, S. G., Maldonado, H., & Molina, V. A. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.75 · Cited by 170
Power, A. E., Berlau, D. J., McGaugh, J. L., & Steward, O. (2006) · Learning & Memory · doi:10.1101/lm.91206 · Cited by 161
Tronel, S., Milekic, M. H., & Alberini, C. M. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030293 · Cited by 156
Self-citationStrengthening the shaky trace through retrieval
Sara, S. J. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044575 · Cited by 144
Winters, B. D., Tucci, M. C., & DaCosta-Furtado, M. (2009) · Learning & Memory · doi:10.1101/lm.1509909 · Cited by 143
Long-Lasting Incubation of Conditioned Fear in Rats
Pickens, C. L., Golden, S. A., Adams‐Deutsch, T., Nair, S. G., & Shaham, Y. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.12.010 · Cited by 136
Rodríguez‐Ortiz, C. J., la Cruz, V. D., Gutiérrez, R., & Bermúdez‐Rattoni, F. (2005) · Learning & Memory · doi:10.1101/lm.94505 · Cited by 122
Frenkel, L., Maldonado, H., & Delorenzi, A. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04373.x · Cited by 99
Circadian rhythms and memory: not so simple as cogs and gears
Eckel‐Mahan, K. L., & Storm, D. R. (2009) · EMBO Reports · doi:10.1038/embor.2009.123 · Cited by 99
Rodríguez‐Ortiz, C. J., Torre, P., Benavidez, E., Ballesteros, M. Á., & Bermúdez‐Rattoni, F. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.10.004 · Cited by 87
Activation of Hippocampal Nuclear Factor-κB by Retrieval Is Required for Memory Reconsolidation
Boccia, M. M., Freudenthal, R., Blake, M. G., de la Fuente, V., Acosta, G. B., Baratti, C. M., & Romano, A. G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4430-07.2007 · Cited by 87
Electroconvulsive Shock Effects on a Reactivated Memory Trace: Further Examination
Dawson, R. G., & McGaugh, J. L. (1969) · Science · doi:10.1126/science.166.3904.525 · Cited by 85
Taubenfeld, S. M., Riceberg, J. S., New, A. S., & Alberini, C. M. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.07.005 · Cited by 73
Self-citationDo memories consolidate to persist or do they persist to consolidate?
Medina, J. H., Bekinschtein, P., Cammarota, M., & Izquierdo, I. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.02.006 · Cited by 70
Combining pharmacotherapy with cognitive behavioral therapy: Traditional and new approaches
Davis, M., Barad, M., Otto, M. W., & Southwick, S. (2006) · Journal of Traumatic Stress · doi:10.1002/jts.20149 · Cited by 55
Glucocorticoid-mediated effects of systemic oxytocin upon memory retrieval
de Oliveira, L. F., Camboim, C., Diehl, F., Consiglio, A. R., & Quillfeldt, J. A. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.05.006 · Cited by 34
Updating contextual information during consolidation as result of a new memory trace
Suárez, L. D., Smal, L., & Delorenzi, A. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.02.004 · Cited by 17
Flagged first, then by citations
Research works printed but not linked: 1
- McAllister, 1967, Incubation of fear: an examination of the concept, J Exp Res Person, 2, 180
Cited by
Sorted by citations
Hölzel, B. K., Lazar, S. W., Gard, T., Schuman-Olivier, Z., Vago, D. R., & Ott, U. (2011) · Perspectives on Psychological Science · doi:10.1177/1745691611419671 · Cited by 3,024
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644
“This might happen in some cases as memory ages (Milekic & Alberini 2002, Eisenberg & Dudai 2004, Inda et al. 2011).”
BackgroundLane, R. D., Ryan, L., Nadel, L., & Greenberg, L. S. (2014) · Behavioral and Brain Sciences · doi:10.1017/s0140525x14000041 · Cited by 611
“In humans, Hupbach et al. (2007, 2008) have shown that when memories are reactivated through reminders, they are open to modification through the presentation of similar material that then becomes incorporated into the original event memory.”
BackgroundMethodImplications of memory modulation for post-traumatic stress and fear disorders
Parsons, R. G., & Ressler, K. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3296 · Cited by 476
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453
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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