Stability of retrieved memory: Inverse correlation with trace dominance
Abstract
In memory consolidation, the memory trace stabilizes and becomes resistant to certain amnesic agents. The textbook account is that for any memorized item, consolidation starts and ends just once. However, evidence has accumulated that upon activation in retrieval, the trace may reconsolidate. Whereas some authors reported transient renewed susceptibility of retrieved memories to consolidation blockers, others could not detect it. Here, we report that in both conditioned taste aversion in the rat and fear conditioning in the medaka fish, the stability of retrieved memory is inversely correlated with the control of behavior by that memory. This result may explain some conflicting findings on reconsolidation of activated memories.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Following the acquisition of a pavlovian memory, re-exposure to the CS alone can induce one of four memory processes: retrieval, reconsolidation, "limbo" or extinction.
“Following the acquisition of a pavlovian memory, re-exposure to the CS alone can induce one of four memory processes: retrieval, reconsolidation, “limbo” or extinction (Figure 1; Eisenberg et al., 2003; Pedreira and Maldonado, 2003; Merlo et al., 2014, 2018).”
From Retrieval-Dependent Mechanisms Affecting Emotional Memory Persistence: Reconsolidation, Extinction, and the Space in Between (2020) · cites this paper as Eisenberg et al., 2003
Typically, for pavlovian CSs, a brief duration of re-exposure or a small number of CS re-exposures is sufficient to induce memory destabilisation without engaging extinction, for both appetitive and aversive memories and across species.
“Typically, for pavlovian CSs, a brief duration of re-exposure or a small number of CS re-exposures is sufficient to induce memory destabilisation without engaging extinction, for both appetitive and aversive memories and across species (Eisenberg et al., 2003; Pedreira and Maldonado, 2003; Flavell and Lee, 2013).”
From Retrieval-Dependent Mechanisms Affecting Emotional Memory Persistence: Reconsolidation, Extinction, and the Space in Between (2020) · cites this paper as Eisenberg et al., 2003
Insufficient exposure may set the stage for reconsolidation of active fear memories, and DCS may enhance these adverse reconsolidation effects, leading to poorer outcome relative to placebo.
“Moreover, insufficient exposure may also set the stage for reconsolidation of active fear memories (23), and there is evidence that DCS may be able to enhance these adverse reconsolidation effects as well, leading to poorer outcome relative to placebo administration, as potentially observed in this and other studies (9, 24).”
From D-cycloserine enhancement of fear extinction is specific to successful exposure sessions: evidence from the treatment of height phobia (2013) · cites this paper as [23]
Cites
Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval
Nader, K., Schafe, G. E., & Le Doux, J. E. (2000) · Nature · doi:10.1038/35021052 · Cited by 2,706 · see citing works
Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex.
Pavlov, P. I. (1930) · Archives of Neurology And Psychiatry · doi:10.1001/archneurpsyc.1930.02220110256018 · Cited by 2,681 · see citing works
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 · see citing works
Retrieval and reconsolidation: Toward a neurobiology of remembering
Sara, S. J. (2000) · Learning & Memory · doi:10.1101/lm.7.2.73 · Cited by 919 · see citing works
Behavioral and Neural Analysis of Extinction
Myers, K. M., & Davis, M. (2002) · Neuron · doi:10.1016/s0896-6273(02)01064-4 · Cited by 918 · see citing works
Peters, A., & Vaughan, D. W. (1981) · Springer eBooks · doi:10.1007/978-1-4684-3929-8_1 · Cited by 900 · see citing works
Misanin, J. R., Miller, R. R., & Lewis, D. J. (1968) · Science · doi:10.1126/science.160.3827.554 · Cited by 872 · see citing works
Montarolo, P. G., Goelet, P., Castellucci, V. F., Morgan, J., Kandel, E. R., & Schacher, S. (1986) · Science · doi:10.1126/science.3775383 · Cited by 769 · see citing works
Nader, K. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)00042-5 · Cited by 763 · see citing works
Psychobiology of active and inactive memory.
Lewis, D. J. (1979) · Psychological Bulletin · doi:10.1037/0033-2909.86.5.1054 · Cited by 486 · see citing works
Berman, D. E., & Dudai, Y. (2001) · Science · doi:10.1126/science.1058165 · Cited by 472 · see citing works
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 420 · see citing works
Conditioning, remembering, and forgetting.
Bouton, M. E. (1994) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.20.3.219 · Cited by 327 · see citing works
Vianna, M., Szapiro, G., McGaugh, J. D., Medina, J., & Izquierdo, I. (2001) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.211433298 · Cited by 301 · see citing works
Zeigler-Hill, V., & Shackelford, T. K. (2020) · Springer eBooks · doi:10.1007/978-3-319-24612-3_300506 · Cited by 258 · see citing works
Anokhin, K. V., Тиунова, А. А., & Rose, S. P. R. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02023.x · Cited by 207 · see citing works
Dudai, Y. (2002) · doi:10.1093/oso/9780198502678.001.0001 · Cited by 168 · see citing works
Self-citationMemory from A to Z: keywords, concepts, and beyond
(2003) · Choice Reviews Online · doi:10.5860/choice.41-0062 · Cited by 164 · see citing works
Bureš, J., Bermúdez‐Rattoni, F., & Yamamoto, T. (1998) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198523475.001.0001 · Cited by 153 · see citing works
Bahar, A. S., Samuel, A., Hazvi, S., & Dudai, Y. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02551.x · Cited by 144 · see citing works
Self-citationBerman, D. E., Hazvi, S., Stehberg, J., Bahar, A. S., & Dudai, Y. (2003) · Learning & Memory · doi:10.1101/lm.53703 · Cited by 86 · see citing works
Self-citationInterpretations of retrograde amnesia: old problems redux
Millin, P. M., Moody, E. W., & Riccio, D. C. (2001) · Nature reviews. Neuroscience · doi:10.1038/35049075 · Cited by 70 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior
Phelps, E. A., & LeDoux, J. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.025 · Cited by 3,203 · see citing works
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 · see citing works
Self-citationNeural Mechanisms of Extinction Learning and Retrieval
Quirk, G. J., & Mueller, D. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301555 · Cited by 1,645 · see citing works
The Molecular and Systems Biology of Memory
Kandel, E. R., Dudai, Y., & Mayford, M. R. (2014) · Cell · doi:10.1016/j.cell.2014.03.001 · Cited by 1,134 · see citing works
Self-citationMemory 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
Memory engrams: Recalling the past and imagining the future
Josselyn, S. A., & Tonegawa, S. (2020) · Science · doi:10.1126/science.aaw4325 · Cited by 1,087 · see citing works
Extinction-Reconsolidation Boundaries: Key to Persistent Attenuation of Fear Memories
Monfils, M.-H., Cowansage, K. K., Klann, E., & LeDoux, J. E. (2009) · Science · doi:10.1126/science.1167975 · Cited by 960 · see citing works
A single standard for memory: The case for reconsolidation
Nader, K., & Hardt, O. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2590 · Cited by 811 · see citing works
Perineuronal Nets Protect Fear Memories from Erasure
Gogolla, N., Caroni, P., Lüthi, A., & Herry, C. (2009) · Science · doi:10.1126/science.1174146 · Cited by 760 · 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
Self-citationReconsolidation: maintaining memory relevance
Lee, J. L. C. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.05.002 · Cited by 516 · see citing works
A Memory Retrieval-Extinction Procedure to Prevent Drug Craving and Relapse
Xue, Y.-X., Luo, Y.-X., Wu, P., Shi, H.-S., Xue, L.-F., Chen, C., Zhu, W.-L., Ding, Z.-B., Bao, Y.-P., Shi, J., et al. (2012) · Science · doi:10.1126/science.1215070 · Cited by 511 · see citing works
Neuronal circuits of fear extinction
Herry, C., Ferraguti, F., Singewald, N., Letzkus, J. J., Ehrlich, I., & Lüthi, A. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07101.x · Cited by 484 · see citing works
Reconsolidation and Extinction of Conditioned Fear: Inhibition and Potentiation
Lee, J. L. C., Milton, A. L., & Everitt, B. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2466-06.2006 · Cited by 479 · see citing works
Synaptic Protein Degradation Underlies Destabilization of Retrieved Fear Memory
Lee, S.-H., Choi, J.-H., Lee, N., Lee, H.-R., Kim, J.-I., Yu, N.-K., Choi, S.-L., Lee, S.-H., Kim, H., & Kaang, B.-K. (2008) · Science · doi:10.1126/science.1150541 · Cited by 409 · see citing works
Pedreira, M. E., Pérez-Cuesta, L. M., & Maldonado, H. (2004) · Learning & Memory · doi:10.1101/lm.76904 · Cited by 367 · see citing works
Characterization of fear memory reconsolidation
Duvarci, S., & Nader, K. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2971-04.2004 · Cited by 379 · see citing works
Redish, A. D., Jensen, S., Johnson, A., & Kurth-Nelson, Z. (2007) · Psychological Review · doi:10.1037/0033-295x.114.3.784 · Cited by 346 · see citing works
Reconsolidation: the advantage of being refocused
Dudai, Y. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.03.010 · Cited by 357 · see citing works
Self-citationRapid Erasure of Long-Term Memory Associations in the Cortex by an Inhibitor of PKMζ
Shema, R., Sacktor, T. C., & Dudai, Y. (2007) · Science · doi:10.1126/science.1144334 · Cited by 353 · see citing works
Self-citationMorris, 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 · see citing works
Self-citationRossato, J. I., Bevilaqua, L. R. M., Myskiw, J. C., Medina, J. H., Izquierdo, I., & Cammarota, M. (2007) · Learning & Memory · doi:10.1101/lm.422607 · Cited by 282 · see citing works
Memory Retrieval and the Passage of Time: From Reconsolidation and Strengthening to Extinction
Inda, M. C., Muravieva, E. V., & Alberini, C. M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4736-10.2011 · Cited by 261 · see citing works
Merlo, E., Milton, A. L., Goozée, Z. Y., Theobald, D. E., & Everitt, B. J. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4001-13.2014 · Cited by 242 · see citing works
Deębiec, J., Doyère, V., Nader, K., & LeDoux, J. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507168103 · Cited by 207 · see citing works
Hardt, O., Einarsson, E. Ö., & Nader, K. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100455 · Cited by 211 · see citing works
Reconsolidation and the dynamic nature of memory
Nader, K. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021782 · Cited by 221 · see citing works
Human memory reconsolidation: A guiding framework and critical review of the evidence.
Elsey, J. W. B., Van Ast, V. A., & Kindt, M. (2018) · Psychological Bulletin · doi:10.1037/bul0000152 · Cited by 199 · see citing works
The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation
Finnie, P. S. B., & Nader, K. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.008 · Cited by 189 · see citing works
Learning to forget: manipulating extinction and reconsolidation processes to treat addiction
Torregrossa, M. M., & Taylor, J. R. (2013) · Psychopharmacology · doi:10.1007/s00213-012-2750-9 · Cited by 172 · see citing works
Prediction error demarcates the transition from retrieval, to reconsolidation, to new learning
Sevenster, D., Beckers, T., & Kindt, M. (2014) · Learning & Memory · doi:10.1101/lm.035493.114 · Cited by 161 · see citing works
The computational nature of memory modification
Gershman, S. J., Monfils, M.-H., Norman, K. A., & Niv, Y. (2017) · eLife · doi:10.7554/elife.23763 · Cited by 172 · see citing works
On disruption of fear memory by reconsolidation blockade: evidence from cannabidiol treatment
Stern, C. A. J., Gazarini, L., Takahashi, R. N., Guimarães, F. S., & Bertoglio, L. J. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.63 · Cited by 156 · see citing works
Soeter, M., & Kindt, M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.307 · Cited by 150 · see citing works
Smits, J. A. J., Rosenfield, D., Otto, M. W., Powers, M. B., Hofmann, S. G., Telch, M. J., Pollack, M. H., & Tart, C. D. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.12.009 · Cited by 142 · 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
Human memory reconsolidation can be explained using the temporal context model
Sederberg, P. B., Gershman, S. J., Polyn, S. M., & Norman, K. A. (2011) · Psychonomic Bulletin & Review · doi:10.3758/s13423-011-0086-9 · Cited by 125 · see citing works
Brown, T. E., Forquer, M. R., Cocking, D. L., Jansen, H. T., Harding, J. W., & Sorg, B. A. (2007) · Learning & Memory · doi:10.1101/lm.476207 · Cited by 121 · see citing works
Fear thou not: activity of frontal and temporal circuits in moments of real-life courage
Nili, U., Goldberg, H., Weizman, A., & Dudai, Y. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.009 · Cited by 100 · see citing works
Self-citationMilton, A. L., Schramm, M. J. W., Wawrzynski, J. R., Gore, F., Oikonomou-Mpegeti, F., Wang, N. Q., Samuel, D., Economidou, D., & Everitt, B. J. (2012) · Psychopharmacology · doi:10.1007/s00213-011-2399-9 · Cited by 96 · see citing works
Levy, I., & Schiller, D. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2020.11.007 · Cited by 95 · see citing works
Failures to reconsolidate memory in a mouse model of Alzheimer’s disease
Ohno, M. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.05.001 · Cited by 95 · see citing works
p300/CBP-Associated Factor Selectively Regulates the Extinction of Conditioned Fear
Wei, W., Coelho, C. M., Li, X., Marek, R., Yan, S., Anderson, S., Meyers, D., Mukherjee, C., Sbardella, G., Castellano, S., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0178-12.2012 · Cited by 93 · see citing works
Noradrenergic Blockade of Memory Reconsolidation: A Failure to Reduce Conditioned Fear Responding
Bos, M. G. N., Beckers, T., & Kindt, M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00412 · Cited by 86 · see citing works
Extinction learning, reconsolidation and the internal reinforcement hypothesis
Eisenhardt, D., & Menzel, R. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.09.005 · Cited by 89 · see citing works
Enhanced Extinction of Aversive Memories by High-Frequency Stimulation of the Rat Infralimbic Cortex
Maroun, M., Kavushansky, A., Holmes, A., Wellman, C., & Motanis, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035853 · Cited by 79 · see citing works
Augmentation of exposure therapy with post-session administration of D-cycloserine
Tart, C. D., Handelsman, P. R., DeBoer, L. B., Rosenfield, D., Pollack, M. H., Hofmann, S. G., Powers, M. B., Otto, M. W., & Smits, J. A. J. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.09.024 · Cited by 75 · see citing works
A critical role for protein degradation in the nucleus accumbens core in cocaine reward memory
Ren, Z.-Y., Liu, M.-M., Xue, Y.-X., Ding, Z.-B., Xue, L.-F., Zhai, S.-D., & Lu, L. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2012.243 · Cited by 73 · see citing works
Alfei, J. M., Ferrer Monti, R. I., Molina, V. A., Bueno, A. M., & Urcelay, G. P. (2015) · Learning & Memory · doi:10.1101/lm.038513.115 · Cited by 71 · see citing works
D-cycloserine potentiates the reconsolidation of cocaine-associated memories
Lee, J. L. C., Gardner, R. J., Butler, V. J., & Everitt, B. J. (2009) · Learning & Memory · doi:10.1101/lm.1186609 · Cited by 70 · see citing works
A mismatch-based model for memory reconsolidation and extinction in attractor networks
Osan, R., Tort, A. B. L., & Amaral, O. B. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023113 · Cited by 63 · 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
Merlo, E., Milton, A. L., & Everitt, B. J. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.3273-17.2018 · Cited by 41 · see citing works
Vaverková, Z., Milton, A. L., & Merlo, E. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.574358 · Cited by 27 · see citing works
Old fears die hard: return of public speaking fear in a virtual reality procedure
van Dis, E. A. M., Landkroon, E., Hagenaars, M. A., van der Does, F. H. S., & Engelhard, I. M. (2021) · Behavior Therapy · doi:10.1016/j.beth.2021.01.005 · Cited by 20 · see citing works
Identification of a Novel Retrieval-Dependent Memory Process in the Crab <i>Neohelice granulata</i>
Merlo, S. A., Santos, M. J., Pedreira, M. E., & Merlo, E. (2019) · doi:10.1101/2019.12.19.881128
- Authors
- Eisenberg, M., Kobilo, T., Berman, D. E., & Dudai, Y.
- Affiliations
- Weizmann Institute of Science (IL)
- Corresponding author
- Berman, Diego E.
- Dudai, Yadin
- ORCID
- Berman, Diego E.
- Venue
- Science
- Published
- 2003-08-22
- Volume
- 301
- Issue
- 5636
- Pages
- 1102-1104
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W1972758800
- Cited by
- 518
- References
- 22
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 8 · 2023: 6 · 2022: 21 · 2021: 18 · 2020: 29 · 2019: 13 · 2018: 21 · 2017: 29 · 2016: 26 · 2015: 34 · 2014: 28 · 2013: 29 · 2012: 35
- FWCI
- 10.30
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (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 › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- memory reconsolidation, memory consolidation, memory retrieval, conditioned taste aversion, fear conditioning, medaka, rats
- MeSH terms
- Analysis of Variance, Animals, Anisomycin, Avoidance Learning, Cerebral Cortex, Conditioning, Psychological, Cues, Electroshock, Extinction, Psychological, Fear, Male, Memory, Oryzias, Mental Recall, Taste, Rats, Wistar, Rats, Aminobenzoates, meta-Aminobenzoates
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
