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Characterization of Fear Memory Reconsolidation
Open accessAbstract
Reactivation of consolidated memories returns them to a protein synthesis-dependent state. One interpretation of these findings is that the memory reconsolidates after use. Two alternative interpretations are that protein synthesis inhibition facilitates extinction and that postreactivation protein synthesis inhibition leads to an inability to retrieve the consolidated memory. First, using two different approaches, we report that reconsolidation cannot be reduced down to facilitated extinction. We show that the reconsolidation deficit does not show renewal after a contextual shift, whereas an extinguished auditory fear memory does under the same conditions and the deficit occurs regardless of whether the memory is reactivated with an extinction [conditioned stimulus (CS) alone] or a reinforced trial (CS-unconditioned stimulus). To address the issue of whether postreactivation anisomycin leads to an inability to retrieve the consolidated memory, we used two traditional assays for retrieval deficits. First, we demonstrate that the amnesia induced by blockade of reconsolidation does not show any spontaneous recovery. Second, we show that application of reminder shock does not result in the reinstatement of the memory. These findings support the idea that reactivation of consolidated memories initiates a second time-dependent memory formation process.
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“Indeed, neuroscience has shown that re-accessing memories generally changes them, rather than enforces them.66,67”
From The overfitted brain: Dreams evolved to assist generalization (2021) · cites this paper as [66]
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Citations
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BackgroundA Method to Provoke Obsessive Compulsive Symptoms for Basic Research and Clinical Interventions
Tendler, A., Sisko, E., Barnea‐Ygael, N., Zangen, A., & Storch, E. A. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00814 · Cited by 24
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“Pharmacological interventions given 6 h after the reactivation of spatial (Przybyslawski and Sara, 1997) and aversive memories (Duvarci and Nader, 2004; Bustos et al., 2006; Stern et al., 2012) have produced no effects on their reconsolidation, indicating that the reconsolidation timewindow had…”
BackgroundDoes Reconsolidation Occur in Humans: A Reply
Brunet, A., Ashbaugh, A. R., Saumier, D., Nelson, M., Pitman, R. K., Tremblay, J., Roullet, P., & Birmes, P. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00074 · Cited by 30
“Most of it appears to take place within the first 2 h (Przybyslawski et al., 1999) and to be over by the sixth hour (Duvarci and Nader, 2004).”
BackgroundMemory Destabilization and Reconsolidation Dynamically Regulate the PKMζ Maintenance Mechanism
Bernabo, M., Haubrich, J., Gamache, K., & Nader, K. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2093-20.2021 · Cited by 17
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Extinction after fear memory reactivation fails to eliminate renewal in rats
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“…windows can be opened by the presentation of the CS alone, the US alone, a conditioned context, or even a conditioning trial (CS + US) and protein synthesis inhibitors delivered after these forms of reactivation lead to impaired retention of conditioned fear memories (Duvarci & Nader, 2004).”
Genes and neurons: molecular insights to fear and anxiety
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“Understanding the impact of particular genes to extinction and re-consolidation (Duvarci & Nader 2004; Suzuki et al. 2004) of fear memories will certainly help to unravel the mechanisms that determine the stability of fear and anxiety phenomena and may guide future ther- apeutic approaches to…”
BackgroundThe Computational Nature of Memory ModificationPreprint
Gershman, S. J., Monfils, M., Norman, K. A., & Niv, Y. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/036442 · Cited by 21
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New Approaches to Addiction Treatment Based on Learning and Memory
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An isolated retrieval trial before extinction session does not prevent the return of fear
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Sugiyama, A., Saitoh, A., Inagaki, M., Oka, J., & Yamada, M. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.06.007 · Cited by 18
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“To distinguish between these two processes, it has been suggested that at least three tests should be conducted: spontaneous recovery, renewal and reinstatement, which are expected to show no return of the previous memory trace in the case of reconsolidation disruption [61,95].”
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Alfei, J. M., Monti, R. I. F., Molina, V. A., Bundel, D. D., Luyten, L., & Beckers, T. (2020) · Journal of Experimental Psychology General · doi:10.1037/xge0000765 · Cited by 21
“…after threat learning involving A), but also in ABA (B is used for memory reactivation and A is used for retention testing after threat learning involving A) and ABC (B is used for memory reactivation and C is used for retention testing after threat learning involving A) (Duvarci & Nader, 2004).”
MethodSocial recognition memory requires protein synthesis after reactivation.
Perrin, G., Ferreira, G., Meurisse, M., Verdin, S., Mouly, A., & Lévy, F. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.1.148 · Cited by 18
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“Importantly, the TMX effect lasted for at least 1 wk, suggesting no spontaneous recovery of fear memory, a result that agrees with reports showing no spontaneous recovery of fearmemory 1 wk after impairing memory reconsolidation (Duvarci and Nader 2004; Bustos et al. 2006; Stern et al. 2012).”
ResultUnconscious learning of likes and dislikes is persistent, resilient, and reconsolidates
Pine, A., Mendelsohn, A., & Dudai, Y. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01051 · Cited by 19
“…no new learning took place during the reminder test trials since there was no feedback, consistent with other examples from the animal literature (Duvarci and Nader, 2004) where reconsolidation was triggered by identical trials involving no new learning, and a human study (Hupbach et al., 2008)…”
ResultSolntseva, S. V., Nikitin, V. P., Kozyrev, S. A., Shevelkin, A. V., Lagutin, A. V., & Sherstnev, V. V. (2007) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-007-0100-x · Cited by 17
“In addition, we observed no extinction of the conditioned reflex food-related skill for 30 days in control animals, or any spontaneous recovery of the acquired skill, or facilitation of retraining, all of which are characteristic for the process of extinction [8, 9, 14].”
BackgroundInfluentialQuillfeldt, J. A. (2019) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00001 · Cited by 18
“, 2006; Quillfeldt and De Oliveira Alvares, 2015); • the model is fully compatible with the memory reconsolidation phenomenon (Lewis, 1979; Nader et al., 2000a,b; Anokhin et al., 2002; Walker et al., 2003; Duvarci and Nader, 2004; Lee et al., 2006; Rose and Rankin, 2006; Hupbach et al., 2008; Nader and Hardt, 2009; Bu…”
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“Importantly, the amnesia induced by blockade of reconsolidation does not show any spontaneous recovery, and application of a reminder shock does not result in the reinstatement of the memory [29].”
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Franzen, J. M., Vanz, F., Werle, I., Guimarães, F. S., & Bertoglio, L. J. (2022) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2022.08.002 · Cited by 18
Evidence on the impairing effects of Ayahuasca on fear memory reconsolidation
Daneluz, D. M., Sohn, J. M. B., Silveira, G. D. O., Yonamine, M., & Stern, C. A. J. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06217-2 · Cited by 17
“The evidence that AYA impaired reconsolidation, instead of facilitating extinction, was further confirmed by the results showing no reinstatement of fear memory in AYA-treated groups after the presentation of a reminder footshock, which agrees with previous studies (Duvarci and Nader 2004; Stern et al. 2012).”
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Deryabina, I., Николаевна, М. Л., Andrianov, V. V., & Латыпович, Г. Х. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00607 · Cited by 16
“That is, in each time the memories we not only express information, but, perhaps, create it again, this means that memory is a dynamic process and it either amplifies or alters during recalling (Schneider and Sherman, 1968; Lewis, 1979; Przybyslawski and Sara, 1997; Anokhin et al., 2002; Pedreira et al., 2002; Duvarci…”
BackgroundDiminishing fear: Optogenetic approach toward understanding neural circuits of fear control
Luchkina, N. V., & Bolshakov, V. Y. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.05.005 · Cited by 16
Effects of Cannabis on PTSD Recovery: Review of the Literature and Clinical Insights
Bedard‐Gilligan, M. A., Lehinger, E. A., Cornell-Maier, S., Holloway, A., & Zoellner, L. A. (2022) · Current Addiction Reports · doi:10.1007/s40429-022-00414-x · Cited by 18
“This hypothesis argues that, by systematically retrieving a conditioned stimulus (CS), previously stable, consolidated memories can be returned to a temporary labile state that allows for either strengthening or weakening of the original memory [44].”
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Temporal memory averaging and post-encoding alterations in temporal expectation
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“In addition, several recent studies have found that disrupting reconsolidation process may erase learned fear responses and prevent the return of fear (”
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Memory Erasure, Enhanced Extinction and Disrupted Reconsolidation
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“…the findings in this study support this dual-process possibility, as they provide evidence for the existence of both processes: on one hand, FGF2-treated rats exhibit an effect of renewal, a phenomenon found after extinction, but not after disruption of reconsolidation (Duvarci and Nader, 2004).”
InfluentialZoladz, P. R., Woodson, J. C., Haynes, V. F., & Diamond, D. M. (2010) · Stress · doi:10.3109/10253890902853123 · Cited by 16
“Theoretically, in the present experiments, reactivation of the memory of the shock experience initiated a reconsolidation process (Duvarci and Nader 2004; Tronson and Taylor 2007) which could have contributed to the impaired retrieval of the memory of the hidden platform in the RAWM.”
BackgroundHow Fear Memory is Updated: From Reconsolidation to Extinction?
Chen, J., Fang, Z., Zhang, X., Zheng, Y., & Chen, Z. (2025) · Neuroscience Bulletin · doi:10.1007/s12264-025-01367-7 · Cited by 16
“This aligns with Nader et al.’s findings [144], emphasizing that reconsolidation cannot be attenuated to facilitate extinction [146].”
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“…and paired with a manipulation: inhibitors of protein synthesis, specific kinases, or receptor activation (Nader et al., 2000; Kelly et al., 2003; Duvarci and Nader, 2004; Morris et al., 2006; Tronson et al., 2006; Boccia et al., 2007; Lubin and Sweatt, 2007; Zhang et al., 2010; Inda et al.,…”
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Anisomycin Inhibits the Behaviors of T cells and the Allogeneic Skin transplantation in mice
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Incomplete reminder cues trigger memory reconsolidation and sustain learned immune responses
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“Thus, the effects of post-training ethanol in a variety of tasks are quite complex (Dudai, 2004; Duvarci and Nader, 2004).”
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Neural and Molecular Mechanisms of Fear Memory
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“Elevated fear provides a unique avenue to investigate the behavioral and neural underpinnings of reconsolidation, as it does not share behavioral similarities with other procedures that do not rely on reconsolidation, like extinction (Bouton, 2004; Duvarci and Nader, 2004).”
BackgroundMechanisms underlying long-term fear memory formation from a metaplastic neuronal state
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“Some studies have shown that retrieval-induced memory impairments reverse with time (Lattal & Abel, 2004), while others have demonstrated long lasting deficits (Duvarci & Nader, 2004).”
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“This can be seen in the case of the reactivation of a previously consolidated auditory fear memory, it starts a reconsolidation process that aims to re‐stabilize the original memory tagging those active synapses involved (Duvarci & Nader, 2004).”
BackgroundRole of prediction error and the cholinergic system on memory reconsolidation processes in mice
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Lose the fear and boost the everyday memory through memory destabilisation and reconsolidation
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“This is however not the case for auditory fear memory (Duvarci and Nader, 2004; Popik et al., 2020).”
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“…2009) and long-term potentiation (LTP), at the synaptic level as well (Lynch, Rex, & Gall, 2007).10 Reconsolidation is another memory mechanism by which each memory, when recalled, is reshaped and modified according to new informational input from the time of recollection (Duvarci & Nader, 2004).”
BackgroundThreat processing: models and mechanisms
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Intensive Short-Term Dynamic Psychotherapy
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Reactivation-induced motor skill modulation does not operate at a rapid micro-timescale level
Herszage, J., Bönstrup, M., Cohen, L. G., & Censor, N. (2023) · Scientific Reports · doi:10.1038/s41598-023-29963-5 · Cited by 10
Neurocognitive dynamics of spontaneous offline simulations: Re-conceptualizing (dream)bizarreness
Kirberg, M. (2022) · Philosophical Psychology · doi:10.1080/09515089.2022.2042231 · Cited by 11
“More broadly, neuroscientific evidence suggests that instead of consolidating and reinforcing a specific episodic event, any reassessment of memories changes them in multiple ways (Duvarci & Nader, 2004).”
BackgroundTransprocessing: a proposed neurobiological mechanism of psychotherapeutic processing
Novac, A., & Bota, R. G. (2014) · Mental Illness · doi:10.4081/mi.2014.5077 · Cited by 11
NLP and PTSD: the Visual-Kinesthetic Dissociation Protocol
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Plasticity-augmented psychotherapy for refractory depressive and anxiety disorders
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Brito, I., de Britto, L. R. G., & Ferrari, E. A. M. (2019) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2019.09.013 · Cited by 8
Reconsolidation: Historical Perspective and Theoretical Aspects
Sara, S. J. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00061-9 · Cited by 8
Fox, K. C. R., Kang, Y., Lifshitz, M., & Kalina Christoff, A. (2016) · arXiv (Cornell University) · doi:10.48550/arxiv.1605.03553 · Cited by 11
“…literature, however, supports the idea that reactivated memories again enter a labile state where their consolidation can be disturbed, and the memory thereby weakened (Duvarci & Nader, 2004; Duvarci, Nader, & LeDoux, 2005, 2008; Finnie & Nader, 2012; Nader et al., 2000; Schwabe et al., 2012).”
BackgroundThe Impact of Unconditioned Stimulus Devaluation on Conditional Fear Extinction
Du, J., Zeng, X., Zheng, X., & ZHUANG, C. (2015) · Acta Psychologica Sinica · doi:10.3724/sp.j.1041.2015.00344 · Cited by 8
“2 编程呈现。首先呈现注视点“+”, 呈现时 间为 1000 ms, 注视点后呈现 CS, 呈现时间为 8000 ms, 随后跟随一个探测界面, 需要被试进行 1-9 的按键 反应判断 US 出现的可能性, 而后跟随 US 或者白屏, 呈现时间均为 1000 ms (如图 1 所示)。试次间的间 隔(ITI)为 16~20 s (Schultz et al., 2013)。CS 出现的 次序以准随机的方式编排, 以使每个 CS 都不会连 续两次以上重复出现。条件恐惧任务分为习得、再 评估、消退三个阶段。正式实验开始前, 被试首先 对实验过程进行习惯化练习 , 习惯化阶段 CS+和 CS‒均呈现 3 次。练习完毕, 被试即进入习得阶…”
InfluentialLi, J., Chen, W., Hu, Y., Caoyang, J., & Zheng, X. (2021) · Acta Psychologica Sinica · doi:10.3724/sp.j.1041.2021.00587 · Cited by 7
“…广州 510631) (4 广东省心理健康与认知科学重点实验室, 广州 510631) (5 东莞市东莞中学, 东莞 523120) (6 西安外国语大学学生心理健康教育中心, 西安 710128) 摘 要 在条件性恐惧记忆再巩固模型下, 预期错误被证明是引发记忆不稳定的必要条件, 但其在不同强度恐惧 记忆下的作用尚不明确。对于高强度可能导致的提取无效, 缺乏相应的探索以寻找解决办法, 而应激(stress)在其中 发挥的作用值得探索。本研究考察人类被试中, 预期错误在不同强度恐惧记忆下的作用, 以及提取之后施加外源性 应激对于消退进程的影响。结果发现, 对于较弱的恐惧记忆,…”
Reconsolidation and Fear Extinction: An Update
Raskin, M., & Monfils, M. (2023) · Current topics in behavioral neurosciences · doi:10.1007/7854_2023_438 · Cited by 9
Regulation of learned fear expression through the MgN-amygdala pathway
Ferrara, N. C., Trask, S., Pullins, S. E., & Helmstetter, F. J. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107526 · Cited by 7
Urcelay, G., & Miller, R. R. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00075-9 · Cited by 3
Brunswick, C. A., Carpenter, C. M., Dennis, N. A., & Kwapis, J. L. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106195 · Cited by 10
The lifetime impact of stress on fear regulation and cortical function
Trask, S., Kuczajda, M. T., & Ferrara, N. C. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109367 · Cited by 6
Tavares, T. F., Bueno, J. L. O., & Doyère, V. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1060587 · Cited by 8
“While prediction error is a critical factor in memory updating, reconsolidation and/or new learning, in Pavlovian conditioning (Debiec and Ledoux, 2004; Duvarci and Nader, 2004; Alberini, 2005; Lee H. J. et al., 2006; Lee J. L. et al., 2006; Lee, 2008), it is still questioned whether memory updating when acquired in o…”
BackgroundAkagi, K., Yamada, M., Saitoh, A., Oka, J., & Yamada, M. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.12.009 · Cited by 6
“It has been reported that reexposure to the context induces reconsolidation and extinction of fear memory simultaneously (Duvarci and Nader, 2004; Lee et al., 2006; Tronson and Taylor, 2007).”
Cox, W. R., Faliagkas, L., Besseling, A., van der Loo, R. J., Spijker, S., Kindt, M., & Rao‐Ruiz, P. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.893572 · Cited by 6
“Administering amnestic agents, such as propranolol, in close temporal proximity of memory reactivation seems to result in more durable reductions in fear responding (Dębiec et al., 2002; Dębiec and Ledoux, 2004; Duvarci and Nader, 2004; Bustos et al., 2006, but see Eisenberg and Dudai, 2004; Lattal and Abel, 2004).”
BackgroundEcker, B. (2017) · PsyArXiv (OSF Preprints) · doi:10.31234/osf.io/zrq2m · Cited by 6
Lin, B., Alganem, K., O'Donovan, S. M., Jin, Z. H., Naghavi, F., Miller, O. A., Ortyl, T. C., Ruan, Y. C., McCullumsmith, R. E., & Du, J. (2021) · Molecular Brain · doi:10.1186/s13041-021-00786-7 · Cited by 5
Picco, S., Bavassi, L., Fernández, R. S., & Pedreira, M. E. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.07.001 · Cited by 8
MacCallum, P. E., Cooze, J. B., Ward, J. M., Moore, K., & Blundell, J. J. (2024) · Behavioural Brain Research · doi:10.1016/j.bbr.2024.114855 · Cited by 6
“Unlike extinction alone, however, impaired reconsolidation does not result in a return of fear (e.g., reinstatement, renewal, spontaneous recovery) [30 – 32].”
BackgroundBarak, S., & Goltseker, K. (2023) · Current topics in behavioral neurosciences · doi:10.1007/7854_2022_411 · Cited by 5
A meta-analysis of the effect of protein synthesis inhibitors on rodent fear conditioning
Carneiro, C. F. D., Amorim, F. E., & Amaral, O. B. (2023) · Peer Community Journal · doi:10.24072/pcjournal.339 · Cited by 7
Ecker, B. (2024) · Journal of Psychiatry and Psychiatric Disorders · doi:10.26502/jppd.2572-519x0226 · Cited by 7
Using Reconsolidation and Extinction to Weaken Fear Memories in Animal Models
Jones, C. E., & Monfils, M. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-386892-3.00008-1 · Cited by 5
Molecular Mechanism of Memory Modification
Balaban, P. M. (2018) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-018-0624-2 · Cited by 4
Yoga and Mindfulness-Based Cognitive Therapy (Y-MBCT©): Use of Yoga in Its Entirety
Pradhan, B. (2014) · Springer eBooks · doi:10.1007/978-3-319-09105-1_7 · Cited by 3
Effects of Mineralocorticoid Receptors Blockade on FearMemory Reconsolidation in Rats
Vafaei, A. A., Pakdel, R., Nikzad, S., & Rashidy‐Pour, A. (2011) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 4
Wood, M. A. (2010) · Apollo (University of Cambridge) · doi:10.17863/cam.16464 · Cited by 3
“Additionally, Duvarci & Nader (2004) demonstrate successful reacquisition of fear responding after anisomycin-induced amnesia for a CS-shock association.”
BackgroundInfluentialHardwicke, T. E. (2017) · Thesis Commons (OSF Preprints) · doi:10.31237/osf.io/r4c32 · Cited by 4
“Several studies report that amnesia e ects in reconsolidation studies are lasting, despite attempts at reinstatement (e.g., Boccia, Blake, Acosta, & Baratti, 2005; Debiec et al., 2002; Duvarci & Nader, 2004).”
BackgroundInfluential
Metadata
- Authors
- Duvarci, S., & Nader, K.
- Affiliations
- W. M. Keck Foundation (US)
- McGill University (CA)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2004-10-20
- Volume
- 24
- Issue
- 42
- Pages
- 9269-9275
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6730081
- OpenAlex
- W2018795098
- Cited by
- 379
- References
- 39
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 6 · 2023: 13 · 2022: 18 · 2021: 15 · 2020: 14 · 2019: 14 · 2018: 16 · 2017: 22 · 2016: 18 · 2015: 24 · 2014: 23 · 2013: 21 · 2012: 24
- FWCI
- 9.75
- 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
- Alfred P. Sloan Foundation
- Volkswagen Foundation
- Canadian Institutes of Health Research
- 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
- fear memory reconsolidation, memory reactivation, protein synthesis inhibition, anisomycin, extinction, memory retrieval, memory consolidation, spontaneous recovery, reinstatement, auditory fear conditioning
- MeSH terms
- Amygdala, Animals, Anisomycin, Conditioning, Psychological, Extinction, Psychological, Fear, Male, Memory, Protein Synthesis Inhibitors, Time Factors, Rats, Sprague-Dawley, Rats
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