Section: Neuroscience
Topic: Neuroscience

A meta-analysis of the effect of protein synthesis inhibitors on rodent fear conditioning

10.24072/pcjournal.339 - Peer Community Journal, Volume 3 (2023), article no. e110.

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Systematic reviews and meta-analyses have been increasingly recognized for their potential value in pre-clinical research, but their applications have not been extensively explored in behavioral neuroscience. In this work, we studied protein synthesis inhibition, a classic intervention used to disrupt fear learning, reconsolidation, and extinction in rodents, to explore how meta-analyses can identify potential moderators of its effect. We initially performed separate meta-analyses for different injection sites and target sessions to evaluate the effect of the intervention in various scenarios. Heterogeneity was further investigated by multilevel meta-regression models aggregating various sites, with article or research group as additional levels. We detected robust effects of protein synthesis inhibitors on training and reconsolidation, but not on extinction, possibly due to the lower number of studies on the latter. Our analyses identified some well-established moderators, such as intervention timing and reexposure duration. However, other factors proposed as boundary conditions for reconsolidation, such as memory age and training strength, were not associated with effect size. While our results point to the value of meta-analyses in consolidating findings from the literature, we believe that associations suggested by data synthesis should ideally be verified by well-powered, rigorous confirmatory experiments.

Published online:
DOI: 10.24072/pcjournal.339
Type: Research article
Keywords: fear conditioning; preclinical meta-analysis; reproducibility;
Carneiro, Clarissa F. D. 1, 2; Amorim, Felippe E. 1; Amaral, Olavo B. 1

1 Institute of Medical Biochemistry Leopoldo de Meis, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
2 Berlin Institute of Health (BIH) at Charité, BIH QUEST Center for Responsible Research, Berlin, Germany
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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Carneiro, Clarissa F. D.; Amorim, Felippe E.; Amaral, Olavo B. A meta-analysis of the effect of protein synthesis inhibitors on rodent fear conditioning. Peer Community Journal, Volume 3 (2023), article  no. e110. doi : 10.24072/pcjournal.339. https://peercommunityjournal.org/articles/10.24072/pcjournal.339/

Peer reviewed and recommended by PCI : 10.24072/pci.neuro.100144

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Abate, G.; Colazingari, S.; Accoto, A.; Conversi, D.; Bevilacqua, A. Dendritic spine density and EphrinB2 levels of hippocampal and anterior cingulate cortex neurons increase sequentially during formation of recent and remote fear memory in the mouse, Behavioural Brain Research, Volume 344 (2018), pp. 120-131 | DOI

[2] Abel, T.; Nguyen, P.; Barad, M.; Deuel, T.; Kandel, E.; Bourtchouladze, R. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory, Cell, Volume 88 (1997), pp. 615-626 | DOI

[3] Abrari, K.; Rashidy-Pour, A.; Semnanian, S.; Fathollahi, Y. Administration of corticosterone after memory reactivation disrupts subsequent retrieval of a contextual conditioned fear memory: Dependence upon training intensity, Neurobiology of Learning and Memory, Volume 89 (2008), pp. 178-184 | DOI

[4] Ageta, H.; Ikegami, S.; Miura, M.; Masuda, M.; Migishima, R.; Hino, T.; Takashima, N.; Murayama, A.; Sugino, H.; Setou, M.; Kida, S.; Yokoyama, M.; Hasegawa, Y.; Tsuchida, K.; Aosaki, T.; Inokuchi, K. Activin plays a key role in the maintenance of long-term memory and late-LTP, Learning and Memory, Volume 17 (2010), pp. 176-185 | DOI

[5] Alfei, J.; Monti, R.; Molina, V.; Bueno, A.; Urcelay, G. Prediction error and trace dominance determine the fate of fear memories after post-training manipulations, Learning and Memory, Volume 22 (2015), pp. 385-400 | DOI

[6] Almeida-Corrêa, S.; Moulin, T.; Carneiro, C.; Gonçalves, M.; Junqueira, L.; Amaral, O. Calcineurin inhibition blocks within-, but not between-session fear extinction in mice, Learning and Memory, Volume 22 (2015), pp. 159-169 | DOI

[7] Amaral, O.; Neves, K. Reproducibility: expect less of the scientific paper, Nature, Volume 597 (2021), pp. 329-331 | DOI

[8] Amaral, O.; Neves, K.; Wasilewska-Sampaio, A.; Carneiro, C. The brazilian reproducibility initiative, eLife, Volume 8 (2019) | DOI

[9] Apergis-Schoute, A.; Dȩbiec, J.; Doyère, V.; LeDoux, J.; Schafe, G. Auditory fear conditioning and long-term potentiation in the lateral amygdala require ERK/MAP kinase signaling in the auditory thalamus: A role for presynaptic plasticity in the fear system, Journal of Neuroscience, Volume 25 (2005), pp. 5730-5739 | DOI

[10] Awad, W.; Ferreira, G.; Maroun, M. Dissociation of the Role of Infralimbic Cortex in Learning and Consolidation of Extinction of Recent and Remote Aversion Memory, Neuropsychopharmacology, Volume 40 (2015), pp. 2566-2575 | DOI

[11] Bal, N.; Rysakova, M.; Vinarskaya, A.; Ivanova, V.; Zuzina, A.; Balaban, P. Cued memory reconsolidation in rats requires nitric oxide, European Journal of Neuroscience, Volume 45 (2017), pp. 643-647 | DOI

[12] Ballarini, F.; Moncada, D.; Martinez, M.; Alen, N.; Viola, H. Behavioral tagging is a general mechanism of long-term memory formation, Proceedings of the National Academy of Sciences of the United States of America, Volume 106, 2009, pp. 14599-14604 | DOI

[13] Bannach-Brown, A.; Hair, K.; Bahor, Z.; Soliman, N.; MacLeod, M.; Liao, J. Technological advances in preclinical meta-research, BMJ Open Science, Volume 5 (2021), p. 100131 | DOI

[14] Barnes, P.; Thomas, K. Proteolysis of proBDNF Is a Key Regulator in the Formation of Memory, PLoS ONE, Volume 3 (2008), p. 3248 | DOI

[15] Barrientos, R.; Higgins, E.; Sprunger, D.; Watkins, L.; Rudy, J.; Maier, S. Memory for context is impaired by injecting anisomycin into dorsal hippocampus following context exploration, Behavioural Brain Research, Volume 134 (2002), pp. 299-306 | DOI

[16] Begley, C.; Ellis, L. Drug development: Raise standards for preclinical cancer research, Nature, Volume 483 (2012), p. 531-3 | DOI

[17] Bekinschtein, P.; Cammarota, M.; Igaz, L.; Bevilaqua, L.; Izquierdo, I.; Medina, J. Persistence of Long-Term Memory Storage Requires a Late Protein Synthesis- and BDNF- Dependent Phase in the Hippocampus, Neuron, Volume 53 (2007), pp. 261-277 | DOI

[18] Berman, D.; Dudai, Y. Memory extinction, learning anew, and learning the new: Dissociations in the molecular machinery of learning in cortex, Science, Volume 291 (2001), pp. 2417-2419 | DOI

[19] Bhattacharya, S.; Kimble, W.; Buabeid, M.; Bhattacharya, D.; Bloemer, J.; Alhowail, A.; Reed, M.; Dhanasekaran, M.; Escobar, M.; Suppiramaniam, V. Altered AMPA receptor expression plays an important role in inducing bidirectional synaptic plasticity during contextual fear memory reconsolidation, Neurobiology of Learning and Memory, Volume 139 (2017), pp. 98-108 | DOI

[20] Biedenkapp, J.; Rudy, J. Context memories and reactivation: constraints on the reconsolidation hypothesis, Behavioral neuroscience, Volume 118 (2004), pp. 956-964 | DOI

[21] Blondel, V.; Guillaume, J.; Lambiotte, R.; Lefebvre, E. Fast unfolding of communities in large networks, Journal of Statistical Mechanics: Theory and Experiment (2008), p. 10008 | DOI

[22] Blum, S.; Runyan, J.; Dash, P. Inhibition of prefrontal protein synthesis following recall does not disrupt memory for trace fear conditioning, BMC neuroscience, Volume 7 (2006), p. 67 | DOI

[23] Blundell, J.; Kouser, M.; Powell, C. Systemic inhibition of mammalian target of rapamycin inhibits fear memory reconsolidation, Neurobiology of Learning and Memory, Volume 90 (2008), pp. 28-35 | DOI

[24] Bourtchouladze, R.; Abel, T.; Berman, N.; Gordon, R.; Lapidus, K.; Kandel, E. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA, Learning and Memory, Volume 5 (1998), pp. 365-374 | DOI

[25] Bouton, M. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction, Biological Psychiatry, Volume 52 (2002), pp. 976-986 | DOI

[26] Cai, W.; Blundell, J.; Han, J.; Greene, R.; Powell, C. Postreactivation glucocorticoids impair recall of established fear memory, Journal of Neuroscience, Volume 26 (2006), pp. 9560-9566 | DOI

[27] Carneiro, C.; Moulin, T.; Macleod, M.; Amaral, O. Effect size and statistical power in the rodent fear conditioning literature - a systematic review, PLoS ONE (2018) | DOI

[28] Carneiro, C.; Amorim, F.; Amaral, O. Meta-analysis of protein synthesis inhibitors in fear conditioning, OSF (2018) | DOI

[29] de Carvalho Myskiw; J; Furini, C.; Schmidt, B.; Ferreira, F.; Izquierdo, I.; F, F.; I, I. Extinction learning, which consists of the inhibition of retrieval, can be learned without retrieval, Proceedings of the National Academy of Sciences of the United States of America, Volume 112, 2015, p. 230-3 | DOI

[30] Chai, N.; Liu, J.-F.; Xue, Y.-X.; Yang, C.; Yan, W.; Wang, H.-M.; Luo, Y.-X.; Shi, H.-S.; Wang, J.-S.; Bao, Y.-P.; Meng, S.-Q.; Ding, Z.-B.; Wang, X.-Y.; Lu, L. Delayed Noradrenergic Activation in the Dorsal Hippocampus Promotes the Long-Term Persistence of Extinguished Fear, NEUROPSYCHOPHARMACOLOGY, Volume 39 (2014), pp. 1933-1945 | DOI

[31] Clayton, J.; Collins, F. Policy: NIH to balance sex in cell and animal studies, Nature, Volume 509 (2014), p. 282-3 | DOI

[32] Davis, H.; Squire, L. Protein synthesis and memory: A review, Psychological Bulletin, Volume 96 (1984), pp. 518-559 | DOI

[33] Dȩbiec, J.; Díaz-Mataix, L.; Bush, D.; Doyère, V.; Ledoux, J. The amygdala encodes specific sensory features of an aversive reinforcer, Nature Neuroscience, Volume 13 (2010), pp. 536-537 | DOI

[34] Deębiec, J.; Doyère, V.; Nader, K.; LeDoux, J. E. Directly reactivated, but not indirectly reactivated, memories undergo reconsolidation in the amygdala, Proceedings of the National Academy of Sciences, Volume 103 (2006) no. 9, pp. 3428-3433 | DOI

[35] Debiec, J.; LeDoux, J.; Nader, K. Cellular and systems reconsolidation in the hippocampus, Neuron, Volume 36 (2002), pp. 527-538 | DOI

[36] Duval, S. The Trim and Fill Method, Publication Bias in Meta-Analysis: prevention, John Wiley Sons Ltd, 2005

[37] Duval, S.; Tweedie, R. A Nonparametric “Trim and Fill” Method of Accounting for Publication Bias in Meta-Analysis, Journal of the American Statistical Association, Volume 95 (2000), pp. 89-98 | DOI

[38] Duval, S.; Tweedie, R. Trim and Fill: A Simple Funnel-Plot-Based Method of Testing and Adjusting for Publication Bias in Meta-Analysis, Biometrics, Volume 56 (2000), pp. 455-463 | DOI

[39] Duvarci, S.; ben Mamou, C.; Nader, K. Extinction is not a sufficient condition to prevent fear memories from undergoing reconsolidation in the basolateral amygdala, European Journal of Neuroscience, Volume 24 (2006), pp. 249-260 | DOI

[40] Duvarci, S.; Nader, K. Characterization of fear memory reconsolidation, Journal of Neuroscience (2004), pp. 9269-9275 (Society for Neuroscience.) | DOI

[41] Duvarci, S.; Nader, K.; LeDoux, J. Activation of extracellular signal-regulated kinase-mitogen-activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning, European Journal of Neuroscience, Volume 21 (2005), pp. 283-289 | DOI

[42] Egger, M.; Smith, G.; Schneider, M.; Minder, C. Bias in meta-analysis detected by a simple, graphical test, British Medical Journal, Volume 315 (1997), pp. 629-634 | DOI

[43] Einarsson, E.; Nader, K. Involvement of the anterior cingulate cortex in formation, consolidation, and reconsolidation of recent and remote contextual fear memory, Learning and Memory, Volume 19 (2012), pp. 449-452 | DOI

[44] Eisenberg, M.; Dudai, Y. Reconsolidation of fresh, remote, and extinguished fear memory in medaka: old fears don’t die, European Journal of Neuroscience, Volume 20 (2004), pp. 3397-3403 | DOI

[45] Eisenberg, M.; Kobilo, T.; Berman, D.; Dudai, Y. Stability of retrieved memory: inverse correlation with trace dominance. Science, 2003 (301, 1102–1104.) | DOI

[46] Errington, T.; Mathur, M.; Soderberg, C.; Denis, A.; Perfito, N.; Iorns, E.; Nosek, B. Investigating the replicability of preclinical cancer biology, eLife, Volume 10 (2021) | DOI

[47] Ferrara, N.; Cullen, P.; Pullins, S.; Rotondo, E.; Helmstetter, F. Input from the medial geniculate nucleus modulates amygdala encoding of fear memory discrimination, Learning and Memory, Volume 24 (2017), pp. 414-421 | DOI

[48] Fischer, A.; Sananbenesi, F.; Schrick, C.; Spiess, J.; Radulovic, J. Distinct Roles of Hippocampal De Novo Protein Synthesis and Actin Rearrangement in Extinction of Contextual Fear, Journal of Neuroscience, Volume 24 (2004), pp. 1962-1966 | DOI

[49] França, T.; Monserrat, J. Reproducibility crisis in science or unrealistic expectations?, EMBO reports, Volume 19 (2018), p. 46008 | DOI

[50] Frankland, P.; Ding, H.; Takahashi, E.; Suzuki, A.; Kida, S.; Silva, A. Stability of recent and remote contextual fear memory, Learning and Memory, Volume 13 (2006), pp. 451-457 | DOI

[51] Frankland, P.; Josselyn, S.; Anagnostaras, S.; Kogan, J.; Takahashi, E.; Silva, A. Consolidation of CS and US representations in associative fear conditioning, Hippocampus, Volume 14 (2004), pp. 557-569 | DOI

[52] Garofalo, S. Bridging consensus and controversy in fear conditioning research via meta-analysis, Peer Community in Neuroscience, Volume 1 (2023), p. 100144 | DOI

[53] Girardi, B.; Ribeiro, D.; Signor, C.; Muller, M.; Gais, M.; Mello, C.; Rubin, M. Spermidine-induced improvement of reconsolidation of memory involves calcium-dependent protein kinase in rats, Learning Memory, Volume 23 (2016), pp. 21-28 | DOI

[54] Gould, T.; Wilkinson, D.; Yildirim, E.; Poole, R.; Leach, P.; Simmons, S. Nicotine shifts the temporal activation of hippocampal protein kinase A and extracellular signal-regulated kinase 1⁄2 to enhance long-term, but not short-term, hippocampus-dependent memory, Neurobiology of Learning and Memory, Volume 109 (2014), pp. 151-159 | DOI

[55] Haubrich, J.; Crestani, A.; Cassini, L.; Santana, F.; Sierra, R.; O, A. L.; Quillfeldt, J. Reconsolidation Allows Fear Memory to Be Upyeard to a Less Aversive Level through the Incorporation of Appetitive Information, NEUROPSYCHOPHARMACOLOGY, Volume 40 (2015), pp. 315-326 | DOI

[56] Haubrich, J.; Machado, A.; Boos, F.; Crestani, A.; Sierra, R.; Alvares, L.; Quillfeldt, J. Enhancement of extinction memory by pharmacological and behavioral interventions targeted to its reactivation, Scientific Reports, Volume 7 (2017), pp. 1-11 | DOI

[57] von Hertzen, L. Memory Reconsolidation Engages Only a Subset of Immediate-Early Genes Induced during Consolidation, Journal of Neuroscience, Volume 25 (2005), pp. 1935-1942 | DOI

[58] Hoeffer, C.; Cowansage, K.; Arnold, E.; Banko, J.; Moerke, N.; Rodriguez, R.; Schmidt, E.; Klosi, E.; Chorev, M.; Lloyd, R.; Pierre, P.; Wagner, G.; LeDoux, J.; Klann, E. Inhibition of the interactions between eukaryotic initiation factors 4E and 4G impairs long-term associative memory consolidation but not reconsolidation, Proceedings of the National Academy of Sciences of the United States of America, Volume 108, 2011, pp. 3383-3388 | DOI

[59] Holehonnur, R.; Phensy, A.; Kim, L.; Milivojevic, M.; Vuong, D.; Daison, D.; Alex, S.; Tiner, M.; Jones, L.; Kroener, S.; Ploski, J. Increasing the GluN2A/GluN2B ratio in neurons of the mouse basal and lateral amygdala inhibits the modification of an existing fear memory trace, Journal of Neuroscience, Volume 36 (2016), pp. 9490-9504 | DOI

[60] Huff, N.; Rudy, J. The amygdala modulates hippocampus-dependent context memory formation and stores cue-shock associations, Behavioral neuroscience, Volume 118 (2004), pp. 53-62 | DOI

[61] Ioannidis, J.; Trikalinos, T. An exploratory test for an excess of significant findings, Clinical Trials, Volume 4 (2007), pp. 245-253 | DOI

[62] Jarome, T.; Ferrara, N.; Kwapis, J.; Helmstetter, F. Contextual Information Drives the Reconsolidation-Dependent Updating of Retrieved Fear Memories, Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology, Volume 40 (2015), pp. 3044-3052 | DOI

[63] Jarome, T.; Ferrara, N.; Kwapis, J.; Helmstetter, F. CaMKII regulates proteasome phosphorylation and activity and promotes memory destabilization following retrieval, Neurobiology of Learning and Memory, Volume 128 (2016), pp. 103-109 | DOI

[64] Jarome, T.; Kwapis, J.; Werner, C.; Parsons, R.; Gafford, G.; Helmstetter, F. The timing of multiple retrieval events can alter GluR1 phosphorylation and the requirement for protein synthesis in fear memory reconsolidation, Learning and Memory, Volume 19 (2012), pp. 300-306 | DOI

[65] Kim, J.; Song, B.; Hong, I.; Kim, J.; Lee, J.; Park, S.; Yong Eom, J.; Lee, C.; Lee, S.; Choi, S. Reactivation of Fear Memory Renders Consoliyeard Amygdala Synapses Labile, Journal of Neuroscience, Volume 30 (2010), pp. 9631-9640 | DOI

[66] Kishioka, A.; Uemura, T.; Fukushima, F.; Mishina, M. Consolidation of auditory fear memories formed by weak unconditioned stimuli requires NMDA receptor activation and de novo protein synthesis in the striatum, Molecular brain, Volume 6 (2013), p. 17 | DOI

[67] Kochli, D.; Campbell, T.; Hollingsworth, E.; Lab, R.; Postle, A.; Perry, M.; Mordzinski, V.; Quinn, J. Combined administration of MK-801 and cycloheximide produces a delayed potentiation of fear discrimination memory extinction, Behavioral Neuroscience, Volume 132 (2018), pp. 99-105 | DOI

[68] Kochli, D.; Thompson, E.; Fricke, E.; Postle, A.; Quinn, J. The amygdala is critical for trace, delay, and contextual fear conditioning, Learning and Memory, Volume 22 (2015), pp. 92-100 | DOI

[69] Kumar, T.; Jha, S. Influence of cued-fear conditioning and its impairment on NREM sleep, Neurobiology of Learning and Memory, Volume 144 (2017), pp. 155-165 | DOI

[70] Kwak, C.; Choi, J.-H.; Bakes, J.; Lee, K.; Kaang, B.-K. Effect of intensity of unconditional stimulus on reconsolidation of contextual fear memory, The Korean journal of physiology pharmacology : official journal of the Korean Physiological Society and the Korean Society of Pharmacology, Volume 16 (2012), pp. 293-296 | DOI

[71] Kwapis, J.; Jarome, T.; Ferrara, N.; Helmstetter, F. Updating Procedures can Reorganize the Neural Circuit Supporting a Fear Memory, official publication of the American College of Neuropsychopharmacology, Neuropsychopharmacology, 2017 | DOI

[72] Kwapis, J.; Jarome, T.; Lee, J.; Helmstetter, F. The retrosplenial cortex is involved in the formation of memory for context and trace fear conditioning, Neurobiology of learning and memory, Volume 123 (2015), pp. 110-116 | DOI

[73] Kwapis, J.; Jarome, T.; Schiff, J.; Helmstetter, F. Memory consolidation in both trace and delay fear conditioning is disrupted by intra-amygdala infusion of the protein synthesis inhibitor anisomycin, Learning memory (Cold Spring Harbor, Volume N.Y.), 18 (2011), pp. 728-732 | DOI

[74] Lattal, K.; Abel, T. Different requirements for protein synthesis in acquisition and extinction of spatial preferences and context-evoked fear, Journal of Neuroscience, Volume 21 (2001), pp. 5773-5780 | DOI

[75] Lattal, K.; Abel, T. Behavioral impairments caused by injections of the protein synthesis inhibitor anisomycin after contextual retrieval reverse with time, Proceedings of the National Academy of Sciences of the United States of America, Volume 101, 2004, pp. 4667-4672 | DOI

[76] Lee, S.; Choi, J.; Lee, N.; Lee, H.; Kim, J.; Yu, N.; Choi, S.; Lee, S.; Kim, H.; Kaang, B. Synaptic protein degradation underlies destabilization of retrieved fear memory, Science, Volume 319 (2008), pp. 1253-1256 | DOI

[77] Lopez, J.; Gamache, K.; Schneider, R.; Nader, K. Memory retrieval requires ongoing protein synthesis and NMDA receptor activity-mediated AMPA receptor trafficking, Journal of Neuroscience, Volume 35 (2015), pp. 2465-2475 | DOI

[78] Luyten, L.; Schnell, A.; Schroyens, N.; Beckers, T. Lack of drug-induced post-retrieval amnesia for auditory fear memories in rats, BMC Biology, Volume 19 (2021), p. 17 | DOI

[79] Mac Callum, P.; Hebert, M.; Adamec, R.; Blundell, J. Systemic inhibition of mTOR kinase via rapamycin disrupts consolidation and reconsolidation of auditory fear memory, Neurobiology of Learning and Memory, Volume 112 (2014), pp. 176-185 | DOI

[80] Maciejak, P.; Szyndler, J.; Lehner, M.; Turzyńska, D.; Sobolewska, A.; Bidziński, A.; Płaźnik, A. The differential effects of protein synthesis inhibition on the expression and reconsolidation of pentylenetetrazole kindled seizures, Epilepsy and Behavior, Volume 18 (2010), pp. 193-200 | DOI

[81] Macleod, M.; Lawson McLean, A.; Kyriakopoulou, A.; Serghiou, S.; Wilde, A.; Sherratt, N.; Hirst, T.; Hemblade, R.; Bahor, Z.; Nunes-Fonseca, C.; Potluru, A.; Thomson, A.; Baginskitae, J.; Egan, K.; Vesterinen, H.; Currie, G.; Churilov, L.; Howells, D.; Sena, E.; Sena, E. Risk of Bias in Reports of In Vivo Research: A Focus for Improvement, PLOS Biology, Volume 13 (2015), p. 1002273 | DOI

[82] Mamiya, N.; Fukushima, H.; Suzuki, A.; Matsuyama, Z.; Homma, S.; Frankland, P.; Kida, S. Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory, Journal of Neuroscience, Volume 29 (2009), pp. 402-413 | DOI

[83] Mamou, C.; Gamache, K.; Nader, K. NMDA receptors are critical for unleashing consoliyeard auditory fear memories, Nature Neuroscience, Volume 9 (2006), pp. 1237-1239 | DOI

[84] Milekic, M.; Alberini, C. Temporally graded requirement for protein synthesis following memory reactivation, Neuron, Volume 36 (2002), pp. 521-525 | DOI

[85] Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.; Altman, D.; Antes, G.; Atkins, D.; Barbour, V.; Barrowman, N.; Berlin, J.; Clark, J.; Clarke, M.; Cook, D.; D’Amico, R.; Deeks, J.; Devereaux, P.; Dickersin, K.; Egger, M.; Ernst, E.; Gøtzsche, P.; Grimshaw, J.; Guyatt, G.; Higgins, J.; Ioannidis, J.; Kleijnen, J.; Lang, T.; Magrini, N.; McNamee, D.; Moja, L.; Mulrow, C.; Napoli, M.; Oxman, A.; Pham, B.; Rennie, D.; Sampson, M.; Schulz, K.; Shekelle, P.; Tovey, D.; Tugwell, P. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement, PLoS Medicine, Volume 6 (2009) | DOI

[86] Motanis, H.; Maroun, M. Differential involvement of protein synthesis and actin rearrangement in the reacquisition of contextual fear conditioning, Hippocampus, Volume 22 (2012), pp. 494-500 | DOI

[87] Moulin, T.; Amaral, O. Using collaboration networks to identify authorship dependence in meta‐analysis results, Research Synthesis Methods, Volume 11 (2020), p. 1430 | DOI

[88] Nader, K. Memory traces unbound, Trends in Neurosciences, Volume 26 (2003), pp. 65-72 | DOI

[89] Nader, K.; Schafe, G.; Le Doux, J. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval, Nature, Volume 406 (2000), pp. 722-726 | DOI

[90] Nakayama, D.; Baraki, Z.; Onoue, K.; Ikegaya, Y.; Matsuki, N.; Nomura, H. Frontal association cortex is engaged in stimulus integration during associative learning, Current Biology, Volume 25 (2015), pp. 117-123 | DOI

[91] Nakayama, D.; Yamasaki, Y.; Matsuki, N.; Nomura, H. Post-retrieval late process contributes to persistence of reactivated fear memory, Learning and Memory, Volume 20 (2013), pp. 307-310 | DOI

[92] Nomura, H.; Matsuki, N. Ethanol enhances reactivated fear memories, NEUROPSYCHOPHARMACOLOGY, Volume 33 (2008), pp. 2912-2921 | DOI

[93] Open Science Collaboration PSYCHOLOGY. Estimating the reproducibility of psychological science, Science, Volume 349 (2015), p. 4716 | DOI

[94] Parsons, R.; Gafford, G.; Baruch, D.; Riedner, B.; Helmstetter, F. Long-term stability of fear memory depends on the synthesis of protein but not mRNA in the amygdala, European Journal of Neuroscience, Volume 23 (2006), pp. 1853-1859 | DOI

[95] Patricio Casanova, J.; Madrid, C.; Contreras, M.; Rodriguez, M.; Vasquez, M.; Torrealba, F. A role for the interoceptive insular cortex in the consolidation of learned fear, BEHAVIOURAL BRAIN RESEARCH, Volume 296 (2016), pp. 70-77 | DOI

[96] Pedreira, M.; Pérez-Cuesta, L.; Maldonado, H. Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction, Learning and Memory, Volume 11 (2004), pp. 579-585 | DOI

[97] Poulos, A.; Ponnusamy, R.; Dong, H.-W.; Fanselow, M. Compensation in the neural circuitry of fear conditioning awakens learning circuits in the bed nuclei of the stria terminalis, Proceedings of the National Academy of Sciences of the United States of America, Volume 107, 2010, pp. 14881-14886 | DOI

[98] Prinz, F.; Schlange, T.; Asadullah, K. Believe it or not: how much can we rely on published data on potential drug targets?, Nature reviews. Drug discovery, Volume 10 (2011), p. 712 | DOI

[99] R Core Team R: A Language and Environment for Statistical Computing, 2022

[100] Radwanska, K.; Medvedev, N.; Pereira, G.; Engmann, O.; Thiede, N.; Moraes, M.; Villers, A.; Irvine, E.; Maunganidze, N.; Pyza, E.; Ris, L.; Szymańska, M.; Lipiński, M.; Kaczmarek, L.; Stewart, M.; Giese, K. Mechanism for long-term memory formation when synaptic strengthening is impaired, Proceedings of the National Academy of Sciences of the United States of America, Volume 108, 2011, pp. 18471-18475 | DOI

[101] Reis, D.; Jarome, T.; Helmstetter, F. Memory formation for trace fear conditioning requires ubiquitin-proteasome mediated protein degradation in the prefrontal cortex, Frontiers in Behavioral Neuroscience, Volume 7 (2013), p. 150 | DOI

[102] Remaud, J.; Ceccom, J.; Carponcy, J.; Dugué, L.; Menchon, G.; Pech, S.; Halley, H.; Francés, B.; Dahan, L. Anisomycin injection in area CA3 of the hippocampus impairs both short-term and long-term memories of contextual fear, Learning and Memory, Volume 21 (2014), pp. 311-315 | DOI

[103] Rizzo, V.; Touzani, K.; Raveendra, B.; Swarnkar, S.; Lora, J.; Kadakkuzha, B.; Liu, X.; Zhang, C.; Betel, D.; Stackman, R.; Puthanveettil, S. Encoding of Contextual Fear Memory Requires De Novo Proteins in the Prelimbic Cortex, Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, Volume 2 (2017), pp. 158-169 | DOI

[104] Rotondo, F.; Biddle, K.; Chen, J.; Ferencik, J.; d’Esneval, M.; Milton, A. Lack of Effect of Propranolol on the Reconsolidation of Conditioned Fear Memory due to a Failure to Engage Memory Destabilisation, Neuroscience, Volume 480 (2022), pp. 9-18 | DOI

[105] Roy, D.; Muralidhar, S.; Smith, L.; Tonegawa, S. Silent memory engrams as the basis for retrograde amnesia, Proceedings of the National Academy of Sciences of the United States of America, Volume 114, 2017, p. 9972 | DOI

[106] Rudy, J.; Matus-Amat, P. The ventral hippocampus supports a memory representation of context and contextual fear conditioning: implications for a unitary function of the hippocampus, Behavioral neuroscience, Volume 119 (2005), pp. 154-163 | DOI

[107] Runyan, J.; Dash, P. Inhibition of hippocampal protein synthesis following recall disrupts expression of episodic-like memory in trace conditioning, Hippocampus, Volume 15 (2005), pp. 333-339 | DOI

[108] Sacchetti, B.; Sacco, T.; Strata, P. Reversible inactivation of amygdala and cerebellum but not perirhinal cortex impairs reactivated fear memories, European Journal of Neuroscience, Volume 25 (2007), pp. 2875-2884 | DOI

[109] Santini, E.; Ge, H.; Ren, K.; Ortiz, S.; Quirk, G. Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex, Journal of Neuroscience, Volume 24 (2004), pp. 5704-5710 | DOI

[110] Schafe, G.; LeDoux, J. Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala, The Journal of neuroscience : the official journal of the Society for Neuroscience, Volume 20 (2000), p. 96 | DOI

[111] Scharf, M.; Woo, N.; Lattal, K.; Young, J.; Nguyen, P.; Abel, T. Protein Synthesis Is Required for the Enhancement of Long-Term Potentiation and Long-Term Memory by Spaced Training, Journal of Neurophysiology, Volume 87 (2002), pp. 2770-2777 | DOI

[112] Schimanski, L.; Nguyen, P. Multidisciplinary approaches for investigating the mechanisms of hippocampus-dependent memory: A focus on inbred mouse strains, Neuroscience and Biobehavioral Reviews, Volume 28 (2004), pp. 463-483 | DOI

[113] Schmidt, S.; Furini, C.; Zinn, C.; Cavalcante, L.; Ferreira, F.; Behling, J.; Myskiw, J.; Izquierdo, I. Modulation of the consolidation and reconsolidation of fear memory by three different serotonin receptors in hippocampus, Neurobiology of Learning and Memory, Volume 142 (2017), pp. 48-54 | DOI

[114] Schroyens, N.; Alfei, J.; Schnell, A.; Luyten, L.; Beckers, T. Limited replicability of drug-induced amnesia after contextual fear memory retrieval in rats, Neurobiology of Learning and Memory, Volume 166 (2019), p. 107105 | DOI

[115] Schroyens, N.; Sigwald, E.; Den Noortgate, W.; Beckers, T.; Luyten, L. Reactivation-dependent amnesia for contextual fear memories: Evidence for publication bias, eNeuro, Volume 8 (2021), pp. 1-16 | DOI

[116] Sevenster, D.; Beckers, T.; Kindt, M. Prediction error demarcates the transition from retrieval, to reconsolidation, to new learning, Learning and Memory, Volume 21 (2014), pp. 580-584 | DOI

[117] Signor, C.; Temp, F.; Mello, C.; Oliveira, M.; Girardi, B.; Gais, M.; Funck, V.; Rubin, M. Intrahippocampal infusion of spermidine improves memory persistence: Involvement of protein kinase A, Neurobiology of Learning and Memory, Volume 131 (2016), pp. 18-25 | DOI

[118] Soeter, M.; Kindt, M. High Trait Anxiety: A Challenge for Disrupting Fear Memory Reconsolidation, PLOS ONE, Volume 8 (2013) | DOI

[119] Song, Z.; Chen, H.; Xu, W.; Wu, S.; Zhu, G. Basolateral amygdala calpain is required for extinction of contextual fear-memory, Neurobiology of Learning and Memory, Volume 155 (2018), pp. 180-188 | DOI

[120] Stafford, J.; Lattal, K. Direct comparisons of the size and persistence of anisomycin-induced consolidation and reconsolidation deficits, Learning and Memory, Volume 16 (2009), pp. 494-503 | DOI

[121] Stanley, D.; Spence, J. Expectations for Replications: Are Yours Realistic? Perspectives on psychological science, a journal of the Association for Psychological Science, Volume 9 (2014), p. 305-18 | DOI

[122] Steward, O.; Popovich, P.; Dietrich, W.; Kleitman, N. Replication and reproducibility in spinal cord injury research, Experimental Neurology, Volume 233 (2012), pp. 597-605 | DOI

[123] Stiedl, O.; Palve, M.; Radulovic, J.; Birkenfeld, K.; Spiess, J. Differential impairment of auditory and contextual fear conditioning by protein synthesis inhibition in C57BL/6N mice, Behavioral Neuroscience, Volume 113 (1999), pp. 496-506 | DOI

[124] Suzuki, A.; Josselyn, S.; Frankland, P.; Masushige, S.; Silva, A.; Kida, S. Memory reconsolidation and extinction have distinct temporal and biochemical signatures, Journal of Neuroscience, Volume 24 (2004), pp. 4787-4795 | DOI

[125] Suzuki, A.; Mukawa, T.; Tsukagoshi, A.; Frankland, P.; Kida, S. Activation of LVGCCs and CB1 receptors required for destabilization of reactivated contextual fear memories, Learning and Memory, Volume 15 (2008), pp. 426-433 | DOI

[126] Tannenbaum, C.; Ellis, R.; Eyssel, F.; Zou, J.; Schiebinger, L. Sex and gender analysis improves science and engineering, Nature, Volume 575 (2019), pp. 137-146 | DOI

[127] Tiunova, A.; Anokhin, K.; Rose, S. Two critical periods of protein and glycoprotein synthesis in memory consolidation for visual categorization learning in chicks, Learning and Memory, Volume 4 (1998), pp. 401-410 | DOI

[128] Trent, S.; Barnes, P.; Hall, J.; Thomas, K. Rescue of long-term memory after reconsolidation blockade, Nature Communications, Volume 6 (2015), pp. 1-7 | DOI

[129] Vesterinen, H.; Sena, E.; Egan, K.; Hirst, T.; Churolov, L.; Currie, G.; Antonic, A.; Howells, D.; Macleod, M. Meta-analysis of data from animal studies: A practical guide, Journal of Neuroscience Methods, Volume 221 (2014), pp. 92-102 | DOI

[130] Vianna, M.; Szapiro, G.; McGaugh, J.; Medina, J.; Izquierdo, I. Retrieval of memory for fear-motivated training initiates extinction requiring protein synthesis in the rat hippocampus, Proceedings of the National Academy of Sciences of the United States of America, Volume 98, 2001, p. 12251-4 | DOI

[131] Viosca, J.; Armentia, M.; Jancic, D.; Barco, A. Enhanced CREB-dependent gene expression increases the excitability of neurons in the basal amygdala and primes the consolidation of contextual and cued fear memory, Learning and Memory, Volume 16 (2009), pp. 193-197 | DOI

[132] Wang, S.; Oliveira Alvares, L.; Nader, K. Cellular and systems mechanisms of memory strength as a constraint on auditory fear reconsolidation, Nature Neuroscience, Volume 12 (2009), pp. 905-912 | DOI

[133] Wanisch, K.; Tang, J.; Mederer, A.; Wotjak, C. Trace fear conditioning depends on NMDA receptor activation and protein synthesis within the dorsal hippocampus of mice, Behavioural brain research, Volume 157 (2005), pp. 63-69 | DOI

[134] Wilensky, A.; Schafe, G.; Kristensen, M.; LeDoux, J. Rethinking the fear circuit: The central nucleus of the amygdala is required for the acquisition, consolidation, and expression of pavlovian fear conditioning, Journal of Neuroscience, Volume 26 (2006), pp. 12387-12396 | DOI

[135] Wotjak, C. Sound check, stage design and screen plot – how to increase the comparability of fear conditioning and fear extinction experiments, Psychopharmacology, Volume 236 (2019), pp. 33-48 | DOI

[136] XinChun, J.; XueLian, Q.; XiaoFei, Y.; BaoMing, L. Protein synthesis inhibition in the basolateral nucleus of amygdala facilitates extinction of auditory fear memory, CHINESE SCIENCE BULLETIN, Volume 52 (2007), pp. 2532-2542 | DOI

[137] Yang, C.-H.; Huang, C.-C.; Hsu, K.-S. Generalization of fear inhibition by disrupting hippocampal protein synthesis-dependent reconsolidation process, Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology, Volume 36 (2011), pp. 1992-2008 | DOI

[138] Yim, A.; Moraes, C.; Ferreira, T.; Oliveira, M. Protein synthesis inhibition in the basolateral amygdala following retrieval does not impair expression of morphine-associated conditioned place preference, Behavioural brain research, Volume 171 (2006), pp. 162-169 | DOI

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