The role of NMDA glutamate receptors, PKA, MAPK, and CAMKII in the hippocampus in extinction of conditioned fear
Abstract
Pavlovian conditioning involves the association of initially neutral conditioned stimuli (CS) with unconditioned stimuli (US) that elicit a response. In contextual fear conditioning in rodents, the CS is the context of a training apparatus and the US is a foot shock. Retrieval of memory of the training is tested by presenting the CS alone. But a retrieval test also initiates extinction of the conditioned response. That is, presentation of the CS alone results in new learning, i.e., the CS no longer predicts the US. Here we report that extinction is triggered by two hippocampal signaling pathways underlying retrieval (the cAMP‐dependent protein kinase and the mitogen‐activated protein kinase pathways) and two other mechanisms that become activated at the same time and are not necessary for retrieval (N‐methyl‐D‐aspartate glutamatergic receptors and the calcium/calmodulin‐dependent protein kinase II signaling pathway). Thus, the molecular mechanisms underlying acquisition and/or consolidation of the memory for extinction are similar to those described for the acquisition and/or consolidation of the original contextual fear. Hippocampus 2003;13:53–58. © 2003 Wiley‐Liss, Inc.
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?
Hippocampal NMDA receptors and subsequent signaling pathways are involved in the mechanism for extinction of contextual fear.
“In addition to amygdaloid NMDA receptors, emerging evidence has recently indicated that hippocampal NMDA receptors (NMDARs) and subsequent signaling pathways are involved in the mechanism for extinction of contextual fear (Bevilaqua et al, 2005;Szapiro et al, 2003).”
From Effects of Single Prolonged Stress and D-Cycloserine on Contextual Fear Extinction and Hippocampal NMDA Receptor Expression in a Rat Model of PTSD (2008) · cites this paper as Szapiro et al, 2003
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Memory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250 · see citing works
Self-citationLedent, C. A., Valverde, O., Cossu, G., Petitet, F., Aubert, J.-F., Beslot, F., Böhme, G. A., Impérato, A., Pedrazzini, T., Roques, B. P., et al. (1999) · Science · doi:10.1126/science.283.5400.401 · Cited by 3,612 · see citing works
Synaptic Plasticity and Memory: An Evaluation of the Hypothesis
Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.649 · Cited by 2,794 · see citing works
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
Availability versus accessibility of information in memory for words
Tulving, E., & Pearlstone, Z. (1966) · Journal of Verbal Learning and Verbal Behavior · doi:10.1016/s0022-5371(66)80048-8 · Cited by 1,512 · see citing works
Izquierdo, I., & Medina, J. H. (1997) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1997.3799 · Cited by 959 · see citing works
Self-citationConditioned Reflexes and Neuron Organization.
(1949) · Annals of Internal Medicine · doi:10.7326/0003-4819-31-6-1133_1 · Cited by 688 · see citing works
Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala
Falls, W., Miserendino, M., & Davis, M. (1992) · The Journal of Neuroscience · doi:10.1523/jneurosci.12-03-00854.1992 · Cited by 673 · see citing works
Bernabeu, R., Bevilaqua, L. R., Ardenghi, P. G., Bromberg, E., Schmitz, P. K., Bianchin, M. M., Izquierdo, I., & Medina, J. H. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.7041 · Cited by 499 · see citing works
Self-citationBerman, D. E., & Dudai, Y. (2001) · Science · doi:10.1126/science.1058165 · Cited by 472 · see citing works
van Kesteren, R. E., Syed, N. I., Munno, D. W., Bouwman, J., Feng, Z., Geraerts, W. P. M., & Smit, A. B. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-16-j0004.2001 · Cited by 471 · see citing works
Hippocampal Inactivation Disrupts Contextual Retrieval of Fear Memory after Extinction
Corcoran, K. A., & Maren, S. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01720.2001 · Cited by 455 · cited 8× · see citing works
“Further, they show that the actual level of retrieval performance in the first test is not crucial for extinction; probably the essential element is merely the detection of the CS–“no shock” association (Konorski, 1948; Pavlov, 1956; Corcoran and Maren, 2001).”
BackgroundInfluentialHall, J., Thomas, K. L., & Everitt, B. J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-06-02186.2001 · Cited by 381 · see citing works
Vianna, M. R. M. R., Alonso, M., Viola, H., Quevedo, J., de Paris, F., Furman, M., de Stein, M. L., Medina, J. H., & Izquierdo, I. (2000) · Learning & Memory · doi:10.1101/lm.34600 · Cited by 284 · see citing works
Self-citationNeuroscience: Breaking Down Scientific Barriers to the Study of Brain and Mind
Kandel, E. R., & Squire, L. R. (2000) · Science · doi:10.1126/science.290.5494.1113 · Cited by 270 · see citing works
Lu, K., Walker, D. L., & Davis, M. E. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-16-j0005.2001 · Cited by 222 · see citing works
Conditioned Reflexes and Neuron Organization
(1949) · JAMA · doi:10.1001/jama.1949.02900320075040 · Cited by 198 · see citing works
Behavioural pharmacology and its contribution to the molecular basis of memory consolidation
Izquierdo, I., & McGaugh, J. L. (2000) · Behavioural Pharmacology · doi:10.1097/00008877-200011000-00001 · Cited by 190 · see citing works
Self-citationBernabeu, R. (1997) · Medical Entomology and Zoology · Cited by 188 · see citing works
Lattal, K. M., & Abel, T. G. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05773.2001 · Cited by 167 · see citing works
Barros, D. M., Izquierdo, L. A., Souza, T. M. E., Ardenghi, P. G., Pereira, P., Medina, J. H., & Izquierdo, I. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00226-6 · Cited by 132 · see citing works
Self-citationWalz, R., Roesler, R., Quevedo, J., Kauer‐Sant’Anna, M., Madruga, M., Rodrigues, C., Gottfried, C., Medina, J. H., & Izquierdo, I. (2000) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1999.3913 · Cited by 111 · see citing works
Self-citationIzquierdo, I., Schröder, N., Netto, C. A., & Medina, J. H. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00742.x · Cited by 94 · see citing works
Self-citationSzapiro, G., Izquierdo, L. A., Alonso, M., Barros, D. M., Paratcha, G., Ardenghi, P. G., Pereira, P., Medina, J. H., & Izquierdo, I. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00236-0 · Cited by 90 · see citing works
Self-citationQuartermain, D., & McEwen, B. S. (1970) · Nature · doi:10.1038/228677a0 · Cited by 83 · see citing works
The status of memory following experimentally induced amnesias: Gone, but not forgotten
Riccio, D. C., & Richardson, R. (1984) · Physiological Psychology · doi:10.3758/bf03332169 · Cited by 67 · see citing works
Picrotoxin enhances latent extinction of conditioned fear.
McGaugh, J. L., Castellano, C., & Brioni, J. D. (1990) · Behavioral Neuroscience · doi:10.1037//0735-7044.104.2.264 · Cited by 62 · see citing works
Self-citationPicrotoxin enhances latent extinction of conditioned fear.
McGaugh, J. L., Castellano, C., & Brioni, J. D. (1990) · Behavioral Neuroscience · doi:10.1037/0735-7044.104.2.264 · Cited by 52 · see citing works
Self-citation[Establishment of a trace reflex during natural sleep of cats].
Izquierdo, I., Wyrwicka, W., Sierra, G., & Segundo, J. P. (1965) · PubMed · Cited by 13 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
da Luz, A. C. D. D. S., Dias, G. P., Bevilaqua, M. C. D. N., Cocks, G. D., Gardino, P. F., Thuret, S., & Nardi, A. E. (2013) · Neuropsychobiology · doi:10.1159/000353269 · Cited by 4,012 · see citing works
Neural 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
Myers, K. M., & Davis, M. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001939 · Cited by 1,277 · see citing works
Pape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · 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
Heldt, S. A., Stanek, L., Chhatwal, J. P., & Ressler, K. J. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001957 · Cited by 684 · see citing works
Effects of D-Cycloserine on Extinction: Translation From Preclinical to Clinical Work
Davis, M., Ressler, K., Rothbaum, B. O., & Richardson, R. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.084 · Cited by 498 · see citing works
Neural and cellular mechanisms of fear and extinction memory formation
Orsini, C. A., & Maren, S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.12.014 · Cited by 429 · see citing works
Singewald, N., Schmuckermair, C., Whittle, N., Holmes, A., & Ressler, K. J. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.12.004 · Cited by 390 · see citing works
The role of serotonin 5-HT2A receptors in memory and cognition
Zhang, G., & Stackman, R. W. (2015) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00225 · Cited by 386 · see citing works
Different mechanisms of fear extinction dependent on length of time since fear acquisition
Myers, K. M., Ressler, K. J., & Davis, M. (2006) · Learning & Memory · doi:10.1101/lm.119806 · Cited by 334 · see citing works
Seeking a Spotless Mind: Extinction, Deconsolidation, and Erasure of Fear Memory
Maren, S. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.023 · Cited by 259 · see citing works
“A number of groups have shown that dis- rupting hippocampal function prior to extinction training impairs the acquisition of extinction (Corcoran et al., 2005; Fischer et al., 2004, 2007; Sananbenesi et al., 2007; Szapiro et al., 2003; Tronson et al., 2009; Vianna et al., 2001).”
BackgroundLin, C.-H., Yeh, S.-H., Lu, H.-Y., & Gean, P.-W. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08310.2003 · Cited by 251 · see citing works
Overexpression of type-1 adenylyl cyclase in mouse forebrain enhances recognition memory and LTP
Wang, H., Ferguson, G. D., Pineda, V. V., Cundiff, P. E., & Storm, D. R. (2004) · Nature Neuroscience · doi:10.1038/nn1248 · Cited by 244 · see citing works
Albert‐Gascó, H., Ros‐Bernal, F., Castillo-Gómez, E., & Olucha-Bordonau, F. E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124471 · Cited by 241 · see citing works
Systemic or intrahippocampal delivery of histone deacetylase inhibitors facilitates fear extinction.
Lattal, K. M., Barrett, R. M., & Wood, M. A. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.5.1125 · Cited by 236 · see citing works
Lattal, K. M., & Abel, T. G. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306546101 · Cited by 220 · see citing works
Yamamoto, S., Morinobu, S., Fuchikami, M., Kurata, A., Kozuru, T., & Yamawaki, S. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301605 · Cited by 224 · see citing works
Fischer, A., Sananbenesi, F., Schrick, C., Spiess, J., & Radulović, J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5112-03.2004 · Cited by 219 · see citing works
BERLAU, D., & MCGAUGH, J. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.12.008 · Cited by 220 · see citing works
Self-citationBehavioral assays with mouse models of Alzheimer's disease: Practical considerations and guidelines
Puzzo, D., Lee, L. S., Palmeri, A., Calabrese, G., & Arancio, O. (2014) · Biochemical Pharmacology · doi:10.1016/j.bcp.2014.01.011 · Cited by 214 · see citing works
PI3 kinase signaling is required for retrieval and extinction of contextual memory
Chen, X., Garelick, M. G., Wang, H., Li, V., Athos, J., & Storm, D. R. (2005) · Nature Neuroscience · doi:10.1038/nn1482 · Cited by 188 · see citing works
Pharmacological treatments that facilitate extinction of fear: Relevance to psychotherapy
Davis, M., Myers, K. M., Chhatwal, J., & Ressler, K. J. (2006) · NeuroRX · doi:10.1016/j.nurx.2005.12.008 · Cited by 174 · see citing works
Glutamate receptors in extinction and extinction-based therapies for psychiatric illness
Myers, K. M., Carlezon, W., & Davis, M. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.88 · Cited by 175 · see citing works
Zhang, G., Ásgeirsdóttir, H. N., Cohen, S. J., Munchow, A. H., Barrera, M. P., & Stackman, R. W. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.007 · Cited by 161 · see citing works
Callaerts‐Vegh, Z., Beckers, T., Ball, S. M., Baeyens, F., Callaerts, P., Cryan, J. F., Molnár, E., & D’Hooge, R. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1497-06.2006 · Cited by 154 · see citing works
Auber, A., Tedesco, V., Jones, C. E., Monfils, M., & Chiamulera, C. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3004-1 · Cited by 148 · see citing works
A hippocampal Cdk5 pathway regulates extinction of contextual fear
Sananbenesi, F., Fischer, A., Wang, X., Schrick, C., Neve, R. L., Radulović, J., & Tsai, L. (2007) · Nature Neuroscience · doi:10.1038/nn1943 · Cited by 141 · see citing works
Tronson, N. C., Schrick, C., Guzman, Y. F., Huh, K. H., Srivastava, D. P., Penzes, P., Guedea, A. L., Gao, C., & Radulovic, J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5619-08.2009 · Cited by 136 · see citing works
Modulation of the extinction of two different fear-motivated tasks in three distinct brain areas
Fiorenza, N. G., Rosa, J., Izquierdo, I., & Myskiw, J. D. C. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.015 · Cited by 129 · see citing works
Self-citationAnimal model for PTSD: From clinical concept to translational research
Cohen, H., Kozlovsky, N., Alona, C., Matar, M. A., & Zohar, J. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.023 · Cited by 128 · see citing works
Heldt, S. A., & Ressler, K. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05970.x · Cited by 125 · see citing works
The learning of fear extinction
Furini, C., Myskiw, J., & Izquierdo, I. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.016 · Cited by 124 · see citing works
Self-citationGass, J. T., & Chandler, L. J. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00046 · Cited by 118 · see citing works
NMDA receptors and fear extinction: implications for cognitive behavioral therapy
Davis, M. (2011) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2011.13.4/mdavis · Cited by 118 · see citing works
Brain sites involved in fear memory reconsolidation and extinction of rodents
Baldi, E., & Bucherelli, C. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.003 · Cited by 116 · see citing works
Proteolysis of proBDNF Is a Key Regulator in the Formation of Memory
Barnes, P., & Thomas, K. L. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003248 · Cited by 117 · see citing works
Azriel-Tamir, H., Sharir, H., Schwartz, B., & Hershfinkel, M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406581200 · Cited by 111 · see citing works
The use of cognitive enhancers in animal models of fear extinction.
Kaplan, G. B., & Moore, K. (2011) · Pharmacology, Biochemistry and Behavior · doi:10.1016/j.pbb.2011.01.009 · Cited by 104 · see citing works
Hippocampal Mek/Erk signaling mediates extinction of contextual freezing behavior
Fischer, A., Radulović, M., Schrick, C., Sananbenesi, F., Godovac‐Zimmermann, J., & Radulović, J. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.08.003 · Cited by 107 · see citing works
Relative Amnesic Potency of Five Inhalational Anesthetics Follows the Meyer-Overton Rule
Alkire, M. T., & Gorski, L. A. (2004) · Anesthesiology · doi:10.1097/00000542-200408000-00023 · Cited by 99 · see citing works
Ori, R., Amos, T., Bergman, H., Soares‐Weiser, K., Ipser, J., & Stein, D. J. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd007803.pub2 · Cited by 93 · see citing works
Genetic inactivation of D-amino acid oxidase enhances extinction and reversal learning in micePreprint
Labrie, V., Duffy, S. N., Wang, W., Barger, S. W., Baker, G. B., & Roder, J. (2008) · Learning & Memory · doi:10.1101/lm.1112209 · Cited by 89 · see citing works
Molecular Specificity of Multiple Hippocampal Processes Governing Fear Extinction
Radulović, J., & Tronson, N. C. (2010) · Reviews in the Neurosciences · doi:10.1515/revneuro.2010.21.1.1 · Cited by 82 · see citing works
Harvey, B. H., & Shahid, M. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.06.014 · Cited by 88 · see citing works
Cammarota, M., Bevilaqua, L., Kerr, D., Medina, J., & Izquierdo, I. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-03-00737.2003 · Cited by 85 · see citing works
Self-citationMemory extinction requires gene expression in rat hippocampus.
Vianna, M., Igaz, L., Coitinho, A., Medina, J., & Izquierdo, I. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(03)00003-0 · Cited by 89 · see citing works
Self-citationRegulatory Mechanisms of Fear Extinction and Depression-Like Behavior
Tronson, N. C., Schrick, C., Fischer, A., Sananbenesi, F., Pagès, G., Pouysségur, J., & Radulović, J. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301550 · Cited by 83 · see citing works
Angiotensin II disrupts inhibitory avoidance memory retrieval
Bonini, J. S., Bevilaqua, L. R., Zinn, C. G., Kerr, D. S., Medina, J. H., Izquierdo, I., & Cammarota, M. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.03.016 · Cited by 83 · see citing works
Self-citationFarinelli, M., Deschaux, O., Hugues, S., Thévenet, A., & Garcia, R. (2006) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.204806 · Cited by 84 · see citing works
Activity-Dependent p25 Generation Regulates Synaptic Plasticity and Aβ-Induced Cognitive Impairment
Seo, J., Giusti‐Rodríguez, P., Zhou, Y., Rudenko, A., Cho, S., Ota, K. T., Park, C. S., Patzke, H., Madabhushi, R., Pan, L., et al. (2014) · Cell · doi:10.1016/j.cell.2014.01.065 · Cited by 80 · see citing works
Lymnaea stagnalis as model for translational neuroscience research: From pond to bench
Rivi, V., Benatti, C., Colliva, C., Radighieri, G., Brunello, N., Tascedda, F., & Blom, J. M. C. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.11.020 · Cited by 77 · see citing works
Lattal, K. M., Radulović, J., & Lukowiak, K. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.05.038 · Cited by 74 · see citing works
Transgenic Inhibition of Neuronal Protein Kinase A Activity Facilitates Fear Extinction
Isiegas, C., Park, A., Kandel, E. R., Abel, T. G., & Lattal, K. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2743-06.2006 · Cited by 73 · see citing works
Reconsolidation after remembering an odor-reward association requires NMDA receptorsPreprint
Torras-García, M., Lelong, J., Tronel, S., & Sara, S. J. (2005) · Learning & Memory · doi:10.1101/lm.80905 · Cited by 73 · see citing works
Medina, J. H., & Viola, H. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00361 · Cited by 72 · see citing works
Self-citationMolecular Mechanisms of Memory Retrieval
Szapiro, G., Galante, J., Barros, D., de Stein, M. L., Vianna, M., Izquierdo, L. A., Izquierdo, I., & Medina, J. (2002) · Neurochemical Research · doi:10.1023/a:1021648405461 · Cited by 75 · see citing works
Self-citationWoods, A. M., & Bouton, M. E. (2008) · Learning & Memory · doi:10.1101/lm.1078508 · Cited by 70 · see citing works
Ghrelin and memory: Differential effects on acquisition and retrieval
Carlini, V. P., Ghersi, M., Schiöth, H. B., & de Barioglio, S. R. (2010) · Peptides · doi:10.1016/j.peptides.2010.02.021 · Cited by 72 · see citing works
Mechanisms of Musculoskeletal Physiotherapy
Zusman, M. (2004) · Physical Therapy Reviews · doi:10.1179/108331904225003973 · Cited by 71 · see citing works
Michalon, A., Bruns, A., Risterucci, C., Honer, M., Ballard, T. M., Ozmen, L., Jaeschke, G., Wettstein, J. G., von Kienlin, M., Künnecke, B., et al. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.05.038 · Cited by 67 · see citing works
Matsumoto, Y., Morinobu, S., Yamamoto, S., Matsumoto, T., Takei, S., Fujita, Y., & Yamawaki, S. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3078-9 · Cited by 66 · see citing works
Augmentation of Cognitive Behavioral Therapy with Pharmacotherapy
Ganasen, K. A., Ipser, J., & Stein, D. J. (2010) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2010.04.008 · Cited by 66 · see citing works
Deficits in acquisition and extinction of conditioned responses in mGluR7 knockout mice
Goddyn, H., Callaerts‐Vegh, Z., Stroobants, S., Dirikx, T., Vansteenwegen, D., Hermans, D., van der Putten, H., & D’Hooge, R. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.01.001 · Cited by 66 · see citing works
Kishimoto, Y., Nakazawa, K., Tonegawa, S., Kirino, Y., & Kano, M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4142-05.2006 · Cited by 63 · see citing works
The MAP(K) of fear: From memory consolidation to memory extinction
Cestari, V., Rossi‐Arnaud, C., Saraulli, D., & Costanzi, M. (2013) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2013.09.007 · Cited by 61 · see citing works
Zhang, M., Storm, D. R., & Wang, H. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0009-11.2011 · Cited by 61 · see citing works
Retrieval and the Extinction of Memory
Cammarota, M., Bevilaqua, L., Barros, D., Vianna, M., Izquierdo, L. A., Medina, J., & Izquierdo, I. (2005) · Cellular and molecular neurobiology · doi:10.1007/s10571-005-4009-z · Cited by 61 · see citing works
Self-citationSchmidt, S. D., Myskiw, J. D. C., Furini, C. R. G., Schmidt, B. E., Cavalcante, L. E. S., & Izquierdo, I. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.11.014 · Cited by 59 · see citing works
Self-citationA sphingolipid mechanism for behavioral extinction
Huston, J. P., Kornhuber, J., Mühle, C., Japtok, L., Komorowski, M., Mattern, C., Reichel, M., Gulbins, E., Kleuser, B., Topic, B., et al. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13537 · Cited by 59 · see citing works
Removing Pathogenic Memories: A Neurobiology of Psychotherapy
Centonze, D., Siracusano, A., Calabresi, P., & Bernardi, G. (2005) · Molecular Neurobiology · doi:10.1385/mn:32:2:123 · Cited by 58 · see citing works
Role of the Hippocampus and Amygdala in the Extinction of Fear- Motivated Learning
Vianna, M. R. M. R., Coitinho, A. S., & Izquierdo, I. (2004) · Current Neurovascular Research · doi:10.2174/1567202043480170 · Cited by 54 · see citing works
Self-citationA role for ERK2 in reconsolidation of fear memories in mice
Cestari, V., Costanzi, M., Castellano, C., & Rossi‐Arnaud, C. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.01.003 · Cited by 52 · see citing works
Judo, C., Matsumoto, M., Yamazaki, D., Hiraide, S., Yanagawa, Y., Kimura, S., Shimamura, K., & Togashi, H. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.06.035 · Cited by 52 · see citing works
Relationship between short- and long-term memory and short- and long-term extinction
Cammarota, M., Bevilaqua, L. R., Rossato, J. I., Ramirez, M. R., Medina, J. H., & Izquierdo, I. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.03.002 · Cited by 50 · see citing works
Self-citationMcNally, G. P., Lee, B.-W., Chiem, J. Y., & Choi, E. A. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.4.1023 · Cited by 50 · see citing works
The entorhinal cortex plays a role in extinction.
Bevilaqua, L., Bonini, J., Rossato, J., Izquierdo, L. A., Cammarota, M., & Izquierdo, I. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.10.001 · Cited by 48 · see citing works
Self-citationAmaral, O. B., Osan, R. M., Roesler, R., & Tort, A. B. L. (2008) · Hippocampus · doi:10.1002/hipo.20420 · Cited by 47 · see citing works
Functional interaction of mGlu5 and NMDA receptors in aversive learning in rats
Fowler, S., Ramsey, A. K., Walker, J. M., Serfözö, P. D., Olive, M. F., Schachtman, T. R., & Simonyi, Á. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.11.009 · Cited by 48 · see citing works
Understanding the dynamic and destiny of memories
Alvares, L. D. O., & Monte, F. H. D. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.009 · Cited by 47 · see citing works
Kimura, R., Silva, A. J., & Ohno, M. (2008) · Learning & Memory · doi:10.1101/lm.1049608 · Cited by 44 · see citing works
On the transition from reconsolidation to extinction of contextual fear memories
Cassini, L. F., Flavell, C. R., Amaral, O. B., & Lee, J. L. C. (2017) · Learning & Memory · doi:10.1101/lm.045724.117 · Cited by 47 · see citing works
Ren, J., Li, X., Zhang, X., Li, M., Wang, Y., & Ma, Y. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.02.017 · Cited by 44 · see citing works
Pharmacological Findings on the Biochemical Bases of Memory Processes: A General View
Izquierdo, I., Cammarota, M., Medina, J., & Bevilaqua, L. (2004) · Journal of Neural Transplantation and Plasticity · doi:10.1155/np.2004.159 · Cited by 41 · see citing works
Self-citationZeitlin, R., Patel, S., Solomon, R., Tran, J., Weeber, E. J., & Echeverrı́a, V. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.11.023 · Cited by 45 · see citing works
Modulation of the extinction of fear learning
Myskiw, J. D. C., Izquierdo, I., & Furini, C. R. G. (2014) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2014.04.006 · Cited by 43 · see citing works
Self-citationExposure to extreme stress impairs contextual odour discrimination in an animal model of PTSD
Cohen, H., Liberzon, I., & Richter‐Levin, G. (2008) · The International Journal of Neuropsychopharmacology · doi:10.1017/s146114570800919x · Cited by 44 · see citing works
Chai, N., Liu, J., Xue, Y.-X., Yang, C., Yan, W., Wang, H.-M., Luo, Y., Shi, H., Wang, J.-S., Bao, Y., et al. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.42 · Cited by 41 · see citing works
Rolipram Attenuates MK-801-Induced Deficits in Latent Inhibition.
Davis, J. A., & Gould, T. J. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.2.595 · Cited by 42 · see citing works
Akirav, I. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301050 · Cited by 42 · see citing works
Rossato, J. I., Bevilaqua, L. R., Lima, R. H., Medina, J. H., Izquierdo, I., & Cammarota, M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.07.025 · Cited by 41 · see citing works
Self-citationERK1/2 and CaMKII-mediated events in memory formation: Is 5HT regulation involved?
Cammarota, M., Bevilaqua, L. R., Medina, J. H., & Izquierdo, I. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.11.029 · Cited by 40 · see citing works
Self-citationThe extinction of conditioned fear: structural and molecular basis and therapeutic use
Cammarota, M., Bevilaqua, L. R., Vianna, M. R. M. R., Medina, J. H., & Izquierdo, I. (2006) · Brazilian Journal of Psychiatry · doi:10.1590/s1516-44462006005000022 · Cited by 40 · see citing works
Self-citationPolyaminergic agents modulate contextual fear extinction in rats.
Gomes, G. M., Mello, C. F., da Rosa, M. M., Bochi, G., Ferreira, J., Barron, S., & Rubin, M. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.02.007 · Cited by 40 · see citing works
JIP1-Mediated JNK Activation Negatively Regulates Synaptic Plasticity and Spatial Memory
Morel, C., Sherrin, T., Kennedy, N. J., Forest, K. H., Barutcu, S., Robles, M. J., Carpenter‐Hyland, E. P., Alfulaij, N., Standen, C. L., Nichols, R. A., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1913-17.2018 · Cited by 38 · see citing works
Billa, S. K., Sinha, N., Rudrabhatla, S. R., & Morón, J. A. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06560.x · Cited by 38 · see citing works
Memory labilization in reconsolidation and extinction – Evidence for a common plasticity system?
Almeida-Corrêa, S., & Amaral, O. B. (2014) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2014.08.006 · Cited by 36 · see citing works
Burgdorf, C. E., Schierberl, K. C., Lee, A. S., Fischer, D. K., Kempen, T. A. V., Mudragel, V., Huganir, R. L., Milner, T. A., Glass, M. J., & Rajadhyaksha, A. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2397-17.2017 · Cited by 36 · see citing works
Cohen, H., Matar, M., & Zohar, J. (2014) · ILAR Journal · doi:10.1093/ilar/ilu006 · Cited by 37 · see citing works
The inhibition of acquired fear
Izquierdo, I., Cammarota, M., Vianna, M. R. M. R., & Bevilaqua, L. R. (2004) · Neurotoxicity Research · doi:10.1007/bf03033220 · Cited by 37 · see citing works
Self-citation
- Authors
- Szapiro, G., Vianna, M. R. M., McGaugh, J. L., Medina, J. H., & Izquierdo, I.
- Affiliations
- University of California, Irvine (US)
- Universidad de Buenos Aires (AR)
- ORCID
- Medina, Jorge H.
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2002-10-28
- Volume
- 13
- Issue
- 1
- Pages
- 53-58
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W2046861885
- Cited by
- 221
- References
- 29
- Citations by year
- 2025: 3 · 2024: 2 · 2023: 3 · 2022: 4 · 2021: 5 · 2020: 5 · 2019: 7 · 2018: 6 · 2017: 7 · 2016: 5 · 2015: 15 · 2014: 14 · 2013: 13 · 2012: 10
- FWCI
- 5.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- fear extinction, contextual fear conditioning, NMDA receptor, protein kinase A, mitogen-activated protein kinase, calcium/calmodulin-dependent protein kinase II, memory retrieval, memory consolidation, classical conditioning, glutamate signaling
- MeSH terms
- Animals, Conditioning, Psychological, Enzyme Inhibitors, Extinction, Psychological, Fear, Hippocampus, Learning, Male, Memory, Synaptic Transmission, Synapses, Receptors, N-Methyl-D-Aspartate, Rats, Wistar, Cyclic AMP-Dependent Protein Kinases, Calcium-Calmodulin-Dependent Protein Kinases, Excitatory Amino Acid Antagonists, MAP Kinase Signaling System, Rats, Calcium-Calmodulin-Dependent Protein Kinase Type 2
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
