Different mechanisms of fear extinction dependent on length of time since fear acquisition
Open accessAbstract
Fear extinction is defined as a decline in conditioned fear responses (CRs) following nonreinforced exposure to a feared conditioned stimulus (CS). Behavioral evidence indicates that extinction is a form of inhibitory learning: Extinguished fear responses reappear with the passage of time (spontaneous recovery), a shift of context (renewal), and unsignaled presentations of the unconditioned stimulus (reinstatement). However, there also is evidence to suggest that extinction is an "unlearning" process corresponding to depotentiation of potentiated synapses within the amygdala. Because depotentiation is induced more readily at short intervals following LTP induction and is not inducible at all at a sufficient delay, it may be that extinction initiated shortly following fear acquisition preferentially engages depotentiation/"unlearning," whereas extinction initiated at longer delays recruits a different mechanism. We investigated this possibility through a series of behavioral experiments examining the recoverability of conditioned fear following extinction. Consistent with an inhibitory learning mechanism of extinction, rats extinguished 24-72 h following acquisition exhibited moderate to strong reinstatement, renewal, and spontaneous recovery. In contrast, and consistent with an erasure mechanism, rats extinguished 10 min to 1 h after acquisition exhibited little or no reinstatement, renewal, or spontaneous recovery. These data support a model in which different neural mechanisms are recruited depending on the temporal delay of fear extinction.
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Extinction training initiated immediately after (10 min) fear acquisition prevented the return of learned fear via reinstatement, renewal, or spontaneous recovery.
“Myers et al. (32) showed that extinction training initiated immediately after (10 min) fear acquisition prevented the return of learned fear via reinstatement, renewal, or spontaneous recovery.”
From Conditioned fear associated phenotypes as robust, translational indices of trauma-, stressor-, and anxiety-related behaviors (2014) · cites this paper as [32]
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AMPA Receptor Trafficking and Synaptic Plasticity
Malinow, R., & Malenka, R. C. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142758 · Cited by 2,588 · see citing works
Context, time, and memory retrieval in the interference paradigms of Pavlovian learning
Bouton, M. E. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.114.1.80 · Cited by 1,896 · see citing works
Neurons in medial prefrontal cortex signal memory for fear extinction
Milad, M. R., & Quirk, G. J. (2002) · Nature · doi:10.1038/nature01138 · Cited by 1,836 · see citing works
Are theories of learning necessary?
Skinner, B. F. (1950) · Psychological Review · doi:10.1037/h0054367 · Cited by 1,808 · see citing works
Effects of an expanding-spaced vs massed exposure schedule on fear reduction and return of fear
Rowe, M. K., & Craske, M. G. (1998) · Behaviour Research and Therapy · doi:10.1016/s0005-7967(97)10016-x · Cited by 1,778 · see citing works
Ressler, K. J., Rothbaum, B. O., Tannenbaum, L., Anderson, P., Graap, K., Zimand, E., Hodges, L., & Davis, M. (2004) · Archives of General Psychiatry · doi:10.1001/archpsyc.61.11.1136 · Cited by 1,063 · see citing works
Self-citationThe Amygdala: a functional analysis
Aggleton, J. P. (2000) · Cited by 964 · see citing works
The role of ventromedial prefrontal cortex in the recovery of extinguished fear
Quirk, G. J., Russo, G. K., Barron, J. L., & Lebron, K. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06225.2000 · Cited by 957 · see citing works
Quirk, G. J., Likhtik, E., Pelletier, J. G., & Paré, D. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-25-08800.2003 · Cited by 927 · 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
Walker, D. L., Ressler, K. J., Lu, K.-T., & Davis, M. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-06-02343.2002 · Cited by 815 · see citing works
Contextual control of the extinction of conditioned fear
Bouton, M. E., & Bolles, R. C. (1979) · Learning and Motivation · doi:10.1016/0023-9690(79)90057-2 · Cited by 796 · see citing works
Bouton, M. E., & King, D. A. (1983) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.9.3.248 · Cited by 771 · see citing works
Reinstatement of fear to an extinguished conditioned stimulus.
Rescorla, R. A., & Heth, C. D. (1975) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.1.1.88 · Cited by 768 · see citing works
"Attention-like" processes in classical conditioning
Kamin, L. J. (1967) · NASA Technical Reports Server (NASA) · Cited by 716 · 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
Molecular mechanisms underlying emotional learning and memory in the lateral amygdala
Rodrigues, S. M., Schafe, G. E., & LeDoux, J. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.014 · Cited by 491 · see citing works
Role of conditioned contextual stimuli in reinstatement of extinguished fear.
Bouton, M. E., & Bolles, R. C. (1979) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.5.4.368 · Cited by 481 · see citing works
Consolidation of Fear Extinction Requires Protein Synthesis in the Medial Prefrontal Cortex
Santini, E., Ge, H., Ren, K., de Ortiz, S. P., & Quirk, G. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0786-04.2004 · Cited by 479 · see citing works
Two different lateral amygdala cell populations contribute to the initiation and storage of memory
Repa, J. C., Muller, J., Apergis, J., Desrochers, T. M., Zhou, Y., & LeDoux, J. E. (2001) · Nature Neuroscience · doi:10.1038/89512 · Cited by 440 · see citing works
Role of the Basolateral Amygdala in the Storage of Fear Memories across the Adult Lifetime of Rats
Gale, G. D., Anagnostaras, S., Godsil, B. P., Mitchell, S., Nozawa, T., Sage, J. R., Wiltgen, B. J., & Fanselow, M. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4100-03.2004 · Cited by 427 · see citing works
The role of the amygdala in conditioned and unconditioned fear and anxiety
Davis, M. (2000) · The Amygdala · doi:10.1093/oso/9780198505013.003.0006 · Cited by 384 · see citing works
Role of conditioned contextual stimuli in reinstatement of extinguished fear.
Bouton, M. E., & Bolles, R. C. (1979) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.5.4.368 · Cited by 376 · see citing works
Fujii, S., Saito, K., Miyakawa, H., Ito, K., & Kato, H. (1991) · Brain Research · doi:10.1016/0006-8993(91)90867-u · Cited by 375 · see citing works
Quirk, G. J. (2002) · Learning & Memory · doi:10.1101/lm.49602 · Cited by 360 · cited 1× · see citing works
“The recovery in the 1-h group came as a surprise in light of the lack of significant recovery in this group in previous experiments, although interestingly it is consistent with a report by Quirk (2002) of reliable spontaneous recovery of freezing over time following extinction conducted 1 h after acquisition.”
ResultRosenkranz, J. A., Moore, H., & Grace, A. A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-35-11054.2003 · Cited by 344 · see citing works
Bouton, M. E., & Swartzentruber, D. (1986) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.12.4.333 · Cited by 335 · see citing works
Inhibition of the Amygdala: Key to Pathological States?
Quirk, G. J., & Gehlert, D. R. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07087.x · Cited by 308 · 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
Signaling from cAMP/PKA to MAPK and Synaptic Plasticity
Waltereit, R., & Weller, M. (2003) · Molecular Neurobiology · doi:10.1385/mn:27:1:99 · Cited by 300 · see citing works
Lin, 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
Experimental extinction in Pavlovian conditioning: Behavioural and neuroscience perspectives
Delamater, A. R. (2004) · The Quarterly Journal of Experimental Psychology Section B · doi:10.1080/02724990344000097 · Cited by 247 · see citing works
Ledgerwood, L., Richardson, R., & Cranney, J. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.01.023 · Cited by 243 · see citing works
Mechanisms underlying spontaneous recovery in autoshaping.
Robbins, S. J. (1990) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.16.3.235 · Cited by 234 · see citing works
Infralimbic cortex activation increases c-fos expression in intercalated neurons of the amygdala
Berretta, S., Pantazopoulos, H., Caldera, M., Pantazopoulos, P., & Paré, D. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.01.020 · Cited by 223 · 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
Szapiro, G., Vianna, M. R. M., McGaugh, J. L., Medina, J. H., & Izquierdo, I. (2003) · Hippocampus · doi:10.1002/hipo.10043 · Cited by 221 · 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
Chhatwal, J. P., Myers, K. M., Ressler, K. J., & Davis, M. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3301-04.2005 · Cited by 214 · see citing works
Contextual control over conditioned responding in an extinction paradigm.
Harris, J. A., Jones, M. L., Bailey, G. K., & Westbrook, R. F. (2000) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.26.2.174 · Cited by 210 · see citing works
Davis, M., & Myers, K. M. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01507-x · Cited by 200 · see citing works
Ledgerwood, L., Richardson, R., & Cranney, J. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.3.505 · Cited by 190 · 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
Hobin, J. A., Goosens, K. A., & Maren, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08410.2003 · Cited by 187 · see citing works
Identification of Calcineurin as a Key Signal in the Extinction of Fear Memory
Lin, C.-H., Yeh, S.-H., Leu, T.-H., Chang, W.-C., Wang, S.-S., & Gean, P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-05-01574.2003 · Cited by 174 · see citing works
Factors regulating the reversibility of long-term potentiation
Staubli, U., & Chun, D. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-02-00853.1996 · Cited by 169 · 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
Evidence that GABA transmission mediates context-specific extinction of learned fear
Harris, J. A., & Westbrook, R. F. (1998) · Psychopharmacology · doi:10.1007/s002130050745 · Cited by 164 · see citing works
Modulatory mechanisms in Pavlovian conditioning
Swartzentruber, D. (1995) · Animal Learning & Behavior · doi:10.3758/bf03199928 · Cited by 163 · see citing works
Involvement of a Calcineurin Cascade in Amygdala Depotentiation and Quenching of Fear Memory
Lin, C.-H., Lee, C.-C., & Gean, P. (2003) · Molecular Pharmacology · doi:10.1124/mol.63.1.44 · Cited by 158 · see citing works
Huang, C., Liang, Y., & Hsu, K. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m106388200 · Cited by 152 · see citing works
The design and calibration of a startle measurement system
Cassella, J. V., & Davis, M. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90032-6 · Cited by 140 · see citing works
Cain, C. K., Blouin, A. M., & Barad, M. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-20-09113.2002 · Cited by 130 · see citing works
Cannich, A., Wotjak, C. T., Kamprath, K., Hermann, H., Lutz, B., & Marsicano, G. (2004) · Learning & Memory · doi:10.1101/lm.77904 · Cited by 130 · see citing works
Contextual control over conditioned responding in an extinction paradigm.
Harris, J. A., Jones, M. L., Bailey, G. K., et al. (2000) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.26.2.174 · Cited by 129 · see citing works
Reinstatement of fear to an extinguished conditioned stimulus: Two roles for context.
Westbrook, R. F., Iordanova, M. D., McNally, G. P., Richardson, R., & Harris, J. A. (2002) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.28.1.97 · Cited by 128 · see citing works
Stimulus Selection and A “Modified Continuity Theoryrdquo;
Wagner, A. R. (1970) · The Psychology of learning and motivation/The psychology of learning and motivation · doi:10.1016/s0079-7421(08)60396-5 · Cited by 120 · see citing works
Reversal and consolidation of activity-induced synaptic modifications
Zhou, Q., & Poo, M. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.05.006 · Cited by 110 · see citing works
Rauhut, A. S., Thomas, B. L., & Ayres, J. J. B. (2001) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.27.2.99 · Cited by 109 · see citing works
Occasional reinforced trials during extinction can slow the rate of rapid reacquisition
Bouton, M. E., Woods, A. M., & Pineño, O. (2004) · Learning and Motivation · doi:10.1016/j.lmot.2004.05.001 · Cited by 109 · see citing works
Reberg, D. (1972) · Learning and Motivation · doi:10.1016/0023-9690(72)90021-5 · Cited by 108 · see citing works
Yang, Y.-L., & Lu, K. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.04.003 · Cited by 93 · see citing works
Woods, A. M., & Bouton, M. E. (2006) · Learning and Motivation · doi:10.1016/j.lmot.2006.07.003 · Cited by 81 · see citing works
Spontaneous recovery varies inversely with the training-extinction interval
Rescorla, R. A. (2004) · Learning & Behavior · doi:10.3758/bf03196037 · Cited by 81 · see citing works
Cain, C. K., Godsil, B., Jami, S. A., & Barad, M. (2005) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.88805 · Cited by 73 · see citing works
Spontaneous recovery without interference: Why remembering is adaptive
Devenport, L. D. (1998) · Animal Learning & Behavior · doi:10.3758/bf03199210 · Cited by 72 · see citing works
Summation of undetected excitation following extinction of the CER
Hendry, J. S. (1982) · Animal Learning & Behavior · doi:10.3758/bf03212287 · Cited by 58 · see citing works
Lin, C.-H., Lee, C.-C., Huang, Y.-C., Wang, S., & Gean, P. (2005) · Learning & Memory · doi:10.1101/lm.85304 · Cited by 45 · see citing works
Input-specific LTP and depotentiation in the basolateral amygdala
Aroniadou‐Anderjaska, V., Post, R. M., Rogawski, M. A., & Li, H. (2001) · Neuroreport · doi:10.1097/00001756-200103050-00041 · Cited by 34 · see citing works
If phosphatases go up, memory goes down
Riedel, G. (1999) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050313 · Cited by 33 · see citing works
Lattal, K. M., Honarvar, S., & Abel, T. G. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.12.009 · Cited by 32 · see citing works
AN ASSESSMENT OF THE ROLE OF HANDLING CUES IN “SPONTANEOUS RECOVERY” AFTER EXTINCTION
Thomas, D. R., & Sherman, L. (1986) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1986.46-305 · Cited by 20 · see citing works
Flagged first, then by citations
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- Pavlov, I.P. 1927. Conditioned reflexes. Oxford University Press, London.
Cited by
Sorted by citations
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
Optimizing inhibitory learning during exposure therapy
Craske, M. G., Kircanski, K., Zelikowsky, M., Mystkowski, J., Chowdhury, N., & Baker, A. (2008) · Behaviour Research and Therapy · doi:10.1016/j.brat.2007.10.003 · Cited by 1,607 · see citing works
Preventing the return of fear in humans using reconsolidation update mechanisms
Schiller, D., Monfils, M.-H., Raio, C. M., Johnson, D. C., LeDoux, J. E., & Phelps, E. A. (2010) · Nature · doi:10.1038/nature08637 · Cited by 1,248 · 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
Synaptic AMPA receptor plasticity and behavior
Kessels, H. W., & Malinow, R. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.015 · Cited by 993 · 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
Lonsdorf, T. B., Menz, M. M., Andreatta, M., Fullana, M. A., Golkar, A., Haaker, J., Heitland, I., Hermann, A., Kuhn, M., Kruse, O., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.026 · Cited by 837 · see citing works
Fear Extinction and Relapse: State of the Art
Vervliet, B., Craske, M. G., & Hermans, D. (2013) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050212-185542 · Cited by 671 · see citing works
Silenced by fear:The nature, sources, and consequences of fear at work
Kish-Gephart, J. J., Detert, J. R., Treviño, L. K., & Edmondson, A. C. (2009) · Research in Organizational Behavior · doi:10.1016/j.riob.2009.07.002 · Cited by 596 · see citing works
The Role of the Medial Prefrontal Cortex in the Conditioning and Extinction of Fear
Giustino, T. F., & Maren, S. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00298 · Cited by 519 · see citing works
Impaired safety signal learning may be a biomarker of PTSD
Jovanovic, T., Kazama, A., Bachevalier, J., & Davis, M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.02.023 · Cited by 473 · 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
Implications of memory modulation for post-traumatic stress and fear disorders
Parsons, R. G., & Ressler, K. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3296 · Cited by 476 · see citing works
Distributed synergistic plasticity and cerebellar learning
Gao, Z., van Beugen, B. J., & De Zeeuw, C. I. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3312 · Cited by 479 · see citing works
How the Neurocircuitry and Genetics of Fear Inhibition May Inform Our Understanding of PTSD
Jovanović, T., & Ressler, K. J. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.09071074 · Cited by 441 · see citing works
Sotres-Bayon, F., Cain, C. K., & LeDoux, J. E. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.012 · Cited by 433 · 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
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
Dunsmoor, J. E., Niv, Y., Daw, N., & Phelps, E. A. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.028 · Cited by 329 · see citing works
Immediate Early Genes, Memory and Psychiatric Disorders: Focus on c-Fos, Egr1 and Arc
Gallo, F. T., Katche, C., Morici, J. F., Medina, J. H., & Weisstaub, N. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00079 · Cited by 339 · see citing works
The Science of Cognitive Therapy
Hofmann, S. G., Asmundson, G. J. G., & Beck, A. T. (2013) · Behavior Therapy · doi:10.1016/j.beth.2009.01.007 · Cited by 336 · see citing works
Haglund, M., Nestadt, P. S., Cooper, N. S., Southwick, S. M., & Charney, D. S. (2007) · Development and Psychopathology · doi:10.1017/s0954579407000430 · Cited by 315 · see citing works
EARLY INTERVENTIONS FOR PTSD: A REVIEW: Review: Early Intervention
Kearns, M. C., Ressler, K. J., Zatzick, D., & Rothbaum, B. O. (2012) · Depression and Anxiety · doi:10.1002/da.21997 · Cited by 310 · see citing works
Fear extinction in the human brain: A meta-analysis of fMRI studies in healthy participants
Fullana, M. A., Albajes-Eizagirre, A., Soriano-Mas, C., Vervliet, B., Cardoner, N., Benet, O., Radua, J., & Harrison, B. J. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.03.002 · Cited by 308 · see citing works
Rothbaum, B. O., Kearns, M. C., Price, M., Malcoun, E., Davis, M., Ressler, K. J., Lang, D., & Houry, D. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.06.002 · Cited by 305 · see citing works
Jüngling, K., Seidenbecher, T., Sosulina, L., Lesting, J., Sangha, S., Clark, S. D., Okamura, N., Duangdao, D. M., Xu, Y.-L., Reinscheid, R. K., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.002 · Cited by 299 · see citing works
Admon, R., Milad, M. R., & Hendler, T. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.05.005 · Cited by 269 · see citing works
Knapska, E., & Maren, S. (2009) · Learning & Memory · doi:10.1101/lm.1463909 · Cited by 264 · 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
“extinction training (Myers et al., 2006).”
BackgroundAmygdala depotentiation and fear extinction
Kim, J., Lee, S., Park, K., Hong, I., Song, B., Son, G. H., Park, H., Kim, W. R., Park, E. J., Choe, H. K., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710548105 · Cited by 252 · see citing works
Genetic Gating of Human Fear Learning and Extinction
Lonsdorf, T. B., Weike, A. I., Nikamo, P., Schalling, M., Hamm, A. O., & Öhman, A. (2009) · Psychological Science · doi:10.1111/j.1467-9280.2009.02280.x · Cited by 242 · see citing works
Makkar, S., Zhang, S., & Cranney, J. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.53 · Cited by 232 · see citing works
mGluR5 Has a Critical Role in Inhibitory Learning
Xu, J., Zhu, Y., Contractor, A., & Heinemann, S. F. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5716-08.2009 · Cited by 221 · see citing works
Erasing Fear Memories with Extinction Training: Figure 1.
Quirk, G. J., Paré, D., Richardson, R., Herry, C., Monfils, M., Schiller, D., & Vicentic, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4268-10.2010 · Cited by 220 · see citing works
Integration of Parallel Opposing Memories Underlies Memory Extinction
Felsenberg, J., Jacob, P. F., Walker, T. M., Barnstedt, O., Edmondson-Stait, A. J., Pleijzier, M. W., Otto, N., Schlegel, P., Sharifi, N., Perisse, E., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.021 · Cited by 217 · see citing works
Fear Conditioning in Adolescents With Anxiety Disorders: Results From a Novel Experimental Paradigm
Lau, J. Y. F., Lissek, S. M., Nelson, E. E., Lee, Y. M., Roberson‐Nay, R., Poeth, K., Jenness, J. L., Monique Ernst, D., Grillon, C., & Pine, D. S. (2008) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b01e31815a5f01 · Cited by 215 · see citing works
Fear conditioning and extinction: Influence of sex and menstrual cycle in healthy humans.
Milad, M. R., Goldstein, J. M., Orr, S. P., Wedig, M. M., Klibanski, A., Pitman, R. K., & Rauch, S. L. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.5.1196 · Cited by 212 · see citing works
Prevention of Post-Traumatic Stress Disorder After Trauma: Current Evidence and Future Directions
Qi, W., Gevonden, M. J., & Shalev, A. Y. (2016) · Current Psychiatry Reports · doi:10.1007/s11920-015-0655-0 · Cited by 209 · see citing works
A review on human reinstatement studies: an overview and methodological challengesPreprint
Haaker, J., Golkar, A., Hermans, D., & Lonsdorf, T. B. (2014) · Learning & Memory · doi:10.1101/lm.036053.114 · Cited by 186 · see citing works
Recent fear is resistant to extinction
Maren, S., & Chang, C.-H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608398103 · Cited by 184 · 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
Conditioned fear extinction and reinstatement in a human fear-potentiated startle paradigm
Norrholm, S. D., Jovanovic, T., Vervliet, B., Myers, K. M., Davis, M., Rothbaum, B. O., & Duncan, E. J. (2006) · Learning & Memory · doi:10.1101/lm.393906 · Cited by 167 · see citing works
The role of the amygdala in the extinction of conditioned fear.
Barad, M., Gean, P., & Lutz, B. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.05.029 · Cited by 168 · see citing works
Pattwell, S. S., Bath, K. G., Perez-Castro, R., Lee, F. S., Chao, M. V., & Ninan, I. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5205-11.2012 · Cited by 156 · see citing works
Effects of recent exposure to a conditioned stimulus on extinction of Pavlovian fear conditioningPreprint
Chan, W. Y. M., Leung, H. T., Westbrook, R. F., & McNally, G. P. (2010) · Learning & Memory · doi:10.1101/lm.1912510 · Cited by 156 · see citing works
Disruption of AMPA Receptor Endocytosis Impairs the Extinction, but not Acquisition of Learned Fear
Dalton, G. L., Wang, Y. T., Floresco, S., & Phillips, A. G. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301642 · Cited by 154 · see citing works
Deconstructing the Gestalt: Mechanisms of Fear, Threat, and Trauma Memory Encoding
Maddox, S. A., Hartmann, J., Ross, R., & Ressler, K. J. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.017 · Cited by 150 · see citing works
Sangha, S., Diehl, M. M., Bergstrom, H. C., & Drew, M. R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.11.006 · Cited by 144 · see citing works
Evidence for recovery of fear following immediate extinction in rats and humansPreprint
Schiller, D., Cain, C. K., Curley, N. G., Schwartz, J. S., Stern, S. A., LeDoux, J. E., & Phelps, E. A. (2008) · Learning & Memory · doi:10.1101/lm.909208 · Cited by 150 · see citing works
Dissociation of within- and between-Session Extinction of Conditioned Fear
Plendl, W., & Wotjak, C. T. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.6038-09.2010 · Cited by 148 · see citing works
Amygdala hyperfunction in phobic fear normalizes after exposure.
Goossens, L., Sunaert, S., Peeters, R., Griez, E., & Schruers, K. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.024 · Cited by 151 · see citing works
Neural Mechanisms of Impaired Fear Inhibition in Posttraumatic Stress Disorder
Jovanović, T., & Norrholm, S. D. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00044 · Cited by 142 · see citing works
Amygdala Neurons Differentially Encode Motivation and Reinforcement
Tye, K. M., & Janak, P. H. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5281-06.2007 · Cited by 130 · see citing works
“Importantly, it has been shown that varying with- drawal periods can affect extinction behavior and the degree to which cueinduced reinstatement is expressed (Grimm et al., 2002; Myers et al., 2006).”
BackgroundEnhancing exposure-based therapy from a translational research perspective
Hofmann, S. G. (2007) · Behaviour Research and Therapy · doi:10.1016/j.brat.2007.06.006 · Cited by 133 · see citing works
Sex differences in fear extinction
Velasco, E. R., Florido, A., Milad, M. R., & Andero, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.020 · Cited by 125 · see citing works
Timing of extinction relative to acquisition: a parametric analysis of fear extinction in humans
Norrholm, S. D., Vervliet, B., Jovanovic, T., Boshoven, W., Myers, K. M., Davis, M., Rothbaum, B., & Duncan, E. J. (2008) · Behavioral Neuroscience · doi:10.1037/a0012604 · Cited by 120 · see citing works
Conditioning- and time-dependent increases in context fear and generalizationPreprint
Poulos, A. M., Mehta, N., Lu, B., Amir, D., Livingston, B., Santarelli, A., Zhuravka, I., & Fanselow, M. S. (2016) · Learning & Memory · doi:10.1101/lm.041400.115 · Cited by 116 · 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
Psychological and Neural Mechanisms of Experimental Extinction: A Selective Review
Delamater, A., & Westbrook, R. F. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.09.016 · Cited by 110 · see citing works
A developmental dissociation of context and GABA effects on extinguished fear in rats.
Kim, J., & Richardson, R. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.1.131 · Cited by 123 · see citing works
Mao, S.-C., Hsiao, Y., & Gean, P. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0365-06.2006 · Cited by 112 · see citing works
Costanzi, M., Cannas, S., Saraulli, D., Rossi‐Arnaud, C., & Cestari, V. (2011) · Learning & Memory · doi:10.1101/lm.2175811 · Cited by 111 · see citing works
Alvarez, R. P., Johnson, L., & Grillon, C. (2007) · Learning & Memory · doi:10.1101/lm.493707 · Cited by 110 · see citing works
Laurent, V., Marchand, A. R., & Westbrook, R. F. (2008) · Learning & Memory · doi:10.1101/lm.928208 · Cited by 104 · see citing works
Briscione, M. A., Jovanovic, T., & Norrholm, S. D. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00088 · Cited by 105 · see citing works
Noradrenergic blockade stabilizes prefrontal activity and enables fear extinction under stress
Fitzgerald, P. J., Giustino, T. F., Seemann, J. R., & Maren, S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1500682112 · Cited by 101 · see citing works
Abumaria, N., Yin, B., Zhang, L., Li, X., Chen, T., Descalzi, G., Zhao, L., Ahn, M., Luo, L., Chen, R., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3782-11.2011 · Cited by 101 · see citing works
Sangha, S., Narayanan, R. T., Bergado-Acosta, J. R., Stork, O., Seidenbecher, T., & Pape, H. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2620-09.2009 · Cited by 99 · see citing works
Nature and causes of the immediate extinction deficit: A brief review
Maren, S. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.10.012 · Cited by 98 · see citing works
Delayed Extinction Attenuates Conditioned Fear Renewal and Spontaneous Recovery in Humans
Huff, N., Hernandez, J., Blanding, N. Q., & LaBar, K. (2009) · Behavioral Neuroscience · doi:10.1037/a0016511 · Cited by 91 · see citing works
Lack of Medial Prefrontal Cortex Activation Underlies the Immediate Extinction Deficit
Kim, S. C., Jo, Y. S., Kim, I. H., Kim, H., & Choi, J.-S. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4145-09.2010 · Cited by 96 · see citing works
Astill Wright, L., Horstmann, L., Holmes, E. A., & Bisson, J. I. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01570-w · Cited by 97 · see citing works
Thy1-Expressing Neurons in the Basolateral Amygdala May Mediate Fear Inhibition
Jasnow, A. M., Ehrlich, D., Choi, D. C., Dabrowska, J., Bowers, M. E., McCullough, K. M., Rainnie, D. G., & Ressler, K. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5539-12.2013 · Cited by 92 · see citing works
Inserra, A. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00330 · Cited by 91 · see citing works
Goode, T. D., & Maren, S. (2014) · ILAR Journal · doi:10.1093/ilar/ilu008 · Cited by 87 · see citing works
Haaker, J., Maren, S., Andreatta, M., Merz, C. J., Richter, J., Richter, S. H., Drexler, S. M., Lange, M. D., Jüngling, K., Nees, F., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.020 · Cited by 89 · see citing works
Li, G., Nair, S. S., & Quirk, G. J. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90765.2008 · Cited by 86 · see citing works
Borgomaneri, S., Battaglia, S., Sciamanna, G., Tortora, F., & Laricchiuta, D. (2021) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.04.036 · Cited by 75 · see citing works
Wout‐Frank, M. V. ‘., Longo, S. M., Reddy, M. K., Philip, N. S., Bowker, M., & Greenberg, B. D. (2017) · Brain and Behavior · doi:10.1002/brb3.681 · Cited by 85 · see citing works
Modulation of Fear Extinction by Stress, Stress Hormones and Estradiol: A Review
Stockhorst, U., & Antov, M. I. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00359 · Cited by 86 · see citing works
Pan, W. X., Schmidt, R., Wickens, J. R., & Hyland, B. I. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0255-08.2008 · Cited by 84 · see citing works
Adding imagery rescripting during extinction leads to less ABA renewal
Dibbets, P., Poort, H., & Arntz, A. (2012) · Journal of Behavior Therapy and Experimental Psychiatry · doi:10.1016/j.jbtep.2011.08.006 · Cited by 81 · see citing works
Can Transcranial Direct Current Stimulation Augment Extinction of Conditioned Fear?
Wout‐Frank, M. V. ‘., Mariano, T. Y., Garnaat, S. L., Reddy, M. K., Rasmussen, S. A., & Greenberg, B. D. (2016) · Brain stimulation · doi:10.1016/j.brs.2016.03.004 · Cited by 81 · see citing works
Langton, J. M., Kim, J. H., Nicholas, J., & Richardson, R. (2007) · Learning & Memory · doi:10.1101/lm.692407 · Cited by 80 · see citing works
Golub, Y., Mauch, C. P., Dahlhoff, M., & Wotjak, C. T. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.08.019 · Cited by 80 · see citing works
Bu, W., Ren, H., Deng, Y., Mar, N. D., Guley, N., Moore, B. M., II, Honig, M. G., & Reiner, A. J. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00449 · Cited by 79 · see citing works
Extinction of Conditioned Fear in Adolescents and Adults: A Human fMRI Study
Ganella, D. E., Drummond, K. D., Ganella, E. P., Whittle, S., & Kim, J. H. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00647 · Cited by 77 · see citing works
Garcia, N. M., Walker, R. S. W., & Zoellner, L. A. (2018) · Clinical Psychology Review · doi:10.1016/j.cpr.2018.06.005 · Cited by 87 · see citing works
Mechanisms of fear learning and extinction: synaptic plasticity–fear memory connection
Luchkina, N. V., & Bolshakov, V. Y. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5104-4 · Cited by 77 · see citing works
Learning and memory in conditioned fear extinction: Effects of d-cycloserine
Vervliet, B. (2007) · Acta Psychologica · doi:10.1016/j.actpsy.2007.07.001 · Cited by 78 · see citing works
Blockade of amygdala metabotropic glutamate receptor subtype 1 impairs fear extinction
Kim, J., Lee, S., Park, H., Song, B., Hong, I., Geum, D., Shin, K., & Choi, S. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.01.125 · Cited by 78 · see citing works
Sijbrandij, M., Engelhard, I. M., Lommen, M. J. J., Leer, A., & Baas, J. M. P. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.09.008 · Cited by 77 · see citing works
Memory reactivation effects independent of reconsolidationPreprint
Gisquet-Verrier, P., & Riccio, D. C. (2012) · Learning & Memory · doi:10.1101/lm.026054.112 · Cited by 77 · see citing works
Attentional, associative, and configural mechanisms in extinction.
Larrauri, J. A., & Schmajuk, N. A. (2008) · Psychological Review · doi:10.1037/0033-295x.115.3.640 · Cited by 74 · see citing works
Woods, A. M., & Bouton, M. E. (2008) · Learning & Memory · doi:10.1101/lm.1078508 · Cited by 70 · see citing works
Lonsdorf, T. B., & Kalisch, R. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.36 · Cited by 70 · see citing works
Cholinergic blockade frees fear extinction from its contextual dependency
Zelikowsky, M., Hast, T. A., Bennett, R. Z., Merjanian, M., Nocera, N. A., Ponnusamy, R., & Fanselow, M. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.08.006 · Cited by 71 · see citing works
Bukalo, O., Pinard, C. R., & Holmes, A. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12779 · Cited by 67 · see citing works
Event segmentation protects emotional memories from competing experiences encoded close in time
Dunsmoor, J. E., Kroes, M. C. W., Moscatelli, C. M., Evans, M. D., Davachi, L., & Phelps, E. A. (2018) · Nature Human Behaviour · doi:10.1038/s41562-018-0317-4 · Cited by 69 · see citing works
- Authors
- Myers, K. M., Ressler, K. J., & Davis, M.
- Affiliations
- Emory University (US)
- Venue
- Learning & Memory
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2006-03
- Volume
- 13
- Issue
- 2
- Pages
- 216-223
- ISSN
- 1072-0502 (ISSN-L)
- 1549-5485
- PMC
- PMC1409828
- OpenAlex
- W2156746271
- Cited by
- 334
- References
- 70
- Citations by year
- 2026: 12 · 2025: 14 · 2024: 9 · 2023: 11 · 2022: 17 · 2021: 15 · 2020: 12 · 2019: 18 · 2018: 23 · 2017: 10 · 2016: 16 · 2015: 12 · 2014: 17 · 2013: 20 · 2012: 24
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Learning & Memory (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (9876754)
- Woodruff Foundation
- National Institute of Mental Health (MH 47840, R37MH047840, R01MH047840)
- 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, spontaneous recovery, reinstatement, renewal, inhibitory learning, depotentiation, unlearning, long-term potentiation, amygdala, fear conditioning
- MeSH terms
- Animals, Association Learning, Conditioning, Classical, Extinction, Psychological, Fear, Male, Retention, Psychology, Time Factors, Rats, Sprague-Dawley, Rats
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