Preventing the return of fear in humans using reconsolidation update mechanisms
Open accessAbstract
Recent research on changing fears has examined targeting reconsolidation. During reconsolidation, stored information is rendered labile after being retrieved. Pharmacological manipulations at this stage result in an inability to retrieve the memories at later times, suggesting that they are erased or persistently inhibited. Unfortunately, the use of these pharmacological manipulations in humans can be problematic. Here we introduce a non-invasive technique to target the reconsolidation of fear memories in humans. We provide evidence that old fear memories can be updated with non-fearful information provided during the reconsolidation window. As a consequence, fear responses are no longer expressed, an effect that lasted at least a year and was selective only to reactivated memories without affecting others. These findings demonstrate the adaptive role of reconsolidation as a window of opportunity to rewrite emotional memories, and suggest a non-invasive technique that can be used safely in humans to prevent the return of fear.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Reactivation during wakefulness destabilized memories rendering them susceptible to interference learning, as indicated by impaired memory recall for the originally learned card-pair locations after interference learning.
“As expected from reconsolidation studies (e.g., Refs.844, 845, 1043), reactivation during wakefulness destabilized memories rendering them susceptible to interference learning, as indicated by impaired memory recall for the originally learned card-pair locations after interference learning (FIGURE 4D).”
From About Sleep's Role in Memory (2013) · cites this paper as [1043]
The Persistence of reconsolidation blockade section (page not provided) says reactivation rendered fear memories labile and extinction during that period prevented the return of fear. The paper does not report a card-pair location task or impaired recall of originally learned locations after interference learning; its experiments measured conditioned fear responses. (LLM, conf=0.90)
Experimental — accuracy not yet measuredThe first studies that translated findings in non-human animals to humans used classical aversive conditioning to induce a simple emotional memory.
“The first studies that translated findings in non-human animals [48,88,89] to humans used classical aversive conditioning to induce a simple emotional memory [94,95].”
From Multiple memory systems, multiple time points: How science can inform treatment to control the expression of unwanted emotional memories (2018) · cites this paper as [94]
Conditioned physiological responses could be eliminated by presenting a single reminder cue and administering propranolol or an extinction procedure within the putative reconsolidation window.
“These showed that conditioned physiological responses could be eliminated by presenting a single reminder cue (the CS+) and administering a pharmacological agent (the beta-adrenergic antagonist propranolol [95]) or a behavioural intervention (an extinction procedure [94]) within the putative reconsolidation window.”
From Multiple memory systems, multiple time points: How science can inform treatment to control the expression of unwanted emotional memories (2018) · cites this paper as [94]
The effect of retrieval + extinction on attenuation of spontaneous recovery and reinstatement was evident a year after the original acquisition of fear.
“Following this work, Schiller et al. (59), using skin conductance measures, showed that retrieval + extinction (with 10 min but not 6 h between sessions) attenuated spontaneous recovery and reinstatement of fear in human subjects, an effect that was evident a year after the original acquisition of fear.”
From Conditioned fear associated phenotypes as robust, translational indices of trauma-, stressor-, and anxiety-related behaviors (2014) · cites this paper as [59]
Retrieval + extinction with 10 min but not 6 h between sessions attenuated spontaneous recovery and reinstatement of fear in human subjects.
“Following this work, Schiller et al. (59), using skin conductance measures, showed that retrieval + extinction (with 10 min but not 6 h between sessions) attenuated spontaneous recovery and reinstatement of fear in human subjects, an effect that was evident a year after the original acquisition of fear.”
From Conditioned fear associated phenotypes as robust, translational indices of trauma-, stressor-, and anxiety-related behaviors (2014) · cites this paper as [59]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
Self-citationMemory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250 · 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
Self-citationGazzaniga, M. S., & Bizzi, E. (2000) · Cited by 2,525 · 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
Phelps, E. A., Delgado, M. R., Nearing, K. I., & LeDoux, J. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.042 · Cited by 1,753 · see citing works
Self-citationContext, ambiguity, and unlearning: sources of relapse after behavioral extinction
Bouton, M. E. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01546-9 · Cited by 1,662 · 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
Rauch, S. L., Shin, L. M., & Phelps, E. A. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.06.004 · Cited by 1,397 · see citing works
Self-citationMilad, M. R., Wright, C. I., Orr, S. P., Pitman, R. K., Quirk, G. J., & Rauch, S. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.10.011 · Cited by 1,197 · see citing works
Dissociable stages of human memory consolidation and reconsolidation
Walker, M. P., Brakefield, T., Allan Hobson, J., & Stickgold, R. (2003) · Nature · doi:10.1038/nature01930 · Cited by 1,025 · 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
Self-citationMisanin, J. R., Miller, R. R., & Lewis, D. J. (1968) · Science · doi:10.1126/science.160.3827.554 · Cited by 872 · see citing works
Beyond extinction: erasing human fear responses and preventing the return of fear
Kindt, M., Soeter, M., & Vervliet, B. (2009) · Nature Neuroscience · doi:10.1038/nn.2271 · Cited by 826 · see citing works
Independent cellular processes for hippocampal memory consolidation and reconsolidation
Lee, J. L. C., Everitt, B. J., & Thomas, K. L. (2004) · Science · doi:10.1126/science.1095760 · Cited by 825 · see citing works
Alberini, C. M. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2004.11.001 · Cited by 594 · see citing works
Brunet, A., Orr, S. P., Tremblay, J., Robertson, K., Nader, K., & Pitman, R. K. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2007.05.006 · Cited by 548 · see citing works
Reconsolidation of episodic memories: A subtle reminder triggers integration of new information
Hupbach, A., Gomez, R., Hardt, O., & Nadel, L. (2007) · Learning & Memory · doi:10.1101/lm.365707 · Cited by 544 · see citing works
Kalisch, R., Korenfeld, E., Stephan, K. E., Weiskopf, N., Seymour, B., & Dolan, R. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2021-06.2006 · Cited by 493 · see citing works
Reconsolidation and Extinction of Conditioned Fear: Inhibition and Potentiation
Lee, J. L. C., Milton, A. L., & Everitt, B. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2466-06.2006 · Cited by 479 · see citing works
Characterization of fear memory reconsolidation
Duvarci, S., & Nader, K. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2971-04.2004 · Cited by 379 · see citing works
Reconsolidation: the advantage of being refocused
Dudai, Y. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.03.010 · Cited by 357 · see citing works
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
The Pharmacology of Memory: A Neurobiological Perspective
Squire, L. R., & Davis, H. P. (1981) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pa.21.040181.001543 · Cited by 332 · see citing works
Reconsolidation of declarative memory in humans
Forcato, C., Burgos, V. L., Argibay, P. F., Molina, V. A., Pedreira, M. E., & Maldonado, H. (2007) · Learning & Memory · doi:10.1101/lm.486107 · Cited by 229 · see citing works
Foa, E. B., Franklin, M. E., & Moser, J. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01552-4 · Cited by 219 · see citing works
Chronic stress impairs recall of extinction of conditioned fear
Miracle, A. D., BRACE, M., HUYCK, K., SINGLER, S., & Wellman, C. L. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.10.005 · Cited by 217 · see citing works
Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala
Doyère, V., Dębiec, J., Monfils, M.-H., Schafe, G. E., & LeDoux, J. E. (2007) · Nature Neuroscience · doi:10.1038/nn1871 · Cited by 200 · see citing works
Self-citationAlberini (2006) · doi:10.1007/s00018-006-6025-7 · Cited by 158 · 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
Self-citationIn memory of consolidationPreprint
Sara, S. J., & Hars, B. (2006) · Learning & Memory · doi:10.1101/lm.338406 · Cited by 114 · see citing works
Alvarez, R. P., Johnson, L., & Grillon, C. (2007) · Learning & Memory · doi:10.1101/lm.493707 · Cited by 110 · see citing works
Tollenaar, M. S., Elzinga, B. M., Spinhoven, P., & Everaerd, W. T. A. M. (2009) · Psychopharmacology · doi:10.1007/s00213-008-1427-x · Cited by 49 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
Maximizing exposure therapy: An inhibitory learning approach
Craske, M. G., Treanor, M., Conway, C. C., Zbozinek, T., & Vervliet, B. (2014) · Behaviour Research and Therapy · doi:10.1016/j.brat.2014.04.006 · Cited by 2,339 · see citing works
“This effect has since been demonstrated in healthy human samples (Agren et al., 2012; Schiller et al., 2010).”
From circuits to behaviour in the amygdala
Janak, P. H., & Tye, K. M. (2015) · Nature · doi:10.1038/nature14188 · Cited by 2,011 · see citing works
Biological studies of post-traumatic stress disorder
Pitman, R. K., Rasmusson, A. M., Koenen, K. C., Shin, L. M., Orr, S. P., Gilbertson, M. W., Milad, M. R., & Liberzon, I. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3339 · Cited by 1,529 · see citing works
Fear Extinction as a Model for Translational Neuroscience: Ten Years of Progress
Milad, M. R., & Quirk, G. J. (2012) · Annual Review of Psychology · doi:10.1146/annurev.psych.121208.131631 · Cited by 1,466 · see citing works
Drug addiction: updating actions to habits to compulsions ten years on
Everitt, B. J., & Robbins, T. W. (2016) · Annual Review of Psychology · doi:10.1146/annurev-psych-122414-033457 · Cited by 1,225 · see citing works
The Molecular and Systems Biology of Memory
Kandel, E. R., Dudai, Y., & Mayford, M. R. (2014) · Cell · doi:10.1016/j.cell.2014.03.001 · Cited by 1,134 · see citing works
Memory engrams: Recalling the past and imagining the future
Josselyn, S. A., & Tonegawa, S. (2020) · Science · doi:10.1126/science.aaw4325 · Cited by 1,087 · see citing works
Using Neuroscience to Help Understand Fear and Anxiety: A Two-System Framework
LeDoux, J. E., & Pine, D. S. (2016) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2016.16030353 · Cited by 1,035 · see citing works
Self-citationMolecular mechanisms of fear learning and memory
Johansen, J. P., Cain, C. K., Ostroff, L. E., & LeDoux, J. E. (2011) · Cell · doi:10.1016/j.cell.2011.10.009 · Cited by 1,012 · see citing works
Self-citationPape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · see citing works
LeDoux, J. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400335111 · Cited by 891 · see citing works
Self-citationLonsdorf, 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
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644 · see citing works
Adolphs, R. (2013) · Current Biology · doi:10.1016/j.cub.2012.11.055 · Cited by 524 · see citing works
A Memory Retrieval-Extinction Procedure to Prevent Drug Craving and Relapse
Xue, Y.-X., Luo, Y.-X., Wu, P., Shi, H.-S., Xue, L.-F., Chen, C., Zhu, W.-L., Ding, Z.-B., Bao, Y.-P., Shi, J., et al. (2012) · Science · doi:10.1126/science.1215070 · Cited by 511 · see citing works
The ecology of human fear: survival optimization and the nervous system
Mobbs, D., Hagan, C. C., Dalgleish, T., Silston, B., & Prévost, C. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00055 · Cited by 498 · see citing works
Efficacy of Cognitive Behavioral Therapy for Anxiety Disorders: A Review of Meta-Analytic Findings
Olatunji, B. O., Cisler, J. M., & Deacon, B. J. (2010) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2010.04.002 · Cited by 483 · 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
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works
Environment and Brain Plasticity: Towards an Endogenous Pharmacotherapy
Sale, A., Berardi, N., & Maffei, L. (2014) · Physiological Reviews · doi:10.1152/physrev.00036.2012 · Cited by 402 · see citing works
Fear erasure in mice requires synergy between antidepressant drugs and extinction training
Karpova, N. N., Pickenhagen, A., Lindholm, J., Tiraboschi, E., Kulesskaya, N., Ágústsdóttir, A., Antila, H., Popova, D., Akamine, Y., Sullivan, R., et al. (2011) · Science · doi:10.1126/science.1214592 · Cited by 382 · see citing works
Foa, E. B., & McLean, C. P. (2016) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-021815-093533 · Cited by 360 · see citing works
Epigenetic Priming of Memory Updating during Reconsolidation to Attenuate Remote Fear Memories
Gräff, J., Joseph, N. F., Horn, M. E., Samiei, A., Meng, J., Seo, J., Rei, D., Bero, A. W., Phan, T. X., Wagner, F., et al. (2014) · Cell · doi:10.1016/j.cell.2013.12.020 · Cited by 357 · 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
Self-citationJames, E. L., Bonsall, M. B., Hoppitt, L., Tunbridge, E. M., Geddes, J. R., Milton, A. L., & Holmes, E. A. (2015) · Psychological Science · doi:10.1177/0956797615583071 · Cited by 333 · see citing works
Labile or stable: opposing consequences for memory when reactivated during waking and sleep
Diekelmann, S., Büchel, C., Born, J., & Rasch, B. (2011) · Nature Neuroscience · doi:10.1038/nn.2744 · Cited by 344 · see citing works
Emotional learning selectively and retroactively strengthens memories for related events
Dunsmoor, J. E., Murty, V. P., Davachi, L., & Phelps, E. A. (2015) · Nature · doi:10.1038/nature14106 · Cited by 332 · see citing works
Everitt, B. J. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12644 · Cited by 318 · see citing works
James, E. L., Lau-Zhu, A., Clark, I. A., Visser, R. M., Hagenaars, M. A., & Holmes, E. A. (2016) · Clinical Psychology Review · doi:10.1016/j.cpr.2016.04.010 · Cited by 300 · see citing works
Cognitive emotion regulation fails the stress test
Raio, C. M., Orederu, T. A., Palazzolo, L., Shurick, A. A., & Phelps, E. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305706110 · Cited by 302 · see citing works
Self-citationDissociating response systems: Erasing fear from memory
Soeter, M., & Kindt, M. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.03.004 · Cited by 290 · see citing works
FAAH genetic variation enhances fronto-amygdala function in mouse and human
Dincheva, I., Drysdale, A. T., Hartley, C. A., Johnson, D. C., Jing, D., King, E. C., Ra, S., Gray, J. M., Yang, R., DeGruccio, A. M., et al. (2015) · Nature Communications · doi:10.1038/ncomms7395 · Cited by 289 · see citing works
Self-citationThe persistence of maladaptive memory: Addiction, drug memories and anti-relapse treatments
Milton, A. L., & Everitt, B. J. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.01.002 · Cited by 279 · see citing works
Holmes, E. A., James, E. L., Kilford, E. J., & Deeprose, C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013706 · Cited by 273 · 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
“studies examined the duration of the effect, and in that case it was reported to last at least 1 year (Schiller et al., 2010).”
BackgroundMethodInfluentialDisrupting reconsolidation: Pharmacological and behavioral manipulations
Soeter, M., & Kindt, M. (2011) · Learning & Memory · doi:10.1101/lm.2148511 · Cited by 262 · see citing works
Memory Retrieval and the Passage of Time: From Reconsolidation and Strengthening to Extinction
Inda, M. C., Muravieva, E. V., & Alberini, C. M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4736-10.2011 · Cited by 261 · see citing works
Sleep and REM sleep disturbance in the pathophysiology of PTSD: the role of extinction memory
Pace-Schott, E. F., Germain, A., & Milad, M. R. (2015) · Biology of Mood & Anxiety Disorders · doi:10.1186/s13587-015-0018-9 · Cited by 255 · see citing works
Promoting memory consolidation during sleep: A meta-analysis of targeted memory reactivation
Hu, X., Cheng, L. Y., Chiu, M. H., & Paller, K. A. (2020) · Psychological Bulletin · doi:10.1037/bul0000223 · Cited by 232 · see citing works
Reconsolidation in a human fear conditioning study: A test of extinction as updating mechanism
Kindt, M., & Soeter, M. (2013) · Biological Psychology · doi:10.1016/j.biopsycho.2011.09.016 · Cited by 240 · see citing works
Aberrant learning and memory in addiction
Torregrossa, M. M., Corlett, P. R., & Taylor, J. R. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.02.014 · Cited by 223 · see citing works
Effects of sleep on memory for conditioned fear and fear extinction.
Pace-Schott, E. F., Germain, A., & Milad, M. R. (2015) · Psychological Bulletin · doi:10.1037/bul0000014 · Cited by 218 · see citing works
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript (Maren, 2011; Monfils, Cowansage, Klann, & LeDoux, 2009; Quirk et al., 2010; Schiller & Delgado, 2010; Schiller et al., 2010).”
BackgroundInsel, T. R. (2010) · JAMA · doi:10.1001/jama.2010.555 · Cited by 224 · see citing works
Carlbring, P., Apelstrand, M., Sehlin, H., Amir, N., Rousseau, A., Hofmann, S. G., & Andersson, G. (2012) · BMC Psychiatry · doi:10.1186/1471-244x-12-66 · Cited by 215 · see citing works
Reconsolidation and the dynamic nature of memory
Nader, K. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021782 · Cited by 221 · see citing works
Human memory reconsolidation: A guiding framework and critical review of the evidence.
Elsey, J. W. B., Van Ast, V. A., & Kindt, M. (2018) · Psychological Bulletin · doi:10.1037/bul0000152 · Cited by 199 · see citing works
The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation
Finnie, P. S. B., & Nader, K. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.008 · Cited by 189 · see citing works
Litz, B. T., Salters-Pedneault, K., Steenkamp, M. M., Hermos, J. A., Bryant, R. A., Otto, M. W., & Hofmann, S. G. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.05.006 · Cited by 196 · see citing works
Retrieval-specific endocytosis of GluA2-AMPARs underlies adaptive reconsolidation of contextual fear
Rao-Ruiz, P., Rotaru, D. C., van der Loo, R. J., Mansvelder, H. D., Stiedl, O., Smit, A. B., & Spijker, S. (2011) · Nature Neuroscience · doi:10.1038/nn.2907 · Cited by 192 · see citing works
Memory and law: what can cognitive neuroscience contribute?
Schacter, D. L., & Loftus, E. F. (2013) · Nature Neuroscience · doi:10.1038/nn.3294 · Cited by 188 · see citing works
Forgetting as a form of adaptive engram cell plasticity
Ryan, T. J., & Frankland, P. W. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00548-3 · Cited by 182 · see citing works
Dunsmoor, J. E., Campese, V. D., Ceceli, A. O., LeDoux, J. E., & Phelps, E. A. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.12.008 · Cited by 165 · see citing works
Self-citationLearning to forget: manipulating extinction and reconsolidation processes to treat addiction
Torregrossa, M. M., & Taylor, J. R. (2013) · Psychopharmacology · doi:10.1007/s00213-012-2750-9 · Cited by 172 · see citing works
The computational nature of memory modification
Gershman, S. J., Monfils, M.-H., Norman, K. A., & Niv, Y. (2017) · eLife · doi:10.7554/elife.23763 · Cited by 172 · see citing works
Self-citationNavigating the garden of forking paths for data exclusions in fear conditioning research
Lonsdorf, T. B., Klingelhöfer-Jens, M., Andreatta, M., Beckers, T., Chalkia, A., Gerlicher, A., Jentsch, V. L., Meir Drexler, S., Mertens, G., Richter, J., et al. (2019) · eLife · doi:10.7554/elife.52465 · Cited by 164 · see citing works
Selective early-acquired fear memories undergo temporary suppression during adolescence
Pattwell, S. S., Bath, K. G., Casey, B. J., Ninan, I., & Lee, F. S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012975108 · Cited by 161 · see citing works
Reactivation of recall-induced neurons contributes to remote fear memory attenuation
Khalaf, O., Resch, S., Dixsaut, L., Gorden, V., Glauser, L., & Gräff, J. (2018) · Science · doi:10.1126/science.aas9875 · Cited by 146 · see citing works
The role of sleep and sleep deprivation in consolidating fear memories
Menz, M. M., Rihm, J. S., Salari, N., Born, J., Kalisch, R., Pape, H. C., Marshall, L., & Büchel, C. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.03.001 · Cited by 158 · see citing works
Soeter, M., & Kindt, M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.307 · Cited by 150 · see citing works
Kredlow, M. A., Unger, L. D., & Otto, M. W. (2016) · Psychological Bulletin · doi:10.1037/bul0000034 · Cited by 130 · see citing works
Cannabinoid facilitation of fear extinction memory recall in humans
Rabinak, C. A., Angstadt, M., Sripada, C. S., Abelson, J. L., Liberzon, I., Milad, M. R., & Phan, K. L. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.063 · Cited by 163 · see citing works
Koizumi, A., Amano, K., Cortese, A., Shibata, K., Yoshida, W., Seymour, B., Kawato, M., & Lau, H. (2016) · Nature Human Behaviour · doi:10.1038/s41562-016-0006 · Cited by 133 · see citing works
“The effect of day was significant (analysis of variance (ANOVA); F(2, 15) = 3.”
MethodHuman memory reconsolidation can be explained using the temporal context model
Sederberg, P. B., Gershman, S. J., Polyn, S. M., & Norman, K. A. (2011) · Psychonomic Bulletin & Review · doi:10.3758/s13423-011-0086-9 · Cited by 125 · see citing works
Exposure therapy in eating disorders revisited
Koskina, A., Campbell, I. C., & Schmidt, U. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.11.010 · Cited by 127 · see citing works
Oyarzún, J. P., Lopez-Barroso, D., Fuentemilla, L., Cucurell, D., Pedraza, C., Rodriguez-Fornells, A., & de Diego-Balaguer, R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038849 · 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
Golkar, A., Bellander, M., Olsson, A., & Öhman, A. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00080 · Cited by 120 · see citing works
St. Jacques, P. L., & Schacter, D. L. (2013) · Psychological Science · doi:10.1177/0956797612457377 · Cited by 119 · see citing works
Jarome, T. J., Ferrara, N. C., Kwapis, J. L., & Helmstetter, F. J. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.01.001 · Cited by 112 · see citing works
Marin, M.-F., Camprodon, J. A., Dougherty, D. D., & Milad, M. R. (2014) · Depression and Anxiety · doi:10.1002/da.22252 · Cited by 106 · see citing works
Ketamine effects on memory reconsolidation favor a learning model of delusions
Corlett, P. R., Cambridge, V., Gardner, J. M., Piggot, J. S., Turner, D. C., Everitt, J. C., Arana, F. S., Morgan, H. L., Milton, A. L., Lee, J. L., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065088 · Cited by 105 · 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
A behavioural neuroscience perspective on the aetiology and treatment of anxiety disorders
Kindt, M. (2014) · Behaviour Research and Therapy · doi:10.1016/j.brat.2014.08.012 · Cited by 103 · see citing works
Visser, R. M., Lau-Zhu, A., Henson, R. N., & Holmes, E. A. (2018) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2017.0209 · Cited by 95 · see citing works
Erasing fear for an imagined threat event
Soeter, M., & Kindt, M. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.03.011 · Cited by 95 · see citing works
Levy, I., & Schiller, D. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2020.11.007 · Cited by 95 · see citing works
Björkstrand, J., Agren, T., Åhs, F., Frick, A., Larsson, E.-M., Hjorth, O., Furmark, T., & Fredrikson, M. (2016) · Current Biology · doi:10.1016/j.cub.2016.08.022 · Cited by 94 · 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
Dreams and Psychedelics: Neurophenomenological Comparison and Therapeutic Implications
Kraehenmann, R. (2017) · Current Neuropharmacology · doi:10.2174/1573413713666170619092629 · Cited by 92 · see citing works
Neurophysiology of Remembering
Buzsáki, G., McKenzie, S., & Davachi, L. (2022) · Annual Review of Psychology · doi:10.1146/annurev-psych-021721-110002 · Cited by 84 · see citing works
Sevenster, D., Beckers, T., & Kindt, M. (2012) · Psychophysiology · doi:10.1111/j.1469-8986.2012.01450.x · Cited by 88 · see citing works
Inserra, A. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00330 · Cited by 91 · see citing works
Nabel, E. M., & Morishita, H. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00146 · Cited by 85 · see citing works
Epigenetic mechanisms in fear conditioning: Implications for treating post-traumatic stress disorder
Kwapis, J. L., & Wood, M. A. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.08.005 · Cited by 87 · see citing works
Extinction during memory reconsolidation blocks recovery of fear in adolescents
Johnson, D. C., & Casey, B. J. (2015) · Scientific Reports · doi:10.1038/srep08863 · Cited by 80 · see citing works
Self-citationSensitive periods in affective development: nonlinear maturation of fear learning
Hartley, C. A., & Lee, F. S. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.179 · Cited by 80 · see citing works
Cognitive neuroscience perspective on memory: overview and summary
Sridhar, S., Khamaj, A., & Asthana, M. K. (2023) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2023.1217093 · Cited by 80 · see citing works
Walsh, K. H., Das, R. K., Saladin, M. E., & Kamboj, S. K. (2018) · Psychopharmacology · doi:10.1007/s00213-018-4983-8 · Cited by 77 · see citing works
Enhanced Extinction of Aversive Memories by High-Frequency Stimulation of the Rat Infralimbic Cortex
Maroun, M., Kavushansky, A., Holmes, A., Wellman, C., & Motanis, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035853 · Cited by 79 · see citing works
Galatzer-Levy, I. R., Bonanno, G. A., Bush, D. E. A., & LeDoux, J. E. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00055 · Cited by 75 · see citing works
Augmentation of exposure therapy with post-session administration of D-cycloserine
Tart, C. D., Handelsman, P. R., DeBoer, L. B., Rosenfield, D., Pollack, M. H., Hofmann, S. G., Powers, M. B., Otto, M. W., & Smits, J. A. J. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.09.024 · Cited by 75 · see citing works
A critical role for protein degradation in the nucleus accumbens core in cocaine reward memory
Ren, Z.-Y., Liu, M.-M., Xue, Y.-X., Ding, Z.-B., Xue, L.-F., Zhai, S.-D., & Lu, L. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2012.243 · Cited by 73 · see citing works
In search for boundary conditions of reconsolidation: a failure of fear memory interference
Schroyens, N., Beckers, T., & Kindt, M. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00065 · Cited by 70 · see citing works
Reconsolidation of traumatic memories for PTSD: a randomized controlled trial of 74 male veterans
Gray, R., Budden-Potts, D., & Bourke, F. (2019) · Psychotherapy Research · doi:10.1080/10503307.2017.1408973 · Cited by 66 · see citing works
Durable effects of cognitive restructuring on conditioned fear.
Shurick, A. A., Hamilton, J. R., Harris, L. T., Roy, A. K., Gross, J. J., & Phelps, E. A. (2012) · Emotion · doi:10.1037/a0029143 · Cited by 65 · see citing works
Self-citationBjörkstrand, J., Agren, T., Frick, A., Engman, J., Larsson, E.-M., Furmark, T., & Fredrikson, M. (2015) · PLOS ONE · doi:10.1371/journal.pone.0129393 · Cited by 65 · see citing works
Deeprose, C., Zhang, S., DeJong, H., Dalgleish, T., & Holmes, E. A. (2012) · Journal of Behavior Therapy and Experimental Psychiatry · doi:10.1016/j.jbtep.2011.10.008 · Cited by 65 · see citing works
Blocking human fear memory with the matrix metalloproteinase inhibitor doxycycline
Bach, D. R., Tzovara, A., & Vunder, J. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.65 · Cited by 64 · see citing works
- Authors
- Schiller, D., Monfils, M.-H., Raio, C. M., Johnson, D. C., LeDoux, J. E., & Phelps, E. A.
- Affiliations
- New York University (US)
- The University of Texas at Austin (US)
- Corresponding author
- Phelps, Elizabeth A.
- Venue
- Nature
- Published
- 2009-12-09
- Volume
- 463
- Issue
- 7277
- Pages
- 49-53
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3640262
- OpenAlex
- W2100172973
- Cited by
- 1,248
- References
- 33
- Citations by year
- 2026: 38 · 2025: 54 · 2024: 45 · 2023: 43 · 2022: 68 · 2021: 66 · 2020: 75 · 2019: 90 · 2018: 102 · 2017: 97 · 2016: 85 · 2015: 115 · 2014: 91 · 2013: 87 · 2012: 76
- FWCI
- 30.49
- Type
- journal article
- Language
- en
- Update notices
- addendum (2018-07-26)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Canadian Institutes of Health Research
- National Institute of Mental Health (R37MH038774, P50MH058911, R21MH072279, K05MH067048, R01MH038774, R01MH046516, R01MH091147)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
- Keywords
- fear memory reconsolidation, fear extinction, memory updating, return of fear, post-traumatic stress disorder, anxiety disorders, emotional memory
- MeSH terms
- Conditioning, Classical, Cues, Electrodes, Electroshock, Extinction, Psychological, Fear, Humans, Memory, Models, Neurological, Models, Psychological, Neuronal Plasticity, Photic Stimulation, Time Factors
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
