Recent fear is resistant to extinction
Open accessAbstract
In some individuals, fearful experiences (e.g., combat) yield persistent and debilitating psychological disturbances, including posttraumatic stress disorder (PTSD). Early intervention (e.g., debriefing) after psychological trauma is widely practiced and argued to be an effective strategy for limiting subsequent psychopathology, although there has been considerable debate on this point. Here we show in an animal model of traumatic fear that early intervention shortly after an aversive experience yields poor long-term fear reduction. Extinction trials administered minutes after aversive fear conditioning in rats suppressed fear acutely, but fear suppression was not maintained the next day. In contrast, delivering extinction trials 1 day after fear conditioning produced an enduring suppression of fear memory. We further show that the recent experience of an aversive event, not the timing of the extinction intervention per se, inhibits the development of long-term fear extinction. These results reveal that the level of fear present at the time of intervention is a critical factor in the efficacy of extinction. Importantly, our work suggests that early intervention may not yield optimal outcomes in reducing posttraumatic stress, particularly after severe trauma.
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The finding that immediate extinction training prevents return of learned fear was not well replicated in rodents.
“This finding was not well replicated in rodents [see Ref. (88, 89)] and was only weakly observed in humans [see Ref. (90)].”
From Conditioned fear associated phenotypes as robust, translational indices of trauma-, stressor-, and anxiety-related behaviors (2014) · cites this paper as [88]
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“However, other pharmacological manipulation yielded mixed results (Maren and Chang, 2006; Myers et al., 2006; Parsons and Ressler, 2013).”
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“This finding also accords with animal studies that show that rats display impaired extinction learning when extinction is preceded by arousing fear (Maren & Chang, 2006).”
ResultHippocampal involvement in contextual modulation of fear extinction
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“These fearful experiences persist and contribute to, such as, psychological disturbances, post-traumatic stress disorders (PTSD), and panic disorders (Friedman et al., 1994; Maren and Chang, 2006; Feldner et al., 2007).”
BackgroundSeeking a Spotless Mind: Extinction, Deconsolidation, and Erasure of Fear Memory
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Erasing Fear Memories with Extinction Training: Figure 1.
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“Subsequent experiments using variations of this protocol have met with limited success (Maren and Chang, 2006; Norrholm et al., 2008; Schiller et al., 2008; Woods and Bouton, 2008), suggesting the involvement of other, as yet unknown, variables.”
MethodSingle prolonged stress disrupts retention of extinguished fear in rats.Preprint
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BackgroundNoradrenergic Modulation of Fear Conditioning and Extinction
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“Others have reported that stress reduces cued fear extinction (Shumake et al., 2005; Izquierdo et al., 2006; Maren and Chang, 2006) or impairs its recall (Maren and Chang, 2006; Miracle et al., 2006; Garcia et al., 2008).”
BackgroundGlutamate receptors in extinction and extinction-based therapies for psychiatric illness
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“The apparent time-dependent nature of mGluR1 involvement is consistent with evidence from other sources that the mechanisms of short- and long-interval extinction may differ (Cain et al, 2005; Mao et al, 2006; Maren and Chang, 2006; Myers et al, 2006).”
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
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“Infusion of DCS into infralimbic cortex before “immediate” extinction, a protocol which uses a small time interval between conditioning and extinction that can impair extinction (Maren and Chang, 2006), did not facilitate within-session extinction, but did prime subsequent re-extinction during a drug-free state (Chang…”
BackgroundEvidence for recovery of fear following immediate extinction in rats and humansPreprint
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“The present experiments were designed to assess whether the finding of Myers et al. (2006) would apply to a different behavioral measure in rats and would extend to humans.”
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“Extinction learning is also sensitive to the timing relative to trauma, and it is typically less effective when given soon after the traumatic experience (Chang, Berke, & Maren, 2010; Fitzgerald, Giustino, Seemann, & Maren, 2015; Kim, Jo, Kim, Kim, & Choi, 2010; Maren, 2014; Maren & Chang, 2006).”
BackgroundTiming of extinction relative to acquisition: a parametric analysis of fear extinction in humans
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“More recently, Maren and Chang (2006) also reported resistance to spontaneous recovery after immediate (15 min) extinction of conditioned freezing, provided that conditioned fear expression during extinction training is not so high as to prevent extinction from occurring ( Maren & Chang, 2006 ).”
BackgroundInfluentialConditioning- 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
“Other studies examining the time-dependent effects of memory and extinction have focused on auditory fear extinction at shorter times scales from minutes to a few days (Myers et al. 2006; Maren and Chang 2006).”
BackgroundPsychological 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
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“Stress-induced increases in BLA activity mediated by LC-NE may be a viable therapeutic target for individuals with PTSD and related disorders. impaired in humans and rodents when it occurs within minutes to hours of fear conditioning (Maren and Chang, 2006; Chang et al., 2010; Kim et al., 2010; Fitzgerald et al., 2015…”
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“Myers et al. (2006) measured conditioned fear using fear-potentiated startle.”
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“Recent work in animal models suggests that early interventions do not yield long-term fear suppression [14,15,57,58,59].”
BackgroundInfluentialRole of Human Ventromedial Prefrontal Cortex in Learning and Recall of Enhanced Extinction
Dunsmoor, J. E., Kroes, M. C. W., Li, J., Daw, N. D., Simpson, H. B., & Phelps, E. A. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2713-18.2019 · Cited by 110 · see citing works
“It will be of interest to test effects of an immediate versus delayed NFE protocol, as its possible NFE is even more effective at a delay, in keeping with findings of EXT standard extinction (Maren and Chang, 2006; Schiller et al., 2008; Huff et al., 2009).”
ResultNoradrenergic 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
Nature and causes of the immediate extinction deficit: A brief review
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“…cases, administering extinction trials soon after fear conditioning results in no long-term fear suppression at all – the so-called immediate extinction deficit (Chang, Berke, & Maren, 2010; Chang & Maren, 2009, 2011; Kim, Jo, Kim, Kim, & Choi, 2010; MacPherson et al., 2013; Maren & Chang, 2006).”
BackgroundDelayed Extinction Attenuates Conditioned Fear Renewal and Spontaneous Recovery in Humans
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“Additionally, other rodent studies have demonstrated that immediate extinction fails to yield long-term fear suppression (Maren & Chang, 2006).”
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
“Recent studies have demonstrated that extinction training administered shortly after the acquisition session does not effectively induce long-term suppression of the fear response (Maren and Chang, 2006; Woods and Bouton, 2008; Chang and Maren, 2009) [but see Myers et al.”
BackgroundResultInfluentialEffect of Conditioned Stimulus Exposure during Slow Wave Sleep on Fear Memory Extinction in Humans
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“Stress prior to conditioning has been shown to facilitate fear learning in rodents and to make fear responding more resistant to attenuation under certain conditions (Corley et al. 2012; Long and Fanselow 2012; Maren and Chang 2006; Rau et al. 2005; Rau and Fanselow 2009; Rodrigues et al. 2009).”
BackgroundHaaker, 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
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
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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
“In adult rodents, findings are mixed with some studies reporting better extinction recall while others reporting worse extinction recall when extinction is given immediately after conditioning (Maren and Chang, 2006; Myers et al., 2006; Monfils et al., 2009).”
BackgroundMechanisms 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
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
“The failure in retention of the extinguished fear in the present study is consistent with a recent report showing that recent fear is resistant to extinction [22].”
ResultThe role of basal forebrain cholinergic neurons in fear and extinction memory
Knox, D. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.06.001 · Cited by 76 · 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
“Second, the results do not support the possibility that a high level of fear around the time of immediate extinction, rather than the brief conditioning-extinction interval on its own, causes strong recovery after immediate extinction (Maren and Chang 2006).”
BackgroundResultInfluentialTaubenfeld, S. M., Riceberg, J. S., New, A. S., & Alberini, C. M. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.07.005 · Cited by 71 · see citing works
“Similarly, in rodents, recent fear is resistant to extinction (65).”
Chang, C.-H., Knapska, E., Orsini, C. A., Rabinak, C. A., Zimmerman, J. M., & Maren, S. (2009) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0823s47 · Cited by 75 · see citing works
Medial prefrontal cortex activation facilitates re-extinction of fear in rats.Preprint
Chang, C.-H., & Maren, S. (2011) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.2070111 · Cited by 69 · 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
“Also of note, performing extinction training soon after conditioning impairs extinction (the ‘immediate extinction effect’) (Maren and Chang, 2006; Myers et al., 2006; Macpherson et al., 2013; Maren, 2014).”
BackgroundEvent 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
Knox, D., & Keller, S. M. (2015) · Hippocampus · doi:10.1002/hipo.22553 · Cited by 66 · see citing works
Chang, C.-H., & Maren, S. (2009) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.1085009 · Cited by 65 · see citing works
“Indeed, we found that reducing the number of conditioning trials enabled extinction shortly after conditioning (Maren and Chang 2006).”
BackgroundInfluentialStress-enhanced fear learning in rats is resistant to the effects of immediate massed extinction
Long, V., & Fanselow, M. S. (2012) · Stress · doi:10.3109/10253890.2011.650251 · Cited by 62 · see citing works
Strain difference in the effect of infralimbic cortex lesions on fear extinction in rats
Chang, C.-H., & Maren, S. (2010) · Behavioral Neuroscience · doi:10.1037/a0019479 · Cited by 57 · see citing works
“Interestingly, LE rats exhibited much higher levels of contextual fear before the outset of extinction training, and this may have impaired both extinction learning and IL function (Akirav & Maroun, 2007; Correll, Rosenkranz, & Grace, 2005; Izquierdo, Wellman, & Holmes, 2006; Maren & Chang, 2006).”
Translationally relevant modeling of PTSD in rodents
Matar, M. A., Zohar, J., & Cohen, H. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1687-6 · Cited by 55 · see citing works
“More recently, impaired extinction learning has been proposed as an alternative mechanism for the formation of PTSD symptoms (Maren and Chang 2006; Myers and Davis 2002).”
BackgroundLong-Term Neural Correlates of Reversible Fear Learning in the Lateral Amygdala
An, B., Hong, I., & Choi, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3017-12.2012 · Cited by 54 · see citing works
Evidence for the persistence of contextual fear memories following immediate extinction
Archbold, G. E. B., Bouton, M. E., & Nader, K. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07161.x · Cited by 52 · see citing works
Jo, Y. S., Namboodiri, V. M. K., Stuber, G. D., & Zweifel, L. S. (2020) · Nature Communications · doi:10.1038/s41467-020-14393-y · Cited by 53 · see citing works
Social buffering enhances extinction of conditioned fear responses in male rats
Mikami, K., Kiyokawa, Y., Takeuchi, Y., & Mori, Y. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.05.001 · Cited by 51 · see citing works
Akirav, I., Segev, A., Motanis, H., & Maroun, M. (2009) · Learning & Memory · doi:10.1101/lm.1565109 · Cited by 51 · see citing works
“Others have reported that stress reduces cued fear extinction (Shumake et al. 2005; Izquierdo et al. 2006; Maren and Chang 2006) or impairs its recall (Maren and Chang 2006; Miracle et al. 2006; Garcia et al. 2007).”
BackgroundNeural circuits for the adaptive regulation of fear and extinction memory
Plas, S. L., Tuna, T., Bayer, H., Juliano, V. A. L., Sweck, S. O., Perez, A. D. A., Hassell, J. E., & Maren, S. (2024) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2024.1352797 · 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
Extinction: Behavioral Mechanisms and Their Implications
Bouton, M. E., & Woods, A. M. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00088-7 · Cited by 47 · see citing works
Binette, A. N., Liu, J., Bayer, H., Crayton, K. L., Melissari, L., Sweck, S. O., & Maren, S. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1442-22.2023 · Cited by 45 · see citing works
“It should be noted that a weaker conditioning procedure consisting of either fewer trials (Maren and Chang, 2006) or weaker footshocks (Giustino et al., 2020) does not result in an immediate extinction deficit.”
BackgroundInfluentialRevealing Context-Specific Conditioned Fear Memories with Full Immersion Virtual Reality
Huff, N., Hernandez, J., Fecteau, M. E., Zielinski, D. J., Brady, R., & LaBar, K. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00075 · Cited by 45 · see citing works
“In light of generating translational research, it is important to determine why it is rare to find robust long-term contextually cued fear in humans whereas rodent studies readily demonstrate that fear to a conditioned cue is well remembered in the original context (e.g., Phillips and LeDoux, 1994; Corcoran and Maren,…”
BackgroundGiustino, T. F., Seemann, J. R., Acca, G. M., Goode, T. D., Fitzgerald, P. J., & Maren, S. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.89 · Cited by 45 · see citing works
Stafford, J. M., Maughan, D. K., Ilioi, E. C., & Lattal, K. M. (2013) · Learning & Memory · doi:10.1101/lm.029801.112 · Cited by 45 · see citing works
Exposure 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
“, 2006), impaired extinction learning has been proposed as an alternative mechanism for the formation of PTSD symptoms (Blechert et al., 2007 ; Guthrie and Bryant, 2006 ; Maren and Chang, 2006 ; Myers and Davis, 2002).”
BackgroundInfluentialGenerating new neurons to circumvent your fears: the role of IGF signaling
Agís‐Balboa, R. C., & Fischer, A. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1316-2 · Cited by 41 · see citing works
Klavir, O., Genud-Gabai, R., & Paz, R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6481-11.2012 · Cited by 42 · see citing works
“…Bouton, 1993; Monfils et al., 2009), and here, we chose to use extinction that immediately follows acquisition, because several studies have observed significant recovery in this protocol (Rescorla, 2004; Maren and Chang, 2006; Alvarez et al., 2007; Schiller et al., 2008; Woods and Bouton, 2008).”
BackgroundMethodModulating reconsolidation and extinction to regulate drug reward memory
Liu, J., Tian, J., & Li, J. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14072 · Cited by 38 · see citing works
Associative Learning and Conditioning Theory
Laborda, M. A., McConnell, B. L., & Miller, R. R. (2011) · Cited by 37 · see citing works
The interhemispheric CA1 circuit governs rapid generalisation but not fear memory
Zhou, H., Xiong, G.-J., Jing, L., Song, N., Pu, D.-L., Tang, X., He, X.-B., Xu, F., Huang, J., Li, L., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-02315-4 · Cited by 37 · see citing works
Cohen, H., Matar, M., & Zohar, J. (2014) · ILAR Journal · doi:10.1093/ilar/ilu006 · Cited by 37 · see citing works
The exclusive induction of extinction is gated by BDNF
Kirtley, A., & Thomas, K. L. (2010) · Learning & Memory · doi:10.1101/lm.1877010 · Cited by 37 · see citing works
“…Alvarez et al. 2007; Schiller et al. 2008; Archbold et al. 2010), the interval between extinction and test (Bouton 1993, 2004; Quirk 2002), the level of fear behavior at extinction (Maren and Chang 2006), and the number and pattern of nonreinforced trails (Cain et al. 2003; Urcelay et al. 2009).”
BackgroundInvolvement of CRFR 1 in the Basolateral Amygdala in the Immediate Fear Extinction Deficit
Hollis, F., Sevelinges, Y., Grosse, J., Zanoletti, O., & Sandi, C. (2016) · eNeuro · doi:10.1523/eneuro.0084-16.2016 · Cited by 36 · see citing works
“Although pre-tone freezing levels for the immediate extinction groups were high, we found this behavior to be common in the literature when extinction training sessions were given shortly after fear conditioning (Maren and Chang, 2006; Chang and Maren, 2009; Chan et al., 2010; Goode et al., 2015).”
BackgroundResultInfluentialChudoba, R., & Dabrowska, J. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109461 · Cited by 37 · see citing works
Livneh, U., & Paz, R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0323-12.2012 · Cited by 34 · see citing works
“Several studies have recently shown that immediate extinction-training results in less extinction consolidation and higher levels of the original memory in the following day (Maren and Chang, 2006; Schiller et al., 2008; Woods and Bouton, 2008).”
BackgroundMikami, K., Kiyokawa, Y., Ishii, A., & Takeuchi, Y. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.104654 · Cited by 31 · see citing works
Unrelenting Fear Under Stress: Neural Circuits and Mechanisms for the Immediate Extinction Deficit
Maren, S. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.888461 · Cited by 33 · see citing works
“Similarly, limiting conditioned freezing before an immediate extinction session by reducing the number of conditioning trials or US intensity eliminates the IED (Maren and Chang, 2006; Jo and Choi, 2020).”
BackgroundMethodInfluentialTargeted Memory Reactivation During REM Sleep in Patients With Social Anxiety Disorder
Borghese, F., Henckaerts, P., Guy, F., Mayo, C., Delplanque, S., Schwartz, S., & Perogamvros, L. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.904704 · Cited by 33 · see citing works
“986] and no main effect of group [F(1,44) = 0.”
BackgroundAntov, M. I., Wölk, C., & Stockhorst, U. (2013) · Biological Psychology · doi:10.1016/j.biopsycho.2013.08.007 · Cited by 34 · see citing works
A Contemporary Behavioral Perspective on Extinction
Vurbic, D., & Bouton, M. E. (2014) · Wiley eBooks · doi:10.1002/9781118468135.ch3 · Cited by 33 · see citing works
Fear extinction in humans: Effects of acquisition–extinction delay and masked stimulus presentations
Golkar, A., & Öhman, A. (2012) · Biological Psychology · doi:10.1016/j.biopsycho.2012.07.007 · Cited by 33 · see citing works
Computational Models of Conditioning
Schmajuk, N. A. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511760402 · Cited by 32 · see citing works
Mendoza, J. A., Sanio, C., & Chaudhri, N. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.12.006 · Cited by 31 · see citing works
“However, the extinction of aversive conditioning is typically assessed using Pavlovian learning models (Garcia, Chang, & Maren, 2006; Maren & Chang, 2006; Milad & Quirk, 2002; Quirk & Mueller, 2008), whereas the extinction of appetitive conditioning is largely tested using instrumental conditioning…”
Zuccolo, P. F., & Hunziker, M. H. L. (2019) · Behavioural Processes · doi:10.1016/j.beproc.2019.01.011 · Cited by 30 · see citing works
Immediate extinction promotes the return of fear
Merz, C. J., Hamacher‐Dang, T. C., & Wolf, O. T. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.03.013 · Cited by 29 · see citing works
Nyctophobia: From Imagined to Realistic Fears of the Dark
Levos, J., & Zacchilli, T. L. (2015) · Psi Chi Journal of Psychological Research · doi:10.24839/2164-8204.jn20.2.102 · Cited by 28 · see citing works
Temporal factors in the extinction of fear in inbred mouse strains differing in extinction efficacy
MacPherson, K. P., Whittle, N., Camp, M., Gunduz‐Cinar, O., Singewald, N., & Holmes, A. (2013) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-3-13 · Cited by 28 · see citing works
“Some studies report a facilitatory effect of ‘immediate’ extinction [24], while others have observed impaired extinction [23,25,36].”
BackgroundMethodResultInfluentialThe role of context in the re-extinction of learned fear
Langton, J. M., & Richardson, R. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.06.008 · Cited by 28 · see citing works
Microglial activation and neuroinflammation in acute and chronic cognitive deficits in sepsis
Denver, P., & Cunningham, C. M. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110285 · Cited by 27 · see citing works
Sex differences in the immediate extinction deficit and renewal of extinguished fear in rats
Binette, A. N., Totty, M. S., & Maren, S. (2022) · PLoS ONE · doi:10.1371/journal.pone.0264797 · Cited by 26 · see citing works
“Because the IED has not previously been studied in Wistar rats, we used a no-extinction control similar to our previously published work in Long-Evans rats [26].”
BackgroundMethodExtinction: Behavioral Mechanisms and Their Implications ☆
Bouton, M. E. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21006-7 · Cited by 25 · see citing works
- Authors
- Maren, S., & Chang, C.-H.
- Affiliations
- University of Michigan (US)
- *Department of Psychology and
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2006-11-21
- Volume
- 103
- Issue
- 47
- Pages
- 18020-18025
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1693865
- OpenAlex
- W1991036243
- Cited by
- 184
- References
- 43
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 5 · 2023: 9 · 2022: 8 · 2021: 4 · 2020: 6 · 2019: 12 · 2018: 12 · 2017: 7 · 2016: 11 · 2015: 11 · 2014: 12 · 2013: 13 · 2012: 10
- FWCI
- 5.51
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Deep Blue (University of Michigan) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH065961)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- fear extinction, post-traumatic stress disorder, fear conditioning, early intervention, debriefing, extinction time, fear memory consolidation, war injuries
- MeSH terms
- Animals, Behavior, Conditioning, Classical, Extinction, Psychological, Fear, Humans, Male, Stress Disorders, Post-Traumatic, Rats, Long-Evans, Rats
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