Cited by 184Memory and Neural MechanismsPosttraumatic Stress Disorder ResearchMemory Processes and Influences

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Recent fear is resistant to extinction

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Maren, Stephen, Chang, Chun-hui·2006·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0608398103PMC PMC1693865

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Abstract

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 levels of BL fear prior to immediate extinction appear to be considerably lower in our study than in Maren and Chang (2006) and Chang and Maren (2009).”
BackgroundMethodResultInfluential
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Background
Using c-Jun to identify fear extinction learning-specific patterns of neural activity that are affected by single prolonged stress
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Urcelay, G. P. (2012) · Springer eBooks · doi:10.1007/978-1-4614-3342-2_4 · Cited by 26
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“…memory acquisition with extinction onset can significantly impact the effect of extinction on Genes, Brain and Behavior (2010) 9: 203–212 209 memory retention (Chang & Maren 2009; Lopez et al. 2008; Maren & Chang 2006; Myers et al. 2006; Rescorla 2004; Schiller et al. 2008; Woods & Bouton 2008).”
Background
Long-term maintenance of immediate or delayed extinction is determined by the extinction-test intervalPreprint
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“…suggest that the 3-s auditory CS (Fuzzo et al., 2015) or a shorter auditory CS, e.g. a 2-s CS (Quirk et al., 1995, 1997; Maren, 2000; Goosens et al., 2003; Maren and Chang, 2006), elicits the BNST-independent fear response even if the response is observed primarily in the absence of the CS.”
Background
Renewal of extinguished behavior in pigeons (Columba livia) does not require memory consolidation of acquisition or extinction in a free-operant appetitive conditioning paradigm
Packheiser, J., Güntürkün, O., & Pusch, R. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.111947 · Cited by 22
“[25] and in line with several other studies [33,49,50,52,53], a secondary inhibitory learning during extinction training does not seem to be based on a long “acquisition training – extinction training” interval.”
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“…of contextual fear in WT mice, which is in agreement with several previous studies where an IE after contextual and auditory fear conditioning showed null effect in extinguishing original fear memory (Maren and Chang, 2006; Schiller et al., 2008; Woods and Bouton, 2008; Archbold et al., 2010).”
BackgroundResult
Oscillatory and non‐oscillatory brain activity reflects fear expression in an immediate and delayed fear extinction task
Bierwirth, P., Antov, M. I., & Stockhorst, U. (2023) · Psychophysiology · doi:10.1111/psyp.14283 · Cited by 16
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“Indeed, spontaneous recovery is strongly inﬂuenced by the timing of the exposure to fear of the used extinction protocol and by reconsolidation processes (Maren and Chang, 2006; Ponnusamy et al., 2016).”
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Characterizing changes in glucocorticoid receptor internalization in the fear circuit in an animal model of post traumatic stress disorder
Moulton, E., Chamness, M., & Knox, D. (2018) · PLoS ONE · doi:10.1371/journal.pone.0205144 · Cited by 14
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“Heightened arousal/stress can lead to enhanced freezing during extinction testing (Maren and Chang 2006).”
Background
Behavioral and neural bases of extinction learning in Hermissenda
Cavallo, J. S., Hamilton, B. N., & Farley, J. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00277 · Cited by 13
“In other cases, unmodified fear extinction in rats produces similar behavioral and cellular reversal effects when administered within specific time intervals following learning acquisition (e.g., 1 h) (Mao et al., 2006; Myers et al., 2006, but see Maren and Chang, 2006; Woods and Bouton, 2008).”
BackgroundInfluential
Decreased level of histone acetylation in the infralimbic prefrontal cortex following immediate extinction may result in deficit of extinction memory
Singh, S. P., Siddiqui, S. A., Tripathy, S., Kumar, S., Saha, S., Ugale, R. R., Modi, D. R., & Prakash, A. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.06.004 · Cited by 14
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“Extinction training shortly after conditioning has been shown to reduce later fear recovery, compared to extinction after consolidation (Myers et al. , 2006 ) [but see (Maren and Chang , 2006 ; Schiller et al. , 2008a )].”
Background
Transcranial focused ultrasound stimulation in the infralimbic cortex facilitates extinction of conditioned fear in rats
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“Nonetheless, extant research has shown that intense emotion can not only interfere with extinction learning (Maren and Chang, 2006), but can even strengthen the relationship between the CS and CR (Campbell and Jaynes, 1966).”
Background
Peroxisome proliferator-activated receptor-α activation facilitates contextual fear extinction and modulates intrinsic excitability of dentate gyrus neurons
Guo, X., Liu, X., Wang, J., Lu, S., Yu, M., Zhang, Y., Sun, B., Huang, B., Lu, X., Li, X., et al. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02496-1 · Cited by 9
“Because the level of fear before extinction could influence the rate of subsequent extinction [50], we could not exclude the possibility that such high level of fear retrieval, rather than the protein itself, contributed to the impaired fear extinction exhibited in the PPARα deficient mice.”
Background
Potent attenuation of context fear by extinction training contiguous with acquisitionPreprint
Bernier, B. E., Lacagnina, A. F., & Drew, M. R. (2014) · Learning & Memory · doi:10.1101/lm.036673.114 · Cited by 9
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“…VITRO EXTINCTION FAILS TO PRODUCE REDUCTIONS IN SPIKE FREQUENCY Prior research has demonstrated that the interval between the end of learning acquisition and the beginning of extinction training can affect the outcome of extinction (Maren and Chang, 2006; Myers et al., 2006; Cavallo et al., 2014).”
Background
Individual variability in the recall of fear extinction is associated with phosphorylation of mitogen-activated protein kinase in the infralimbic cortex
Russo, A. S., Lee, J., & Parsons, R. G. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05195-2 · Cited by 7
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Groblewski, P. A., & Stafford, J. M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1413-10.2010 · Cited by 7
“However, the discrepant findings of these clinical studies are not surprising when considering the sensitivity of the IED phenomenon to procedural manipulations in preclinical animal models (Maren and Chang, 2006).”
Background
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LeCocq, M. R., Sun, S. B., & Chaudhri, N. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113686 · Cited by 6
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The immediate extinction deficit occurs in a nonemotional learning paradigmPreprint
Merz, C. J., & Wolf, O. T. (2019) · Learning & Memory · doi:10.1101/lm.048223.118 · Cited by 7
“This deficit has been shown in particular using fear conditioning paradigms in rodents (Maren and Chang 2006; Woods and Bouton 2008; Chang and Maren 2009, 2011; Chang et al. 2010; Kim et al. 2010; MacPherson et al. 2013; Stafford et al. 2013; Hollis et al. 2016; Giustino et al. 2017; Singh et al.…”
BackgroundMethodResultInfluential
Neural correlates of immediate versus delayed extinction when simultaneously varying the time of the test in humans
Kampa, M., Hermann, A., Stark, R. M., & Klucken, T. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad205 · Cited by 5
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“However, research indicates that the level of fear at the time of intervention is critical to the effectiveness of extinction [35].”
Background
Is it possible to modify fear memories in humans with extinction training within a single day?
Redondo, J., Rey, J. F., & Gonzalez-Gonzalez, D. (2018) · Psychological Research · doi:10.1007/s00426-018-1017-4 · Cited by 4
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“induce the IED (Maren and Chang, 2006) and we have demonstrated the IED using these parameters (Papagianni et al.”
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“Inaseriesofratstudies,increasedfreezingwasobservedasasignof elevated arousal before immediate extinction (Maren and Chang 2006).”
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“One of the hallmarks of trauma disorders is a resistance to extinction 71 .”
Robust renewal after extinction of remotely acquired Pavlovian conditioningPreprint
Charles, J. W., Moriarty, S. K., Fournier, D. I., Winterbauer, N. E., Cooper, E. A., & Todd, T. P. (2025) · Learning & Memory · doi:10.1101/lm.054103.125
“As noted, prior studies have also examined the timing of extinction relative to conditioning (Maren and Chang 2006; Myers et al. 2006; Woods and Bouton 2008; Chang and Maren 2009).”
Stress-Responsive Neuronal Ensembles and β-Adrenergic Signaling in the Basolateral Amygdala Modulate the Infralimbic Cortical Activity and Govern the Delayed Stress-Induced Fear Extinction Deficit
Juliano, V. A. L., Shigeo-de-Almeida, A., Cruz-Nascimento, T., Sampaio, L. L., Cruz, F. C., Novaes, L. S., & Munhoz, C. D. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.2392-24.2025
The effects of spaced versus massed extinction training on extinction retention of conditioned fear learning in male rats
LeVasseur, G. W., Cilley, T., Szewczuk, M., Perrine, S. A., & Norrholm, S. D. (2025) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2025.1727468
Why laterality matters in trauma: sinister aspects of memory and emotion
Choudhary, C. J. (2008) · Stirling Online Research Repository (University of Stirling)

Authors: Maren, S., & Chang, C.-H.
Affiliations: University of Michigan (US)
*Department of Psychology and
ORCID: Maren, Stephen
Chang, Chun-hui
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
DOI: 10.1073/pnas.0608398103
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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