Stress-Enhanced Fear Learning in Rodents: A Systematic Review and Meta-Analysis of Fear-Learning Sensitization After Severe Stress

Background/Objectives: Stress-enhanced fear learning (SEFL) tests whether severe stress amplifies a later, separate fear-learning episode. Although SEFL studies commonly report increased freezing, its overall effect size, robustness, protocol-level variation, and translational interpretation have not been systematically quantified. This review evaluated SEFL as a focused paradigm of stress-induced fear-learning sensitization rather than as a comprehensive model of posttraumatic stress disorder (PTSD). Methods: Web of Science Core Collection, PubMed, Embase, and Scopus were searched from inception to June 2026. Eligible studies used an SEFL-related procedure, included independent stress-exposed and control groups, and reported extractable freezing outcomes during later fear testing. Hedges’ g values were pooled using restricted maximum-likelihood random-effects models. We also examined exploratory subgroup analyses, sensitivity analyses, and small-study-effect assessments. Results: Twenty-five studies comprising 49 comparisons were included. Stress-exposed animals showed higher freezing than controls during later fear testing (Hedges’ g = 1.71, 95% CI [1.38, 2.04], p < 0.001). Heterogeneity was substantial (I2 = 81.91%, τ2 = 1.07), and the 95% prediction interval crossed zero (−0.40 to 3.82), indicating that SEFL is not protocol-invariant. Exploratory subgroup analyses suggested protocol- and sample-level variation, particularly by species, strain, stress method, testing interval, and stress type. Contextual-fear-conditioning-only, study-level, non-footshock-exclusion, and leave-one-out sensitivity analyses supported the overall positive effect, although possible small-study effects should be considered when interpreting the pooled estimate. Conclusions: SEFL is best interpreted as a protocol-sensitive behavioral neuroscience paradigm for studying stress-enhanced later fear learning after severe stress rather than as a broad PTSD model. The current evidence supports a large average freezing-defined SEFL effect, but the marked heterogeneity and limited intervention-related evidence indicate that the paradigm should be interpreted with attention to protocol conditions and translational scope.

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Journal
Brain Sciences
Published
2026-06-30
DOI
https://doi.org/10.3390/brainsci16070691
Primary Topic
Memory and Neural Mechanisms
Type
article
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article

Stress-Enhanced Fear Learning in Rodents: A Systematic Review and Meta-Analysis of Fear-Learning Sensitization After Severe Stress

贺庚贤, Shou Qiu, S.J. Lin, Xiaoyan Zhu et al.
Brain Sciences
Memory and Neural Mechanisms
article

Stress-Enhanced Fear Learning in Rodents: A Systematic Review and Meta-Analysis of Fear-Learning Sensitization After Severe Stress

贺庚贤, Shou Qiu, S.J. Lin, Xiaoyan Zhu, Shanni Fu, Jing Pan, Jialu Feng, Xinying Zhang, R Liu, Zhijie Zhu
article en

Abstract

Background/Objectives: Stress-enhanced fear learning (SEFL) tests whether severe stress amplifies a later, separate fear-learning episode. Although SEFL studies commonly report increased freezing, its overall effect size, robustness, protocol-level variation, and translational interpretation have not been systematically quantified. This review evaluated SEFL as a focused paradigm of stress-induced fear-learning sensitization rather than as a comprehensive model of posttraumatic stress disorder (PTSD). Methods: Web of Science Core Collection, PubMed, Embase, and Scopus were searched from inception to June 2026. Eligible studies used an SEFL-related procedure, included independent stress-exposed and control groups, and reported extractable freezing outcomes during later fear testing. Hedges’ g values were pooled using restricted maximum-likelihood random-effects models. We also examined exploratory subgroup analyses, sensitivity analyses, and small-study-effect assessments. Results: Twenty-five studies comprising 49 comparisons were included. Stress-exposed animals showed higher freezing than controls during later fear testing (Hedges’ g = 1.71, 95% CI [1.38, 2.04], p < 0.001). Heterogeneity was substantial (I2 = 81.91%, τ2 = 1.07), and the 95% prediction interval crossed zero (−0.40 to 3.82), indicating that SEFL is not protocol-invariant. Exploratory subgroup analyses suggested protocol- and sample-level variation, particularly by species, strain, stress method, testing interval, and stress type. Contextual-fear-conditioning-only, study-level, non-footshock-exclusion, and leave-one-out sensitivity analyses supported the overall positive effect, although possible small-study effects should be considered when interpreting the pooled estimate. Conclusions: SEFL is best interpreted as a protocol-sensitive behavioral neuroscience paradigm for studying stress-enhanced later fear learning after severe stress rather than as a broad PTSD model. The current evidence supports a large average freezing-defined SEFL effect, but the marked heterogeneity and limited intervention-related evidence indicate that the paradigm should be interpreted with attention to protocol conditions and translational scope.

Brain SciencesVol. 16(7)
Wuhan University of Science and Technology (CN)
Reduced inequalities
Openalex Percentile: Top 7%
Memory and Neural Mechanisms
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