Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones
Open accessAbstract
Exposure to restraint and brief intermittent tailshocks facilitates associative learning of the classical conditioned eyeblink response in male rats. Based on evidence of sex differences in learning and responses to stressful events, we investigated sexually dimorphic effects of a stressor of restraint and intermittent tailshock on classical eyeblink conditioning 24 h after stressor cessation. Our results indicate that exposure to the acute stressor had diametrically opposed effects on the rate of acquisition of the conditioned response in male vs. female rats. Exposure to the stressor facilitated acquisition of the conditioned response in males, whereas exposure to the same stressful event dramatically impaired acquisition in females. We further demonstrate that the stress-induced impairment in female conditioning is dependent on the presence of ovarian hormones. Conditioning of stressed sham-ovariectomized females was significantly impaired relative to the unstressed controls, whereas conditioning in stressed ovariectomized females was not impaired. We present additional evidence that estrogen mediates the stress-induced impairment in female acquisition. Females administered sesame oil vehicle and then stressed were significantly impaired relative to their unstressed controls, whereas females administered the estrogen antagonist tamoxifen prior to stress were not impaired. In summary, these results indicate that exposure to the same aversive event can induce opposite behavioral responses in males vs. females. These effects underscore sex differences in associative learning and emotional responding, and implicate estrogen in the underlying neuronal mechanism.
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In tests of acute stress or aversive conditioning, stress enhances learning in males and impairs it in females.
“in tests of acute stress or aversive conditioning, stress enhances learning in males and impairs it in females89, 90”
From Neurobiology of resilience (2012) · cites this paper as [89]
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- Authors
- Wood, G. E., & Shors, T. J.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1998-03-31
- Volume
- 95
- Issue
- 7
- Pages
- 4066-4071
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC19964
- OpenAlex
- W2162312524
- Cited by
- 359
- References
- 72
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 5 · 2022: 10 · 2021: 9 · 2020: 10 · 2019: 9 · 2018: 13 · 2017: 14 · 2016: 19 · 2015: 12 · 2014: 19 · 2013: 13 · 2012: 20
- FWCI
- 5.10
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- classical conditioning, eyeblink conditioning, acute stress, sex differences, restraint stress, ovarian hormones, estrogen, tamoxifen, ovariectomy, associative learning, emotional responses
- MeSH terms
- Animals, Estrogens, Female, Male, Ovariectomy, Ovary, Sex Factors, Stress, Physiological, Rats, Sprague-Dawley, Rats
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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.
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