Exercise Improves Cognitive Responses to Psychological Stress through Enhancement of Epigenetic Mechanisms and Gene Expression in the Dentate Gyrus
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BACKGROUND: We have shown previously that exercise benefits stress resistance and stress coping capabilities. Furthermore, we reported recently that epigenetic changes related to gene transcription are involved in memory formation of stressful events. In view of the enhanced coping capabilities in exercised subjects we investigated epigenetic, gene expression and behavioral changes in 4-weeks voluntarily exercised rats. METHODOLOGY/PRINCIPAL FINDINGS: Exercised and control rats coped differently when exposed to a novel environment. Whereas the control rats explored the new cage for the complete 30-min period, exercised animals only did so during the first 15 min after which they returned to sleeping or resting behavior. Both groups of animals showed similar behavioral responses in the initial forced swim session. When re-tested 24 h later however the exercised rats showed significantly more immobility behavior and less struggling and swimming. If rats were killed at 2 h after novelty or the initial swim test, i.e. at the peak of histone H3 phospho-acetylation and c-Fos induction, then the exercised rats showed a significantly higher number of dentate granule neurons expressing the histone modifications and immediate-early gene induction. CONCLUSIONS/SIGNIFICANCE: Thus, irrespective of the behavioral response in the novel cage or initial forced swim session, the impact of the event at the dentate gyrus level was greater in exercised rats than in control animals. Furthermore, in view of our concept that the neuronal response in the dentate gyrus after forced swimming is involved in memory formation of the stressful event, the observations in exercised rats of enhanced neuronal responses as well as higher immobility responses in the re-test are consistent with the reportedly improved cognitive performance in these animals. Thus, improved stress coping in exercised subjects seems to involve enhanced cognitive capabilities possibly resulting from distinct epigenetic mechanisms in dentate gyrus neurons.
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Rodents with higher levels of physical activity have been shown to display attenuated effects of psychological stressors on depression-like behaviour and cognition, enhanced neuroplasticity and an improved stress response.
“Rodents with higher levels of physical activity have been shown to display attenuated effects of psychological stressors on depression-like behaviour and cognition 36, enhanced neuroplasticity 37 and an improved stress response 38.”
From Resilience in mental health: linking psychological and neurobiological perspectives. (2013) · cites this paper as [36]
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- Authors
- Collins, A., Hill, L. E., Chandramohan, Y., Whitcomb, D., Droste, S. K., & Reul, J. M. H. M.
- Affiliations
- University of Bristol (GB)
- Corresponding author
- Reul, Johannes M. H. M.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2009-01-30
- Volume
- 4
- Issue
- 1
- Pages
- e4330
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2628725
- OpenAlex
- W2065907989
- Cited by
- 145
- References
- 54
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 5 · 2023: 4 · 2022: 4 · 2021: 5 · 2020: 8 · 2019: 6 · 2018: 6 · 2017: 10 · 2016: 10 · 2015: 12 · 2014: 13 · 2013: 12 · 2012: 15
- FWCI
- 5.71
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Explore Bristol Research (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UCL Discovery (University College London) (submittedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Funders
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- physical activity, psychological stress, stress coping, epigenetic mechanisms, dentate gyrus, histone H3 phosphorylation, histone acetylation, c-fos, immediate early genes, forced swim test, novelty exploration, stress memory, gene expression, hippocampus
- MeSH terms
- Acetylation, Animals, Behavior, Animal, Gene Expression Regulation, Histones, Male, Memory, Neurons, Physical Conditioning, Animal, Stress, Psychological, Gene Expression, Proto-Oncogene Proteins c-fos, Genes, fos, Rats, Sprague-Dawley, Dentate Gyrus, Epigenesis, Genetic, Rats
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