DNA Methylation in the Developing Hippocampus and Amygdala of Anxiety-Prone versus Risk-Taking Rats
Open accessAbstract
All organisms exhibit a wide range of emotional behaviors and interact with the environment in different ways. Some individuals may be more quiet and shy whereas others are more outgoing and adventurous. These temperamental and personality differences can predispose individuals to certain psychopathologies which may be influenced by genetic vulnerability and/or early life experiences. Rodent models can be used to recapitulate emotional reactivity differences, and these models can, in turn, be used to examine potential neurobiological underpinnings of these traits. The present study utilizes two strains of rats that were selectively bred for differences in novelty seeking. High Novelty-Responding (bHR) rats are very active in response to novelty, exhibit exaggerated risk-taking, aggression, impulsivity, and show increased behavioral response to cocaine. Low Novelty-Responding (bLR) rats show increased anxiety, depressive behavior and vulnerability to chronic stress. One way in which the bHR versus bLR behavioral phenotypes may differ is through epigenetic modification of DNA. DNA can be modified through processes such as acetylation or methylation to either enhance or subdue gene expression. This study examines putative differences in methylation levels in the hippocampus and amygdala of developing bHR-bLR rats. Previous research observed widespread gene expression differences in the bLR developing hippocampus, and the current study aims to begin to examine potential epigenetic factors that may contribute to those gene differences. The amygdala was chosen because it is involved in emotional processes, in part through its connections with the hippocampus. Therefore, the present study used in situ hybridization to assess the expression of DNA methyltransferase-1 (DNMT1) mRNA in the hippocampus, amygdala and several other brain areas of bHR and bLR pups at three developmental time points: postnatal days (P) 7, 14, and 21. We focused on the first 3 postnatal weeks, in part to parallel our early microarray gene expression work, and because this represents a critical period of brain development, which shapes individuals’ lifelong emotional and stress reactivity. We found significant differences in dentate gyrus and CA3 regions of the hippocampus at P7 with no differences seen at P14 or P21. Interestingly, we also found significant bHR-bLR DNMT1 differences at P7 within the lateral, basolateral and medial nuclei of the amygdala, with no difference at P14 and P21, suggesting that the first postnatal week is a critical period for DNA methylation during brain development.
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Low Novelty-Responding rats, bred to exhibit increased anxiety and depressive-like behaviors, displayed decreased mRNA levels of Dnmt1 in the dentate gyrus and CA3 of the hippocampus compared with their High Novelty-Responding counterparts.
“In a previous study, Low Novelty-Responding (bLR) rats, bred to exhibit increased anxiety and depressive-like behaviors, displayed decreased mRNA levels of Dnmt1 in the dentate gyrus (DG) and CA3 of the hippocampus, compared with their High Novelty-Responding (bHR) counterparts (Simmons et al., 2012).”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Simmons et al., 2012
The Results section (page unavailable) reports lower DNMT1 mRNA in bLR than bHR rats in CA3 and the upper blade of the dentate gyrus, but only at postnatal day 7. The claim omits that timing and describes the dentate gyrus as a whole, although the Results report no difference in its lower blade. A Discussion passage (page unavailable) also reverses the reported direction of the upper-blade difference, so the paper is internally inconsistent on that point. (LLM, conf=0.83)
Experimental — accuracy not yet measuredReduced Dnmt1 expression led to an increase in the anxiety phenotype in anxious bLR rats and Noguchi's prenatal Dnmt1 deletion mice.
“However, these findings contradict those of the study by Simmons et al. (2012) in anxious bLR rats as well as Noguchi’s prenatal Dnmt1 deletion mice, where reduced Dnmt1 expression led to an increase in the anxiety phenotype.”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Simmons et al., 2012
The Results (hippocampus and amygdala; page not provided) report lower DNMT1 mRNA in anxious bLR pups than in bHR pups in some regions, but higher expression in others. The Discussion says the behavioral implications require further study; it does not establish that reduced DNMT1 caused increased anxiety. The cited paper studies rats, not Noguchi’s prenatal Dnmt1 deletion mice. (LLM, conf=0.86)
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Self-citation
- Authors
- Simmons, R. K., Howard, J. L., Simpson, D. N., Akil, H., & Clinton, S. M.
- Affiliations
- University of Alabama at Birmingham (US)
- University of Michigan (US)
- Corresponding author
- Clinton, Sarah M.
- Venue
- Developmental Neuroscience
- Publisher
- S. Karger AG
- Published
- 2012
- Volume
- 34
- Issue
- 1
- Pages
- 58-67
- ISSN
- 0378-5866 (ISSN-L)
- 1421-9859
- PMC
- PMC3583346
- OpenAlex
- W1999108343
- Cited by
- 48
- References
- 35
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 1 · 2022: 3 · 2021: 8 · 2020: 3 · 2019: 5 · 2018: 1 · 2017: 2 · 2016: 3 · 2015: 2 · 2014: 8 · 2013: 8 · 2012: 1
- FWCI
- 2.44
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Developmental Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R00MH085859)
- National Institute on Drug Abuse (P01DA021633)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- DNA methylation, hippocampus, amygdala, novelty seeking, anxiety, risk-taking, DNMT1, brain development, postnatal development, epigenetics, emotional reactivity, dentate gyrus, CA3, amygdala nuclei, critical periods of development
- MeSH terms
- DNA (Cytosine-5-)-Methyltransferase 1, Aggression, Amygdala, Analysis of Variance, Animals, Anxiety, Brain, Depression, DNA (Cytosine-5-)-Methyltransferases, Exploratory Behavior, Female, Hippocampus, Male, Motor Activity, Time Factors, Rats, Sprague-Dawley, In Situ Hybridization, Dentate Gyrus, DNA Methylation, Rats
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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