Predictable maternal separation confers adult stress resilience via the medial prefrontal cortex oxytocin signaling pathway in rats
Abstract
Early-life stress is normally thought of as a major risk for psychiatric disorders, but many researchers have revealed that adversity early in life may enhance stress resilience later in life. Few studies have been performed in rodents to address the possibility that exposure to early-life stress may enhance stress resilience, and the underlying neural mechanisms are far from being understood. Here, we established a "two-hit" stress model in rats by applying two different early-life stress paradigms: predictable and unpredictable maternal separation (MS). Predictable MS during the postnatal period promotes resilience to adult restraint stress, while unpredictable MS increases stress susceptibility. We demonstrate that structural and functional impairments occur in glutamatergic synapses in pyramidal neurons of the medial prefrontal cortex (mPFC) in rats with unpredictable MS but not in rats with predictable MS. Then, we used differentially expressed gene (DEG) analysis of RNA sequencing data from the adult male PFC to identify a hub gene that is responsible for stress resilience. Oxytocin, a peptide hormone, was the highest ranked differentially expressed gene of these altered genes. Predictable MS increases the expression of oxytocin in the mPFC compared to normal raised and unpredictable MS rats. Conditional knockout of the oxytocin receptor in the mPFC was sufficient to generate excitatory synaptic dysfunction and anxiety behavior in rats with predictable MS, whereas restoration of oxytocin receptor expression in the mPFC modified excitatory synaptic function and anxiety behavior in rats subjected to unpredictable MS. These findings were further supported by the demonstration that blocking oxytocinergic projections from the paraventricular nucleus of the hypothalamus (PVN) to the mPFC was sufficient to exacerbate anxiety behavior in rats exposed to predictable MS. Our findings provide direct evidence for the notion that predictable MS promotes stress resilience, while unpredictable MS increases stress susceptibility via mPFC oxytocin signaling in rats.
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Early life stress increased vulnerability to adult stress in rodents.
“ELS increased the vulnerability to adult stress in rodents208.”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [208]
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- Authors
- Shi, D.-D., Zhang, Y.-D., Ren, Y.-Y., Peng, S.-Y., Yuan, T.-F., & Wang, Z.
- Affiliations
- Shanghai Jiao Tong University (CN)
- Corresponding author
- Wang, Zhen
- Venue
- Molecular Psychiatry
- Published
- 2021-09-24
- Volume
- 26
- Issue
- 12
- Pages
- 7296-7307
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- OpenAlex
- W3199948820
- Cited by
- 63
- References
- 47
- Citations by year
- 2026: 11 · 2025: 10 · 2024: 15 · 2023: 13 · 2022: 11 · 2021: 2 · 2012: 1
- FWCI
- 10.06
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Molecular Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Shanghai Municipal Education Commission (2021-01-07-00-02-E0086)
- Science and Technology Commission of Shanghai Municipality (20XD1423100)
- Shanghai Municipal Health Bureau (2019ZB0201)
- National Natural Science Foundation of China (31900730)
- Shanghai Science and Technology Development Foundation (19YF14420000)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- maternal separation, early life stress, stress resilience, stress vulnerability, medial prefrontal cortex, oxytocin signaling, oxytocin receptor, glutamatergic synapses, anxiety-like behavior, paraventricular nucleus, restraint stress, hub genes
- MeSH terms
- Animals, Anxiety, Male, Maternal Deprivation, Oxytocin, Stress, Psychological, Signal Transduction, Prefrontal Cortex, Rats
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