Cited by 663Stress Responses and CortisolNeuroendocrine regulation and behaviorMemory and Neural Mechanisms

Environmental Enrichment Reverses the Effects of Maternal Separation on Stress Reactivity

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Francis, Darlene D., Diorio, Josie, Plotsky, Paul M., Meaney, Michael J.·2002·The Journal of Neuroscience

Abstract

Postnatal maternal separation increases hypothalamic corticotropin-releasing factor (CRF) gene expression and hypothalamic-pituitary-adrenal (HPA) and behavioral responses to stress. We report here that environmental enrichment during the peripubertal period completely reverses the effects of maternal separation on both HPA and behavioral responses to stress, with no effect on CRF mRNA expression. We conclude that environmental enrichment leads to a functional reversal of the effects of maternal separation through compensation for, rather than reversal of, the neural effects of early life adversity.

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Crossref · 10.1523/jneurosci.22-18-07840.2002

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  • Environmental enrichment has been shown to successfully reverse several ELS-induced impairments in behavior, including learning and memory, anxiety, depressive-like behavior, and attention.

    “Environmental enrichment has been shown to successfully reverse several ELS-induced impairments in behavior, including learning and memory, anxiety, depressive-like behavior, and attention (Francis et al., 2002; Cui et al., 2006; Vivinetto et al., 2013; Zubedat et al., 2015; Koe et al., 2016).”

    From Effects of Maternal Deprivation and Complex Housing on Rat Social Behavior in Adolescence and Adulthood (2018) · cites this paper as Francis et al., 2002

    The Results section (‘Enrichment reverses effects of MS on HPA function’; page not provided) reports that enrichment reversed maternal-separation effects on fearfulness and novelty-related behavioral inhibition in rats, supporting the anxiety-related part of the claim. It does not report reversal of impairments in learning and memory, depressive-like behavior, or attention. (LLM, conf=0.88)

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  • Studies in humans and animals models show that environmental enrichment can reduce or reverse some of the effects of deprivation, non-normative stimulation and even acute or chronic stress at the behavioural and neural levels.

    “Studies in humans and animals models show that environmental enrichment can reduce or reverse some of the effects of deprivation, non-normative stimulation and even acute or chronic stress [122,123] at the behavioural and neural levels [109,[124][125][126].”
  • Francis et al. (2002) demonstrated reversal of early maternal separation stress effects on HPA response (corticosterone) and learning/memory in rats receiving environmental enrichment.

    “For example, Francis, Diorio, Plotsky, and Meaney (2002) demonstrated reversal of the effect of early stress associated with maternal separation during the neonatal period on the HPA response to stress, as indicated by corticosterone levels, and on learning and memory among rats receiving environmental enrichment.”

    From Stress and the development of self-regulation in context (2010) · cites this paper as Francis, Diorio, Plotsky, and Meaney, 2002

  • In Francis et al. (2002), effects on corticosterone and behavior could not be attributed to expected neural-level changes in primary processes influencing stress reactivity.

    “Effects on corticosterone and behavior, however, could not be attributed to expected changes at the neural level in terms of primary processes that influence stress reactivity.”

    From Stress and the development of self-regulation in context (2010) · cites this paper as Francis et al., 2002

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Authors
Francis, D. D., Diorio, J., Plotsky, P. M., & Meaney, M. J.
Affiliations
  • Douglas Mental Health University Institute (CA)
  • Emory University (US)
Venue
The Journal of Neuroscience
Published
2002-09-15
Volume
22
Issue
18
Pages
7840-7843
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2144859742
Cited by
663
References
39
Citations by year
2026: 9 · 2025: 13 · 2024: 6 · 2023: 10 · 2022: 18 · 2021: 26 · 2020: 32 · 2019: 23 · 2018: 31 · 2017: 34 · 2016: 37 · 2015: 35 · 2014: 31 · 2013: 34 · 2012: 35
FWCI
9.08
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
National Institute of Mental Health
Topics
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
environmental enrichment, maternal separation, postpartum stress, stress reactivity, corticotropin-releasing factor, hypothalamic-pituitary-adrenal axis, childhood adversity, peripubertal period, behavioral stress response, neural compensation
MeSH terms
Animals, Appetitive Behavior, Behavior, Animal, Brain, Brain Chemistry, Corticotropin-Releasing Hormone, Exploratory Behavior, Handling, Psychological, Hypothalamo-Hypophyseal System, Maternal Deprivation, Pituitary-Adrenal System, Receptors, Glucocorticoid, RNA, Messenger, Social Environment, Stress, Physiological, In Situ Hybridization, Rats, Long-Evans, Rats

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