Cited by 1,638Stress Responses and CortisolNeuroendocrine regulation and behaviorNeuropeptides and Animal Physiology

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Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats

Plotsky, Paul M., Meaney, Michael J.·1993·Molecular Brain Research

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Abstract

Rat pups 2-14 days of age were exposed daily to handling (15 min of separation from mother and home cage), maternal separation (MS; 180 min of comparable separation), or were left entirely undisturbed (non-handled; NH). As adults, MS rats showed increased hypothalamic corticotropin-releasing factor (CRF) mRNA levels compared with NH rats, while CRF mRNA levels in H rats were significantly lower than either MS or NH animals. Hypothalamic CRF content under basal conditions followed exactly the same pattern. A 20-min period of restraint stress produced significant CRF depletion in all groups, although the percentage of depletion was significantly lower in H animals compared with either MS or NH animals. Restraint stress produced significantly higher increases in plasma corticosterone in MS and NH animals than in H animals. These data reflect the importance of early environmental factors in regulating the development of the hypothalamic CRF system and the responsiveness of the hypothalamic-pituitary-adrenal axis to stress.

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A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,515
The Neuroendocrinology of Stress and Aging: The Glucocorticoid Cascade Hypothesis
Sapolsky, R. M., Krey, L. C., & McEwen, B. S. (1986) · Science of Aging Knowledge Environment · doi:10.1126/sageke.2002.38.cp21 · Cited by 2,343
Effect of Neonatal Handling on Age-Related Impairments Associated with the Hippocampus
Meaney, M. J., Aitken, D. H., van Berkel, C., Bhatnagar, S., & Sapolsky, R. M. (1988) · Science · doi:10.1126/science.3340858 · Cited by 1,074
Self-citation
Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response.
Sapolsky, R. M., Krey, L. C., & McEwen, B. S. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.19.6174 · Cited by 758
Infantile Experience and Resistance to Physiological Stress
Levine, S. (1957) · Science · doi:10.1126/science.126.3270.405 · Cited by 659
Physiological and behavioral effects of infantile stimulation
Levine, S., Haltmeyer, G. C., Karas, G. G., & Denenberg, V. H. (1967) · Physiology & Behavior · doi:10.1016/0031-9384(67)90011-x · Cited by 553
Surgical Disconnection of the Medial Basal Hypothalamus and Pituitary Function in the Rhesus Monkey. I. Gonadotropin Secretion1,2
Krey, L. C., Butler, W. R., & Knobil, E. (1975) · Endocrinology · doi:10.1210/endo-96-5-1073 · Cited by 473
Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pituitary-adrenocortical axis
Herman, J. P., Schafer, M., Young, E. A., Thompson, R. C., DOUGLASS, J. O., Akil, H., & Watson, S. J. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-09-03072.1989 · Cited by 467
Neonatal Handling Alters Adrenocortical Negative Feedback Sensitivity and Hippocampal Type II Glucocorticoid Receptor Binding in the Rat
Meaney, M. J., Aitken, D. H., Viau, V., Sharma, S., & Sarrieau, A. (2008) · Neuroendocrinology · doi:10.1159/000125287 · Cited by 457
Self-citation

Show all 34 references

Research works printed but not linked: 1

Shanks, 1992, The effects of endotoxin exposure on hypothalamic-pituitary-adrenal activity in rat pups, Soc. Neurosci. Abst., 18

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Background
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Anacker, C., O'Donnell, K. J., & Meaney, M. J. (2014) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2014.16.3/canacker · Cited by 237
Self-citation
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Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats
Macrı̀, S., Mason, G. J., & Würbel, H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03541.x · Cited by 245
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Depression during pregnancy and the puerperium.
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Background
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Self-citation

Authors: Plotsky, P. M., & Meaney, M. J.
Affiliations: Salk Institute for Biological Studies (US)
Douglas Mental Health University Institute (CA)
Corresponding author: Meaney, Michael J.
ORCID: Meaney, Michael J.
Venue: Molecular Brain Research
Publisher: Elsevier BV
Published: 1993-05
Volume: 18
Issue: 3
Pages: 195-200
ISSN: 0169-328X (ISSN-L)
DOI: 10.1016/0169-328x(93)90189-v
OpenAlex: W1984427714
Cited by: 1,638
References: 34
Citations by year: 2026: 26 · 2025: 12 · 2024: 18 · 2023: 21 · 2022: 32 · 2021: 36 · 2020: 40 · 2019: 40 · 2018: 49 · 2017: 47 · 2016: 61 · 2015: 49 · 2014: 83 · 2013: 65 · 2012: 75
FWCI: 7.02
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Molecular Brain Research (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01mh045216-05)
National Institute of Mental Health (MH45216)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords: corticotropin-releasing factor, hypothalamus, maternal separation, early life stress, handling, restraint stress, hypothalamic-pituitary-adrenal axis, corticosterone, median eminence, stress responsiveness, developmental programming
MeSH terms: Actins, Aging, Animals, Animals, Newborn, Corticosterone, Corticotropin-Releasing Hormone, Female, Handling, Psychological, Hypothalamus, Maternal Behavior, Median Eminence, Reference Values, Restraint, Physical, RNA, Messenger, Social Isolation, Stress, Psychological, Blotting, Northern, Rats

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Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats

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