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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Avitsur, R., & Sheridan, J. F. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.05.056 · Cited by 44
“Since neonatal stress altered HPA reactivity (Suchecki and Tufik, 1997; van Oers et al., 1998; Plotsky and Meaney, 1993; Schmidt et al., 2003), it was hypothesized that MSP would also affect host response to an infectious challenge (Avitsur et al.”
BackgroundMethodInfluential
From Risky Behavior to Health Risk: Continuity Across Two Generations
Genna, N. M. D., Stack, D. M., Serbin, L. A., Ledingham, J. E., & Schwartzman, A. E. (2006) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/00004703-200608000-00004 · Cited by 44
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Effects of neonatal inhalation exposure to ultrafine carbon particles on pathology and behavioral outcomes in C57BL/6J mice
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Neurobiology of Bipolar Illness: Implications for Future Study and Therapeutics
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Effects of early rearing conditions on cognitive performance in prepubescent male and female rats
Frankola, K. A., Flora, A. L., Torres, A. K., Grissom, E. M., Overstreet, S., & Dohanich, G. P. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.04.005 · Cited by 47
“…Denenberg, 1964; Francis, Dioro, Plotsky, & Meaney, 2002; Huot, Gonzalez, Ladd, Thrivikraman, & Plotsky, 2004; Ladd, Thrivikraman, Huot, & Plotsky, 2005; Meaney, Aitken, Viau, Sharma, & Sarrieau, 1989; Meerlo, Horvath, Nagy, Bohus, & Koolhaas, 1999; Plotsky & Meaney, 1993; Vallee et al., 1997).”
Suicide attempters: biological stressmarkers and adverse life events
Sunnqvist, C., Westrin, Å., & Träskman‐Bendz, L. (2008) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-008-0819-6 · Cited by 45
Cross-fostering does not alter the neurochemistry or behavior of spontaneously hypertensive rats
Howells, F. M., Bindewald, L., & Russell, V. A. (2009) · Behavioral and Brain Functions · doi:10.1186/1744-9081-5-24 · Cited by 46
“Cross-fostering and maternal separation are widely used to study the influence of early postnatal environment on rat pups [35-39].”
Quality of maternal and paternal care predicts later stress reactivity in the cooperatively-breeding marmoset (Callithrix geoffroyi)
Birnie, A. K., Taylor, J. H., Cavanaugh, J., & French, J. A. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.08.011 · Cited by 43
“Short periods of maternal separation, however, can elicit higher rates of licking and grooming from rat mothers, which appears to blunt rises in these HPA products (Plotsky and Meaney, 1993).”
Background
Maternal separation modulates short-term behavioral and physiological indices of the stress response
Litvin, Y., Tovote, P., Pentkowski, N. S., Zeyda, T., King, L. B., Vasconcellos, A., Dunlap, C., Spiess, J., Blanchard, D. C., & Blanchard, R. J. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.010 · Cited by 43
“, 2008a), enhanced expression of corticotropin-releasing factor (CRF) in the paraventricular nucleus of the hypothalamus and the hippocampus, and reduced binding to and down-regulation of hippocampal type2 glucocorticoid receptors (GR) (Plotsky and Meaney, 1993; Avishai-Eliner et al., 2001b; Ladd et al., 2004).”
Biomarkers for Psychiatric Disorders
Turck, C. W. (2009) · Springer eBooks · doi:10.1007/978-0-387-79251-4 · Cited by 42
Endocrinologic and Psychologic Evaluation of 21-Hydroxylase Deficiency Carriers and Matched Normal Subjects: Evidence for Physical and/or Psychologic Vulnerability to Stress
Charmandari, E., Merke, D. P., Negro, P., Keil, M. F., Martinez, P. E., Haim, A., Gold, P. W., & Chrousos, G. P. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031322 · Cited by 43
Early weaning decreases play‐fighting behavior during the postweaning developmental period of wistar rats
Shimozuru, M., Kodama, Y., Iwasa, T., Kikusui, T., Takeuchi, Y., & Mori, Y. (2007) · Developmental Psychobiology · doi:10.1002/dev.20202 · Cited by 44
Early life stress sensitizes the renal and systemic sympathetic system in rats
Loria, A. S., Brands, M. W., Pollock, D. M., & Pollock, J. S. (2013) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00008.2013 · Cited by 43
Effects of rearing condition on HPA axis response to fluoxetine and desipramine treatment over repeated social separations in young rhesus monkeys
Clarke, A. S., Kraemer, G. W., & Kupfer, D. J. (1998) · Psychiatry Research · doi:10.1016/s0165-1781(98)00032-8 · Cited by 43
Maternal and environmental factors influence the hypothalamic-pituitary-adrenal axis response to corticotropin-releasing hormone infusion in offspring of mothers with or without mood disorders
RONSAVILLE, D. S., MUNICCHI, G., LANEY, C., CIZZA, G., MEYER, S. E., HAIM, A., RADKE-YARROW, M., CHROUSOS, G., GOLD, P. W., & MARTINEZ, P. E. (2006) · Development and Psychopathology · doi:10.1017/s095457940606010x · Cited by 42
Fasting-induced increases of arcuate NPY mRNA and plasma corticosterone are blunted in the rat experienced neonatal maternal separation
Kim, H. J., Lee, J. H., Choi, S. H., Lee, Y. S., & Jahng, J. W. (2005) · Neuropeptides · doi:10.1016/j.npep.2005.09.003 · Cited by 42
Effects of early weaning on the circadian rhythm and behavioral satiety sequence in rats
Oliveira, L. D. S., da Silva, L. P., da Silva, A. I., Magalhães, C. P., de Souza, S. L., & Manhães‐de‐Castro, R. (2010) · Behavioural Processes · doi:10.1016/j.beproc.2010.10.001 · Cited by 43
Early life stress downregulates endothelin receptor expression and enhances acute stress-mediated blood pressure responses in adult rats.
Loria, A., D’Angelo, G., Pollock, D., & Pollock, J. (2010) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00333.2009 · Cited by 40
“Rat pups separated from their mothers daily for a prolonged period (up to 3 h) during the hyporesponsive period display abnormal anxiety-related behavior (41, 43), as well as increased acute behavioral and endocrine stress reactivity as adults (4, 27, 38, 44).”
Background
Neonatal maternal separation stress elicits lasting DNA methylation changes in the hippocampus of stress‐reactive Wistar Kyoto rats
McCoy, C. R., Rana, S., Stringfellow, S. A., Day, J. J., Wyss, J. M., Clinton, S. M., & Kerman, I. A. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13404 · Cited by 46
Effect of the early social environment on behavioural and genomic responses to a social challenge in a cooperatively breeding vertebrate
Nyman, C., Fischer, S., Aubin‐Horth, N., & Taborsky, B. (2017) · Molecular Ecology · doi:10.1111/mec.14113 · Cited by 43
“…in molecular responses to a behavioural challenge between individuals that faced different early social environments have so far been only demonstrated in laboratory strains of rodents (measured at the mRNA or protein level, Plotsky & Meaney 1993; Wigger & Neumann 1999; Ago et al. 2013).”
Background
Combined dexamethasone/corticotropin-releasing factor test in chronic fatigue syndrome
Eede, F. V. D., Moorkens, G. H., Hulstijn, W., Houdenhove, B. V., Cosyns, P. R., Sabbe, B., & Claes, S. J. (2007) · Psychological Medicine · doi:10.1017/s0033291707001444 · Cited by 43
“Pregnancy, a lifetime history of organic brain disease, current medical condition or drugs that might influence neuroendocrine testing (with the exception of psychotropic drugs and oral contraceptives) were exclusion criteria.”
Background
Persistent behavioral and autonomic supersensitivity to stress following prenatal stress exposure in rats
Rimondini, R., Ågren, G., Börjesson, S., Sommer, W. H., & Heilig, M. A. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00273-5 · Cited by 42
Impact of childhood trauma on hypothalamus-pituitary-adrenal axis activity in alcohol-dependent patients
Schäfer, I., Teske, L., Schulze-Thüsing, J., Homann, K., Reimer, J., Haasen, C., Hissbach, J., & Wiedemann, K. (2010) · European Addiction Research · doi:10.1159/000294362 · Cited by 41
“Studies in rodents and non-human primates reported that early life stress, such as maternal separation, was related to increased plasma glucocorticoid levels and adrenocorticotropin-releasing hormone (ACTH) and to increased HPA axis reactivity to subsequent stressors in adulthood [”
Background
Early rearing experience is related to altered aggression and vasopressin production following chronic social isolation in the prairie vole
Perkeybile, A. M., & Bales, K. L. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.01.025 · Cited by 40
“Conversely, long-term maternal separation results in increased anxiety-like behavior and decreased maternal behavior [5], increased depressivelike behavior [6], and an increased HPA response to a stressor [4, 6, 7].”
Background
Expression of Glucocorticoid Receptor and Early Growth Response Gene 1 during Postnatal Development of Two Inbred Strains of Mice Exposed to Early Life Stress
Navailles, S., Zimnisky, R. M., & Schmauss, C. (2010) · Developmental Neuroscience · doi:10.1159/000293989 · Cited by 44
Early maternal separation followed by later stressors leads to dysregulation of the HPA-axis and increases in hippocampal NGF and NT-3 levels in a rat model
Faure, J., Uys, J. D. K., Marais, L., Stein, D. J., & Daniels, W. M. U. (2006) · Metabolic Brain Disease · doi:10.1007/s11011-006-9013-6 · Cited by 41
Pathway to neural resilience: Self‐esteem buffers against deleterious effects of poverty on the hippocampus
Wang, Y., Zhang, L., Kong, X., Hong, Y., Cheon, B. K., & Liu, J. (2016) · Human Brain Mapping · doi:10.1002/hbm.23273 · Cited by 47
“Because the hippocampus contains a high density of glucocorticoids receptors, it appears particularly susceptible to the deleterious effect of low SSS [Avishai-Eliner et al., 2001; McEwen, 2012; Plotsky and Meaney, 1993].”
Background
Neuropeptides in Anxiety Modulation
Landgraf, R. (2005) · Handbook of experimental pharmacology · doi:10.1007/3-540-28082-0_12 · Cited by 41
Effects of brief and long maternal separations on the HPA axis activity and the performance of rats on context and tone fear conditioning
Guijarro, J. Z., Tiba, P. A., Ferreira, T. L., Kawakami, S. E., Oliveira, M. G. M., & Suchecki, D. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.06.020 · Cited by 41
Immediate and long-lasting effects of chronic stress in the prepubertal age on the startle reflex
Maslova, L. N., Bulygina, V. V., & Popova, N. K. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00648-5 · Cited by 41
The Brown Norway rat displays enhanced stress-induced ACTH reactivity at day 18 after 24-h maternal deprivation at day 3
Workel, J. O., Oitzl, M. S., Ledeboer, A., & de Kloet, E. R. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)81796-8 · Cited by 41
Development of Individual Differences in Behavioral and Endocrine Responses to Stress: Role of the Postnatal Environment
Caldji, C., Liu, D., Sharma, S., Diorio, J. C., Francis, D. D., Meaney, M. J., & Plotsky, P. M. (2001) · Comprehensive physiology · doi:10.1002/cphy.cp070413 · Cited by 41
Self-citation
Allopregnanolone modulation of HPA axis function in the adult rat
Biggio, G., Pisu, M. G., Biggio, F., & Serra, M. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3521-6 · Cited by 40
“In fact, repeated and long-lasting maternal separation (MS) appears to result in increased stress reactivity during adulthood, accompanied by augmented fluctuations in the secretion of CRH, ACTH, and corticosterone (Plotsky and Meane 1993; Macrì et al. 2011).”
Background
Using cross-species comparisons and a neurobiological framework to understand early social deprivation effects on behavioral development
Brett, Z. H., Humphreys, K. L., Fleming, A. S., Kraemer, G. W., & Drury, S. S. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000036 · Cited by 43
“Although substantially more research is needed to define the underlying mechanisms (see Plotsky & Meaney, 1993; Plotsky, Thrivikraman, & Meaney, 1993; Viau, Sharma, Plotsky, & Meaney, 1993), NHP findings related to the effect of PR on the HPA axis are consistent with those from rodent (Plotsky &…”
BackgroundResult
Treatment with tianeptine induces antidepressive-like effects and alters the neurotrophin levels, mitochondrial respiratory chain and cycle Krebs enzymes in the brain of maternally deprived adult rats
Della, F. P., Abelaira, H. M., Réus, G. Z., dos Santos, M. A. B., Tomaz, D. B., Antunes, A. R., Scaini, G., Morais, M. O. D. S., STRECK, E. L., & Quevedo, J. (2013) · Metabolic Brain Disease · doi:10.1007/s11011-012-9375-x · Cited by 41

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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