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

The DOI matches its Crossref record; 33 of the 34 references it cites were found in a registry or an index.

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

Open this paper in CoChat — free account

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.

Integrity signals

Registry

Crossref · 10.1016/0169-328x(93)90189-v

Cites

33 of 33 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

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

Sorted by citations

Items 901–1,000 of 1,008

Long-Lasting Changes in Morphine-Induced Locomotor Sensitization and Tolerance in Long-Evans Mother Rats as a Result of Periodic Postpartum Separation from the Litter: A Novel Model of Increased Vulnerability to Drug Abuse?
Kalinichev, M., Easterling, K. W., & Holtzman, S. G. (2002) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300068 · Cited by 31
Impact of early adverse experience on complexity of adult-generated neurons
Leslie, A. T., Akers, K. G., Krakowski, A. D., Stone, S. S. D., Sakaguchi, M., Arruda-Carvalho, M., & Frankland, P. W. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.38 · Cited by 30
Altered locomotor and stereotyped responses to acute methamphetamine in adolescent, maternally separated rats
Pritchard, L. M., Hensleigh, E., & Lynch, S. W. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2679-z · Cited by 32
“As adults, MS rats exhibit exaggerated neuroendocrine stress responses (Plotsky and Meaney 1993) and increased anxiety-like behavior (Daniels et al.”
Female HPA axis displays heightened sensitivity to pre-pubertal stress
Brydges, N. M., Best, C., & Thomas, K. L. (2019) · Stress · doi:10.1080/10253890.2019.1658738 · Cited by 30
“…the stress) (Aisa, Tordera, Lasheras, Del Rio, & Ramirez, 2008; Brunton & Russell, 2010; Kapoor, Dunn, Kostaki, Andrews, & Matthews, 2006; Levitt, Lindsay, Holmes, & Seckl, 1996; Maccari et al., 1995; Plotsky & Meaney, 1993; van Bodegom, Homberg, & Henckens, 2017; Welberg, Seckl, & Holmes, 2001).”
Neonatal stress modulates sickness behavior: role for proinflammatory cytokines.
Avitsur, R., Maayan, R., & Weizman, A. (2013) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2013.02.009 · Cited by 29
“…to alter multiple physiological systems, consequently affecting early development of neuroendocrine and neuroimmune systems (Ackerman et al., 1988; Plotsky and Meaney, 1993; Neveu et al., 1994; Suchecki and Tufik, 1997; Francis and Meaney, 1999; Gutman and Nemeroff, 2002; Teunis et al., 2002; Coe…”
Background
Cholecystokinin tetrapeptide effects on HPA axis function and elevated plus maze behaviour in maternally separated and handled rats
Greisen, M. H., Bolwig, T. G., & Wörtwein, G. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.02.006 · Cited by 30
Maternal separation increases GABAA receptor-mediated modulation of norepinephrine release in the hippocampus of a rat model of ADHD, the spontaneously hypertensive rat
Sterley, T.-L., Howells, F. M., & Russell, V. A. (2012) · Brain Research · doi:10.1016/j.brainres.2012.12.029 · Cited by 32
“…and prolonged physiological responses to stress later in life, and to cause an increase in anxiety and depressive-like behaviour later in life (Plotsky and Meaney, 1993; McIntosh et al., 1999; Wigger and Neumann, 1999; Caldji et al., 2000; Huot et al., 2001; Ladd et al., 2004; Aisa et al.,…”
The arcuate NPY, POMC, and CART expressions responding to food deprivation are exaggerated in young female rats that experienced neonatal maternal separation
Yoo, S. B., Ryu, V., Park, E. Y., Kim, B.-T., Kang, D. W., Lee, J.-H., & Jahng, J. W. (2011) · Neuropeptides · doi:10.1016/j.npep.2011.07.005 · Cited by 30
Neonatal factors influence adult stroke outcome
Craft, T. K. S., Zhang, N., Glasper, E. R., Hurn, P. D., & DeVries, A. C. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.01.002 · Cited by 30
“…to stressors, decreased neurogenesis, and a greater age-related decline in cognitive function compared to controls (Ladd et al., 2004; Lemaire et al., 2000; Maccari et al., 2003; Mirescu et al., 2004; Parfitt et al., 2004; Plotsky & Meaney, 1993; Romeo et al., 2003; Yamazaki et al., 2005).”
Background
Development by environment interactions controlling tryptophan hydroxylase expression
Hale, M. W., Shekhar, A., & Lowry, C. A. (2011) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2011.05.002 · Cited by 32
“…HPA axis responses to stress and increased anxiety-state, anhedonia, increased ethanol preference and impairment of sexual behavior in males during adulthood (Huot et al., 2001; Kalinichev et al., 2002; Ladd et al., 1996; Plotsky and Meaney, 1993; Rhees et al., 2001; Wigger and Neumann, 1999).”
Early life stress and the propensity to develop addictive behaviors
Walters, H. M., & Kosten, T. A. (2019) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2019.06.004 · Cited by 33
“ternal care disruptions have been described since Harlow’s studies in monkeys (Harlow, 1958) and Levine, Denenberg, and others’ studies in rats (Levine et al., 1956; Levine, 2001; Denenberg, 1964; Plotsky and Meaney, 1993).”
BackgroundMethod
Artificial rearing alters the response of rats to natural and drug-mediated rewards
Lomanowska, A. M., Rana, S. A., McCutcheon, D., Parker, L. A., & Wainwright, P. E. (2006) · Developmental Psychobiology · doi:10.1002/dev.20139 · Cited by 31
Prenatal Alcohol Exposure Alters the Hypothalamic‐Pituitary‐Adrenal Axis Response of Immature Offspring to Interleukin‐1: Is Nitric Oxide Involved?
Lee, S., & RIVIER, C. L. (1994) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1994.tb00112.x · Cited by 30
The molecular neurobiology of stress – evidence from genetic and epigenetic models
Steckler, T. (2001) · Behavioural Pharmacology · doi:10.1097/00008877-200111000-00002 · Cited by 30
Maternal separation as early-life stress: Mechanisms of neuropsychiatric disorders and inspiration for neonatal care
Zhang, Y., Wang, S., & Hei, M. (2024) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2024.111058 · Cited by 36
“Many studies have investigated alterations in the HPA axis in MS. Plotsky and colleagues reported that hypothalamic CRF mRNA levels were greater in MS adult rats than in nonhandle rats (Plotsky and Meaney, 1993).”
Background
Sexually dimorphic long-term effects of an early life experience on AMPA receptor subunit expression in rat brain
Katsouli, S., Stamatakis, A., Giompres, P., Kouvelas, E. D., Stylianopoulou, F., & Mitsacos, A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.10.073 · Cited by 36
“…Meaney et al., 1996; Wilber et al., 2008) as well as reduced corticotropin-releasing hormone (CRH), adrenocorticotropin (ACTH) and corticosterone release following exposure to stressful stimuli (Plotsky and Meaney, 1993; Bhatnagar and Meaney, 1995; Vallee et al., 1996, 1997; Liu et al., 1997).”
BackgroundInfluential
Preimplantation maternal stress impairs embryo development by inducing oviductal apoptosis with activation of the Fas system
Zheng, L.-L., Tan, X.-W., Cui, X.-Z., Yuan, H.-J., Li, H., Jiao, G.-Z., Ji, C.-L., & Tan, J.-H. (2016) · Molecular Human Reproduction · doi:10.1093/molehr/gaw052 · Cited by 29
Early-life stress induces genome-wide sex-dependent miRNA expression and correlation across limbic brain areas in rats
McKibben, L. A., & Dwivedi, Y. (2021) · Epigenomics · doi:10.2217/epi-2021-0037 · Cited by 31
Living long and ageing well: is epigenomics the missing link between nature and nurture?
The ACUME2 Project, Rea, I. M., Dellett, M., & Mills, K. (2015) · Biogerontology · doi:10.1007/s10522-015-9589-5 · Cited by 29
“Early work in animal studies has been highly important in demonstrating the mechanisms whereby that poor maternal care causes dysregulation of the hypopituitary axis (HPA) through altered transcription of the glucocorticoid receptor gene (Plotsky and Meaney 1993; Meaney 2001).”
Background
Early Paternal Deprivation Alters Levels of Hippocampal Brain-Derived Neurotrophic Factor and Glucocorticoid Receptor and Serum Corticosterone and Adrenocorticotropin in a Sex-Specific Way in Socially Monogamous Mandarin Voles
Wu, R., Song, Z., Wang, S., Shui, L., Tai, F., Qiao, X., & He, F. (2014) · Neuroendocrinology · doi:10.1159/000366441 · Cited by 29
Motherless rats show deficits in maternal behavior towards fostered pups
Palombo, D. J., Nowoslawski, M., & Fleming, A. S. (2010) · Developmental Psychobiology · doi:10.1002/dev.20422 · Cited by 30
“…is a substantial body of literature that demonstrates that the maternal environment alters neuroendocrine functioning and physiology, including regulation of the hypothalamic–pituitary–adrenal (HPA) axis (e.g., Burton et al., 2007; Francis, Diorio, Plotsky, & Meaney, 2002; Plotsky & Meaney, 1993).”
Background
Early life stress causes FG-7142-induced corticolimbic dysfunction in adulthood
Stevenson, C. W., Marsden, C. A., & Mason, R. (2008) · Brain Research · doi:10.1016/j.brainres.2007.11.062 · Cited by 31
Increased Activation of Synapsin 1 and Mitogen‐Activated Protein Kinases/Extracellular Signal‐Regulated Kinase in the Amygdala of Maternal Separation Rats
Park, H., Kim, S., Kang, W. S., Chung, J., & Kim, J. (2013) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12202 · Cited by 29
Plasma Hormones Facilitated the Hypermotility of the Colon in a Chronic Stress Rat Model
Liang, C., Luo, H., Liu, Y., Cao, J., & Xia, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031774 · Cited by 29
Crossroads of corticotropin releasing hormone, corticosteroids and monoamines
van Praag, H. M. (2002) · Neurotoxicity Research · doi:10.1080/1029842021000022115 · Cited by 29
Adolescent Psychiatry
Merrick, J., & Sher, L. (2013) · De Gruyter eBooks · doi:10.1515/9783110316612 · Cited by 29
Critical Evaluation of Animal Models of Gastrointestinal Disorders
Johnson, A. C., & Meerveld, B. G. (2017) · Handbook of experimental pharmacology · doi:10.1007/164_2016_120 · Cited by 29
Inflammation-Susceptible Lewis Rats Show Less Sensitivity Than Resistant Fischer Rats in the Formalin Inflammatory Pain Test and With Repeated Thermal Testing
Lariviere, W. R., Sattar, A., & Melzack, R. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00608.2005 · Cited by 29
Mother–infant separation leads to hypoactive behavior in adolescent Holtzman rats
Spivey, J. M., Barrett, D. W., Padilla‐Tolentino, E., & Gonzalez-Lima, F. (2008) · Behavioural Processes · doi:10.1016/j.beproc.2008.05.002 · Cited by 30
“The common feature, regardless of separation protocol and species, is that prolonged MS is a stressful manipulation that results in immediate and longterm changes to both brain and behavior (Kuhn & Schanberg, 1998; Rosenfeld, Wetmore & Levine, 1992; Plotsky & Meaney, 1993; Braun et al., 2003).”
Background
Pre-weaning maternal separation increases eating later in life in male and female offspring, but increases brainstem dopamine receptor 1a and 2a only in males
de Souza, J. A., da Silva, M. C., de Matos, R. J. B., Almeida, L. C. D. A., Beltrão, L. C., de Souza, F. L., Manhães‐de‐Castro, R., & de Souza, S. L. (2017) · Appetite · doi:10.1016/j.appet.2017.12.004 · Cited by 28
Combined early life stressors: Prenatal nicotine and maternal deprivation interact to influence affective and drug seeking behavioral phenotypes in rats
Bassey, R. B., & Gondré‐Lewis, M. C. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.07.022 · Cited by 28
Experience-dependent neuroplasticity of the developing hypothalamus: integrative epigenomic approaches
Ciernia, A. V., Laufer, B. I., Dunaway, K. W., Mordaunt, C. E., Coulson, R. L., Totah, T. S., Stolzenberg, D. S., Frahm, J. C., Singh-Taylor, A., Baram, T. Z., et al. (2018) · Epigenetics · doi:10.1080/15592294.2018.1451720 · Cited by 31
“Together, the elevated hippocampal Nr3c1 expression and reduced hypothalamic Crh expression2,5,11,16 in AMC adult offspring suggest that increased negative feedback signaling may underlie the observed hypo-responsive HPA axis in the adult AMC offspring.”
BackgroundResultInfluential
Sex differences in addiction-relevant behavioral outcomes in rodents following early life stress
Rincón‐Cortés, M. (2023) · Addiction Neuroscience · doi:10.1016/j.addicn.2023.100067 · Cited by 26
Within-litter variance in rat maternal behaviour
Cavigelli, S. A., Ragan, C. M., Barrett, C., & Michael, K. C. (2010) · Behavioural Processes · doi:10.1016/j.beproc.2010.04.005 · Cited by 31
Early life stress affects cerebral glucose metabolism in adult rhesus monkeys (Macaca mulatta)
Parr, L. A., Boudreau, M., Hecht, E. E., Winslow, J., Nemeroff, C. B., & Sánchez, M. M. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.09.003 · Cited by 29
“…axis, which has long been implicated in the etiology of stress and affective disorders (Caldji et al., 2001; Gold et al., 1998; Nemeroff, 1996; Plotsky and Meaney, 1993; Sánchez et al., 2001), and corticolimbic circuits, including the prefrontal cortex (PFC), amygdala (AMYG), hippocampus…”
Anxiety and hypothalamic–pituitary–adrenal axis responses to psychological stress are attenuated in male rats made lean by large litter rearing
Bulfin, L., Clarke, M. A., Buller, K. M., & Spencer, S. J. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.01.006 · Cited by 28
“, 2004), while many groups have demonstrated HPA axis hyperactivity after acute periods of maternal deprivation or separation (Plotsky and Meaney, 1993; Caldji et al., 2000; Levine, 2002).”
Background
Neonatal Stress Has a Long-Lasting Sex-Dependent Effect on Anxiety-Like Behavior and Neuronal Morphology in the Prefrontal Cortex and Hippocampus
de Melo, S. R., Antoniazzi, C. T. D. D., Hossain, S., & Kolb, B. E. (2018) · Developmental Neuroscience · doi:10.1159/000486619 · Cited by 28
Providing a Nurturing Environment for Infants in Adverse Situations: Multisensory Strategies for Newborn Care
White‐Traut, R. C. (2004) · Journal of Midwifery & Women s Health · doi:10.1016/j.jmwh.2004.05.004 · Cited by 35
Influence of handling or aversive stimulation during rats?? neonatal or adolescence periods on oral cocaine self-administration and cocaine withdrawal
Marquardt, A. R., Ortiz-Lemos, L., Lucion, A. B., & Barros, H. M. T. (2004) · Behavioural Pharmacology · doi:10.1097/00008877-200409000-00015 · Cited by 28
Potentiation of tumor metastasis in adulthood by neonatal endotoxin exposure: sex differences
Hodgson, D. M., & Knott, B. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00080-4 · Cited by 28
Maternal behavior in F344/N and LEW/N rats
Gomez-Serrano, M. A., Sternberg, E. M., & Riley, A. L. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00649-2 · Cited by 28
Environmental manipulations in rodents and primates
Pryce, C. R., Mohammed, A. K., & Feldon, J. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00861-4 · Cited by 28
Long lasting alteration in REM sleep of female rats submitted to long maternal separation
Tiba, P. A., Tufik, S., & Suchecki, D. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.10.001 · Cited by 27
“Several animal models have been used to elucidate the functional and biochemical consequences of early life adversity, and have revealed a number of persistent effects including changes in the activity of the hypothalamicpituitary–adrenal axis (HPA) [ 2 ,3].”
Method
Age, sex and early environment contribute to individual differences in nicotine/acetaldehyde-induced behavioral and endocrine responses in rats
Park, M. K., Belluzzi, J. D., Han, S.-H., Cao, J., & Leslie, F. M. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.10.002 · Cited by 26
Neonatal isolation decreases cued fear conditioning and frontal cortical histone 3 lysine 9 methylation in adult female rats
Kao, G.-S., Cheng, L.-Y., Chen, L.-H., Tzeng, W.-Y., Cherng, C. G., Su, C.-C., Wang, C.-Y., & Yu, L. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.09.040 · Cited by 28
The effects of repeated early deprivation on ultrasonic vocalizations and ontogenetic development in mandarin vole pups
Yu, P., Wang, J., Tai, F., Broders, H. G., An, S.-C., Zhang, X., He, F., An, X., & Wu, R. (2011) · Behavioural Processes · doi:10.1016/j.beproc.2011.09.001 · Cited by 27
Long term effects of early life stress on HPA circuit in rodent models
Babicola, L., Ventura, R., D’Addario, S. L., Ielpo, D., Andolina, D., & Segni, M. D. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.111125 · Cited by 31
Early life environmental and pharmacological stressors result in persistent dysregulations of the serotonergic system
Wong, P., Sze, Y., Gray, L. J. M., Chang, C. C. R., Cai, S., & Zhang, X. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00094 · Cited by 27
Vulnerability to dietary n-3 polyunsaturated fatty acid deficiency after exposure to early stress in rats
Ferreira, C. F., Bernardi, J. R., Krolow, R., Arcego, D. M., Fries, G. R., de Aguiar, B. W., Senter, G., Kapczinski, F. P., Silveira, P. P., & Dalmaz, C. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.03.006 · Cited by 28
“There is also clear evidence that exposure to chronic stress in early life increases vulnerability to affective disorders (Plotsky and Meaney, 1993; Meaney et al., 1996).”
Peripheral and central alterations affecting spinal nociceptive processing and pain at adulthood in rats exposed to neonatal maternal deprivation
Juif, P., Salio, C., Zell, V., Melchior, M., Lacaud, A., Petit-Demoulière, N., Ferrini, F., Darbon, P., Hanesch, U., Anton, F., et al. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13294 · Cited by 27
Neurobiology of early life stress and visceral pain: translational relevance from animal models to patient care
Prusator, D. K., Andrews, A., & Meerveld, B. G. (2016) · Neurogastroenterology & Motility · doi:10.1111/nmo.12862 · Cited by 27
Lasting effects of early life stress in mice: interaction of maternal environment and infant genes
Feifel, A., Shair, H. N., & Schmauss, C. (2017) · Genes Brain & Behavior · doi:10.1111/gbb.12395 · Cited by 27
Few long-term consequences after prolonged maternal separation in female Wistar rats
Lundberg, S., Abelson, K., Nylander, I., & Roman, E. (2017) · PLoS ONE · doi:10.1371/journal.pone.0190042 · Cited by 26
Repeated brief postnatal maternal separation enhances hypothalamic gastric autonomic circuits in juvenile rats
Banihashemi, L., & Rinaman, L. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.09.081 · Cited by 27
“Because MS15 during postnatal development alters the assembly of gastric preautonomic circuits (Card et al., 2005) and later stress reactivity (Plotsky and Meaney, 1993, Levine, 2005, Plotsky et al., 2005), we hypothesized that differences in gastric autonomic circuits would be revealed by…”
Background
Postnatal handling does not normalize hypothalamic corticotropin-releasing factor mRNA levels in animals prenatally exposed to ethanol
Gabriel, K. I., Glavas, M. M., Ellis, L. A., & Weinberg, J. (2005) · Developmental Brain Research · doi:10.1016/j.devbrainres.2005.03.005 · Cited by 27
How early maternal separation and juvenile experience with pups affect maternal behavior and emotionality in adult postpartum rats
Rees, S. L., & Fleming, A. S. (2001) · Animal Learning & Behavior · doi:10.3758/bf03192889 · Cited by 27
Long-lasting consequences of early life stress on brain structure, emotion and cognition.
Krugers, H. J., & Joëls, M. (2014) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2014_289 · Cited by 35
Long Term Hippocampal and Cortical Changes Induced by Maternal Deprivation and Neonatal Leptin Treatment in Male and Female Rats
Mela, V., Díaz, F., Borcel, É., Argente, J., Chowen, J. A., & Viveros, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137283 · Cited by 27
Effects of maternal separation, early handling, and gonadal sex on regional metabolic capacity of the preweanling rat brain
Spivey, J. M., Padilla‐Tolentino, E., Shumake, J., & Gonzalez-Lima, F. (2010) · Brain Research · doi:10.1016/j.brainres.2010.10.038 · Cited by 27
“Repeated mother–infant separation (also called maternal separation) is a known stressor in rats (Plotsky and Meaney, 1993), in which the mother is removed from the pups for prolonged periods (usually a 3- to 6-hour time period).”
Epigenetic modification of glucocorticoid receptor promoter I7 in maternally separated and restraint-stressed rats
Park, S. W., Lee, J. G., Seo, M. K., Ly, N. N., Lee, C. H., Cho, H. Y., Hein, L. T., Choi, A. J., Kim, G.-M., & Kim, Y. H. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.04.024 · Cited by 26
Effects of Early Life Stress on Epigenetic Changes of the Glucocorticoid Receptor 17 Promoter during Adulthood
Seo, M. K., Kim, S.-G., Seog, D., Bahk, W., Kim, S.-H., Park, S. W., & Lee, J. G. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21176331 · Cited by 24
Neonatal maternal separation affects metabotropic glutamate receptor 5 expression and anxiety‐related behavior of adult rats
Tsotsokou, G., Νικολακοπούλου, Μ., Kouvelas, E. D., & Mitsacos, A. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15358 · Cited by 25
“The MS model, originally developed by Plotsky and Meaney (1993), consists of separating mother and offspring for a more prolonged period (1–3 h) during the first postnatal weeks.”
Method
Early postnatal handling alters social behavior, learning, and memory of pre- and postnatal VPA-induced rat models of autism in a context-based manner
Shahrbabaki, S. S. V., Jonaidi, H., Sheibani, V., & Bashiri, H. (2022) · Physiology & Behavior · doi:10.1016/j.physbeh.2022.113739 · Cited by 27
Early Life Stress, Nicotinic Acetylcholine Receptors and Alcohol Use Disorders
Holgate, J. Y., & Bartlett, S. E. (2015) · Brain Sciences · doi:10.3390/brainsci5030258 · Cited by 27
“Changes in expression of genes and proteins involved in the stress response, like GRs and corticotrophin releasing hormone (CRH) receptors have also been found following exposure to ELS [70,71].”
Background
Impaired adaptation of gastrointestinal motility following chronic stress in maternally separated rats
Bülbül, M., Babygirija, R., Cerjak, D., Yoshimoto, S., Ludwig, K., & Takahashi, T. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00447.2011 · Cited by 26
“Plotsky and Meaney (47) reported increased CRF mRNA expression at the PVN and increased CRF-like immunoreactivity in the cerebrospinal fluid have been shown in MS rats under NS conditions.”
BackgroundMethod
Sex-Related Differences in GI Disorders
Prusator, D. K., & Chang, L. (2017) · Handbook of experimental pharmacology · doi:10.1007/164_2016_121 · Cited by 26
Early life socioeconomic status associates with interleukin-6 responses to acute laboratory stress in adulthood
Lockwood, K. G., John‐Henderson, N. A., & Marsland, A. L. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.02.016 · Cited by 26
“For instance, rodent models show that exposure to adversity during a critical period in early life results in an adult phenotype that shows hyperactive HPA responses to stress [20,51].”
Maternal separation stress drastically decreases expression of transthyretin in the brains of adult rat offspring
Kohda, K., Jinde, S., Iwamoto, K., Bundo, M., Kato, N., & Kato, T. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145705005857 · Cited by 26
“In previous studies, MS rats have shown enhanced hypothalamo– pituitary–adrenal (HPA) responses to stress in adulthood, probably due to increased expression of corticotropin-releasing factor (CRF) in the hypothalamus and decreased expression of glucocorticoid receptors (GR) in the hippocampus (Francis et al., 2002 ; L…”
Background
Maternal Genotype Influences Stress Reactivity of Vasopressin‐Deficient Brattleboro Rats
Zelena, D., Mergl, Z., & Makara, G. B. (2003) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2003.01101.x · Cited by 26
The Role of Early Experience in Infant Development
Slusarski, J. (2001) · Pediatric Physical Therapy · doi:10.1097/00001577-200110000-00013 · Cited by 43
The Roles of Environment, Experience, and Learning in Behavioral Development
Michel, G. F. (2010) · Wiley eBooks · doi:10.1002/9781444327632.ch6 · Cited by 26
“Thus, when EH rat pups are restrained as adults, their secretion of corticosterone (CORT) from their adrenal cortex and the secretion of adrenocorticotropin animals (Nuñez et al., 1995; Plotsky & Meaney, 1993).”
Background
Neuroendocrine and cellular mechanisms in stress resilience: From hormonal influence in the CNS to mitochondrial dysfunction and oxidative stress
Bhattacharya, A., Chakraborty, M., Chanda, A., Alqahtani, T., Kumer, A., Dhara, B., & Chattopadhyay, M. (2024) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.18220 · Cited by 27
“40 Maternal care behaviour has emerged as a critical determinant of resilience to early-life stress, leading to significant individual differences in gene expression and subsequent activation of the neuroendocrine stress response.”
Background
Early-life stress sensitizes response to future stress: Evidence and mechanisms
Peña, C. J. (2025) · Neurobiology of Stress · doi:10.1016/j.ynstr.2025.100716 · Cited by 29
“Foundational research showed that separating rat pups from their dams for 3 h per day from postnatal day (P) 2 – 14 disrupted the hypothalamic pituitary adrenal (HPA) axis into adulthood (Ader et al., 1960; Plotsky and Meaney, 1993).”
Neonatal maternal separation up-regulates protein signalling for cell survival in rat hypothalamus
Irles, C., Nava-Kopp, A. T., Morán, J., & Zhang, L. (2014) · Stress · doi:10.3109/10253890.2014.913017 · Cited by 25
“MS is a well-validated rodent model used to assess the effect of early postnatal stress on cognition and emotionality in adulthood (Meaney et al., 1985; Plotsky & Meaney, 1993; Veenema, 2009; Zhang et al., 2012).”
Background
Environment and early life: Decisive factors for stress-resilience and vulnerability
Hegde, A., & Mitra, R. (2020) · International review of neurobiology · doi:10.1016/bs.irn.2019.12.002 · Cited by 31
Urinary free cortisol and childhood trauma in cocaine dependent adults
Roy, A. (2002) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(02)00002-x · Cited by 25
Early stress leads to effects on estrous cycle and differential responses to stress
Mourlon, V., Naudon, L., Bruno Giros, A., Crumeyrolle‐Arias, M., & Daugé, V. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.11.003 · Cited by 25
The Impact of Healthy Parenting As a Protective Factor for Posttraumatic Stress Disorder in Adulthood: A Case-Control Study
Lima, A. R., Mello, M. F., Andreoli, S. B., Fossaluza, V., de Araújo, C. M., Jackowski, A. P., Bressan, R. A., & Mari, J. D. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087117 · Cited by 24
“Studies with animal models have demonstrated the importance of parental bonding for rodent development [6;7;8].”
BackgroundMethod
Early maternal separation and sex differences in the aversive effects of amphetamine in adult rats
Roma, P. G., Davis, C. M., Kohut, S. J., Huntsberry, M. E., & Riley, A. L. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.12.007 · Cited by 25
Central neural responses to restraint stress are altered in rats with an early life history of repeated brief maternal separation
Banihashemi, L., O'Neill, E. J., & Rinaman, L. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.06.052 · Cited by 25
“…alter the amount and quality of maternal care received by rat pups during the early postnatal period result in life-long alterations in their behavioral and hypothalamic-pituitary-adrenal (HPA) stress responses (Plotsky and Meaney, 1993; Liu et al., 1997; Caldji et al., 2000; Macrì et al., 2008).”
Aportes de la epigenética en la comprensión del desarrollo del ser humano
Bedregal, P., Beatriz Shand, K., Santos, M. J., & Patricio Ventura-Junca, T. (2010) · Revista médica de Chile · doi:10.4067/s0034-98872010000300018 · Cited by 30
Early life stress induces immune priming in kidneys of adult male rats
Miguel, C. D., Obi, I. E., Ho, D. H., Loria, A. S., & Pollock, J. S. (2017) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00590.2016 · Cited by 26
“Furthermore, MatSep is known to increase activation of the hypothalamic-pituitary-adrenal (HPA) axis during early life (35, 53).”
Background
Visceral Pain and Psychiatric Disorders
Felice, V. D., Moloney, R. D., Cryan, J. F., Dinan, T. G., & O’Mahony, S. M. (2015) · Modern trends in psychiatry · doi:10.1159/000435936 · Cited by 27
Psychological factors in skin diseases: Stress and skin: Facts and controversies
Orion, E., & Wolf, R. (2013) · Clinics in Dermatology · doi:10.1016/j.clindermatol.2013.05.006 · Cited by 28
Sex Differences in Voluntary Drinking by Long Evans Rats following Early Stress
Lancaster, F. E. (1998) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1998.tb03875.x · Cited by 25
Vasopressin pressor receptor-mediated activation of HPA axis by acute ethanol stress in rats
László, F. A., Varga, C., Pavo, I. J., Gardi, J., Vecsernyés, M., Gálfi, M., Morschl, É., László, F. A., & Makara, G. B. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.2.r458 · Cited by 25
Immediate and longterm effects of immune stimulation: hypothesis linking the immune response to subsequent physical and psychological wellbeing
Hurwitz, E. L., & Morgenstern, H. (2001) · Medical Hypotheses · doi:10.1054/mehy.2000.1217 · Cited by 25
REM sleep loss–induced elevated noradrenaline could predispose an individual to psychosomatic disorders: a review focused on proposal for prediction, prevention, and personalized treatment
Mehta, R., Giri, S., & Mallick, B. N. (2020) · The EPMA Journal · doi:10.1007/s13167-020-00222-1 · Cited by 24
Models of progressive neurological dysfunction originating early in life
Marriott, A. L., Rojas-Mancilla, E., Morales, P., Herrera‐Marschitz, M., & Tasker, R. A. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.10.001 · Cited by 25
“…sensitivity to apomorphine (Ellenbroek and Cools, 1995 [31_TD$DIFF]b; Rots et al., 1996) as well as alterations to hypothalamicpituitary (HPA) axis functioning and corticosterone responsiveness to stressors (Ladd et al., 1996; Meaney et al., 1996; Plotsky and Meaney, 1993; Stanton et al., 1988).”
Background
Neonatal handling affects learning, reversal learning and antioxidant enzymes activities in a sex‐specific manner in rats
Noschang, C. G., Krolow, R., Arcego, D. M., Toniazzo, A. P., Huffell, A. P., & Dalmaz, C. (2012) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2012.01.010 · Cited by 24
“In rats, it has been demonstrated that both prenatal and postnatal factors may influence the development of the HPA axis (Liu et al., 1997; Maccari et al., 2003; Plotsky and Meaney, 1992; Weinstock, 1997).”
Background
Serum NGF, BDNF and IL-6 Levels in Postpartum Mothers As Predictors of Infant Development: The Influence of Affective Disorders
Pinheiro, K. A. T., Pinheiro, R. T., Coelho, F. M. D. C., da Silva, R. A., Quevedo, L. D. Á., Schwanz, C. C., Wiener, C. D., Manfro, G. G., Giovenardi, M., Lucion, A. B., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094581 · Cited by 26
“In preclinical studies that model early adversity, maternal separation stress affects the levels of NGF, BDNF and cortisol in the limbic areas of offspring and produces long-lasting changes in emotional behavior and impaired responses to stress, suggesting that these neurotrophins may participate in the mechanism that…”
The effects of early isolation on sexual behavior and c‐fos expression in naïve male long‐evans rats
Akbari, E. M., Budin, R., Parada, M., & Fleming, A. S. (2008) · Developmental Psychobiology · doi:10.1002/dev.20290 · Cited by 24
Circadian Rhythms of Urinary Cortisol Levels Vary Between Individuals in Wild Male Chimpanzees: A Reaction Norm Approach
Sonnweber, R., Araya-Ajoy, Y., Behringer, V., Deschner, T., Tkaczynski, P., Fedurek, P., Preis, A., Samuni, L., Zommers, Z., Gomes, C., et al. (2018) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2018.00085 · Cited by 26
Early-Life Experiences: Enduring Behavioral, Neurological, and Endocrinological Consequences
Romeo, R. D., Tang, A. C., & Sullivan, R. M. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00062-0 · Cited by 25
Influence of cocaine dependence and early life stress on pituitary–adrenal axis responses to CRH and the Trier social stressor
Maria, M. M. M., McRae‐Clark, A. L., Back, S. E., DeSantis, S. M., Baker, N. L., Spratt, E. G., Simpson, A. N., & Brady, K. T. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.05.001 · Cited by 25
“For example, rodents exposed to postnatal stressors such as maternal separation, exhibit elevated corticotropin releasing hormone (CRH) mRNA in the hypothalamus, central amygdala, and increased CRH receptor levels in the locus coeruleus (Plotsky and Meaney 1983; Plotsky et al., 2005).”
Background
Effects of early deprivation and maternal separation on pup‐directed behavior and HPA axis measures in the juvenile female rat
Rees, S. L., Akbari, E. M., Steiner, M. S., & Fleming, A. S. (2008) · Developmental Psychobiology · doi:10.1002/dev.20292 · Cited by 24
Iron Deficiency in Infancy Predicts Altered Serum Prolactin Response 10 Years Later
Felt, B. T., Jiménez, E., Smith, J. A., Calatroni, A., Kaciroti, N., Wheatcroft, G., & Lozoff, B. (2006) · Pediatric Research · doi:10.1203/01.pdr.0000242848.45999.7b · Cited by 24
“Rodent studies of the developing hypothalamicpituitary-adrenal axis and the pattern of corticosterone response to stress have shown that the timing and duration of early stressful experiences affects the direction of the stressresponse system long-term, resulting in exaggerated or blunted corticosterone response patte…”
Background
Do neonatal pain and stress program the brain's response to future stimuli?
Winberg, J. (1998) · Acta Paediatrica · doi:10.1080/080352598750013761 · Cited by 24
Stress-induced red nucleus attenuation induces anxiety-like behavior and lymph node CCL5 secretion
Shi, D., Zhang, Y.-D., Zhang, S., Liao, B.-B., Chu, M., Su, S., Zhuo, K., Hu, H., Zhang, C., & Wang, Z. (2023) · Nature Communications · doi:10.1038/s41467-023-42814-1 · Cited by 22
Chemogenetic activation of the lateral hypothalamus reverses early life stress-induced deficits in motivational drive
Campbell, E. J., Mitchell, C. S., Adams, C. D., Yeoh, J. W., Hodgson, D. M., Graham, B. A., & Dayas, C. V. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13674 · Cited by 17

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

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 ›

Are you an author, or do you see a problem with this page? Request a review

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

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks