Effects of prenatal restraint stress on the hypothalamus–pituitary–adrenal axis and related behavioural and neurobiological alterations
Abstract
Chronic hyper-activation of the hypothalamus-pituitary axis is associated with the suppression of reproductive, growth, thyroid and immune functions that may lead to various pathological states. Although many individuals experiencing stressful events do not develop pathologies, stress seems to be a provoking factor in those individuals with particular vulnerability, determined by genetic factors or earlier experience. Exposure of the developing brain to severe and/or prolonged stress may result in hyper-activity of the stress system, defective glucocorticoids-negative feedback, altered cognition, novelty seeking, increased vulnerability to addictive behaviour, and mood-related disorders. Therefore, stress-related events that occur in the perinatal period can permanently change brain and behaviour of the developing individual. Prenatal restraint stress (PRS) in rats is a well-documented model of early stress known to induce long-lasting neurobiological and behavioural alterations including impaired feedback mechanisms of the HPA axis, disruption of circadian rhythms and altered neuroplasticity. Chronic treatments with antidepressants at adulthood have proven high predictive validity of the PRS rat as animal model of depression and, reinforce the idea of the usefulness of the PRS rat as an interesting animal model for the design and testing of new pharmacologic strategies in the treatment of stress-related disorders.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
The naïve control group was included as a potential control for stress induced by gavage, because prenatal stress can alter later behaviors.
“The naïve control group was included as a potential control for stress induced by gavage, because prenatal stress can alter later behaviors (reviewed in Buynitsky and Mostofsky, 2009;Maccari and Morley-Fletcher, 2007;Weinstock, 2001).”
From Developmental Treatment with Ethinyl Estradiol, but Not Bisphenol A, Causes Alterations in Sexually Dimorphic Behaviors in Male and Female Sprague Dawley Rats (2014) · cites this paper as Maccari and Morley-Fletcher, 2007
Cites
THE EFFECTS OF STRESSFUL LIFE EVENTS ON DEPRESSION
Kessler, R. C. (1997) · Annual Review of Psychology · doi:10.1146/annurev.psych.48.1.191 · Cited by 2,111 · cited 1× · see citing works
“The stress-driven theory of mood disorders (Sapolsky, 1996; Kessler, 1997) suggests that a stress-induced model of depression such as the PRS model has good construct validity (Rosenwasser and Wirz-Justice, 1997).”
BackgroundWhy stress is bad for your brain
Sapolsky, R. M. (1996) · Science · doi:10.1126/science.273.5276.749 · Cited by 1,306 · cited 1× · see citing works
“The stress-driven theory of mood disorders (Sapolsky, 1996; Kessler, 1997) suggests that a stress-induced model of depression such as the PRS model has good construct validity (Rosenwasser and Wirz-Justice, 1997).”
Lemaire, V., Koehl, M., Le Moal, M., & Abrous, D. N. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.20.11032 · Cited by 1,044 · cited 1× · see citing works
“Interestingly, PRS induces a life span reduction of hippocampal neurogenesis in male rats (Lemaire et al., 2000, 2006) but not in females (Darnaudéry et al., 2006), and a chronic agomelatine treatment increases hippocampal neurogenesis especially in the ventral part of the hippocampus of male rats…”
BackgroundLemaire, V., Lamarque, S., Le Moal, M., Piazza, P.-V., & Abrous, D. N. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.11.009 · Cited by 211 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Brain on stress: how the social environment gets under the skin
McEwen, B. S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121254109 · Cited by 1,200 · see citing works
Stress and anxiety: Structural plasticity and epigenetic regulation as a consequence of stress
McEwen, B. S., Eiland, L., Hunter, R. G., & Miller, M. M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.07.014 · Cited by 596 · see citing works
Prenatal maternal stress programs infant stress regulation
Davis, E. P., Glynn, L. M., Waffarn, F., & Sandman, C. A. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02314.x · Cited by 472 · see citing works
Restraint stress in biobehavioral research: Recent developments
Buynitsky, T., & Mostofsky, D. I. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.004 · Cited by 426 · see citing works
Epigenetic programming of the stress response in male and female rats by prenatal restraint stress
Darnaudéry, M., & Maccari, S. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.11.004 · Cited by 412 · see citing works
Self-citationEpigenetic Mechanisms of Depression and Antidepressant Action
Vialou, V., Feng, J., Robison, A. J., & Nestler, E. J. (2013) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010611-134540 · Cited by 277 · see citing works
McEwen, B. S., Gray, J. D., & Nasca, C. (2015) · Journal of Endocrinology · doi:10.1530/joe-15-0121 · Cited by 253 · see citing works
11β-Hydroxysteroid dehydrogenases and the brain: From zero to hero, a decade of progress
Wyrwoll, C. S., Holmes, M. C., & Seckl, J. R. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.12.001 · Cited by 244 · see citing works
Voorhees, J. L., Tarr, A. J., Wohleb, E. S., Godbout, J. P., Mo, X., Sheridan, J. F., Eubank, T. D., & Marsh, C. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058488 · Cited by 236 · see citing works
Circadian rhythms and depression: Human psychopathology and animal models
Kronfeld-Schor, N., & Einat, H. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.08.020 · Cited by 166 · see citing works
Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models
Marco, E. M., Macrì, S., & Laviola, G. (2011) · Neurotoxicity Research · doi:10.1007/s12640-010-9205-z · Cited by 144 · see citing works
Aktar, E., Qu, J., Lawrence, P. J., Tollenaar, M. S., Elzinga, B. M., & Bögels, S. M. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00391 · Cited by 140 · see citing works
Stress-induced mechanisms in mental illness: A role for glucocorticoid signalling
Cattaneo, A., & Riva, M. A. (2016) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2015.07.021 · Cited by 118 · see citing works
Matrisciano, F., Tueting, P., Maccari, S., Nicoletti, F., & Guidotti, A. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.274 · Cited by 110 · see citing works
Self-citationBartlett, A. A., Singh, R., & Hunter, R. G. (2017) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-319-53889-1_8 · Cited by 91 · see citing works
Towards translational rodent models of depression
O’Leary, O. F., & Cryan, J. F. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1587-9 · Cited by 60 · see citing works
Ferguson, S. A., Law, C. D., & Abshire, J. S. (2011) · Toxicological Sciences · doi:10.1093/toxsci/kfr201 · Cited by 54 · see citing works
Ferguson, S. A., Law, C. D., & Kissling, G. E. (2014) · Toxicological Sciences · doi:10.1093/toxsci/kfu077 · Cited by 32 · see citing works
“The naı̈ve control group was included as a potential control for stress induced by gavage, because prenatal stress can alter later behaviors (reviewed in Buynitsky and Mostofsky, 2009; Maccari and Morley-Fletcher, 2007; Weinstock, 2001).”
MethodMacrì, S., Ceci, C., Canese, R., & Laviola, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041821 · Cited by 20 · see citing works
- Authors
- Maccari, S., & Morley-Fletcher, S.
- Affiliations
- Université de Lille (FR)
- Corresponding author
- Maccari, Stefania
- ORCID
- Maccari, Stefania
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2007-08
- Volume
- 32
- Pages
- S10-S15
- ISSN
- 0306-4530 (ISSN-L)
- OpenAlex
- W2107423916
- Cited by
- 302
- References
- 4
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 3 · 2023: 3 · 2022: 8 · 2021: 11 · 2020: 10 · 2019: 8 · 2018: 12 · 2017: 13 · 2016: 16 · 2015: 30 · 2014: 28 · 2013: 35 · 2012: 34
- FWCI
- 1.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Université de Lille
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- prenatal restraint stress, hypothalamic-pituitary-adrenal axis, glucocorticoid negative feedback, early life stress, developmental programming, circadian rhythm, neuroplasticity, novelty seeking, addictive behavior, mood disorders, animal models of depression, antidepressants, stress-related disorders
- MeSH terms
- Animals, Depressive Disorder, Disease Models, Animal, Female, Humans, Hypothalamo-Hypophyseal System, Neuronal Plasticity, Neurosecretory Systems, Pituitary-Adrenal System, Pregnancy, Prenatal Exposure Delayed Effects, Restraint, Physical, Stress, Psychological, 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