Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats.
Abstract
Prenatal stress (PS) can produce profound and long-lasting perturbations of individual adaptive capacities, which in turn can result in an increased proneness to behavioural disorders. Indeed, in PS rats there is evidence of impaired social play behaviour, disturbances in a variety of circadian rhythms, enhanced anxiety and increased hypothalamic-pituitary-adrenal (HPA) axis reactivity. This study was designed to experimentally investigate the degree of reversibility of PS-induced disturbances of social play and HPA reactivity by assessing the effect of the enrichment of the physical environment on PS rats during periadolescence. PS subjects showed a reduced expression of social play behaviour and a prolonged corticosterone secretion in response to restraint stress, but both these effects were markedly reversed following environmental enrichment. Interestingly, the enrichment procedure increased social behaviour but had no effect on corticosterone secretion in nonstressed animals, indicating a differential impact of the postnatal environment as a function of prenatal background. As a whole, results clearly indicate that rats prenatally exposed to stress can benefit during periadolescence from the modulatory effects of an enriched environment. Moreover, they confirm that PS may well represent a suitable animal model for the design and testing of new therapeutic strategies for behavioural disorders produced by early insults.
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Morley-Fletcher et al. (2003) were able to diminish prenatal stress-induced impairments in social play behavior in rats with physical, but not social, environmental enrichment.
“Notably, Morley-Fletcher et al. (2003) were able to diminish prenatal stress-induced impairments in social play behavior in rats with physical, but not social, environmental enrichment (Laviola et al., 2004).”
From Effects of Maternal Deprivation and Complex Housing on Rat Social Behavior in Adolescence and Adulthood (2018) · cites this paper as Morley-Fletcher et al., 2003
Cites
Neural consequences of enviromental enrichment
van Praag, H., Kempermann, G., & Gage, F. H. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044558 · Cited by 2,468 · see citing works
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · see citing works
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 · see citing works
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 · see citing works
Environmental Enrichment Reverses the Effects of Maternal Separation on Stress Reactivity
Francis, D. D., Diorio, J., Plotsky, P. M., & Meaney, M. J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-18-07840.2002 · Cited by 663 · see citing works
Schrijver, N. C. A., Bahr, N. I., Weiss, I. C., & Würbel, H. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00790-6 · Cited by 294 · see citing works
Adriani, W., Chiarotti, F., & Laviola, G. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.5.1152 · Cited by 247 · see citing works
Self-citationPrenatal stress feminizes juvenile play patterns in male rats
Ward, I. L., & Stehm, K. E. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90552-y · Cited by 125 · see citing works
Hotchkiss, A. K., Ostby, J. S., Vandenburgh, J. G., & Gray, L. E. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.02110s3435 · Cited by 82 · see citing works
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Enriched environments, experience-dependent plasticity and disorders of the nervous system
Nithianantharajah, J., & Hannan, A. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1970 · Cited by 1,771 · 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-citationEnvironment and Brain Plasticity: Towards an Endogenous Pharmacotherapy
Sale, A., Berardi, N., & Maffei, L. (2014) · Physiological Reviews · doi:10.1152/physrev.00036.2012 · Cited by 402 · see citing works
Stress and the adolescent brain
ROMEO, R. D., & McEWEN, B. S. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1376.022 · Cited by 379 · see citing works
Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour
Weinstock, M. (2007) · Neurochemical Research · doi:10.1007/s11064-007-9339-4 · Cited by 349 · see citing works
The neurobiology of social play and its rewarding value in rats
Vanderschuren, L. J. M. J., Achterberg, E. J. M., & Trezza, V. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.025 · Cited by 329 · see citing works
Prenatal stress: Effects on fetal and child brain development
(2020) · International Review of Neurobiology · doi:10.1016/bs.irn.2019.11.002 · Cited by 326 · see citing works
Laviola, G., Hannan, A. J., Macrì, S., Solinas, M., & Jaber, M. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.05.001 · Cited by 300 · see citing works
Schneider, T., Turczak, J., & Przewłocki, R. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300767 · Cited by 298 · see citing works
McCormick, C. M., Mathews, I. Z., Thomas, C., & Waters, P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.06.003 · Cited by 276 · see citing works
Epigenetic influence of social experiences across the lifespan
Champagne, F. A. (2010) · Developmental Psychobiology · doi:10.1002/dev.20436 · Cited by 273 · see citing works
Gunnar, M. R., DePasquale, C. E., Reid, B. M., Donzella, B., & Miller, B. S. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1909699116 · Cited by 207 · 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
Yang, J., Hou, C., Ma, N., Liu, J., Zhang, Y., Zhou, J., Xu, L., & Li, L. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.09.001 · Cited by 127 · see citing works
Gur, T. L., Palkar, A. V., Rajasekera, T., Allen, J., Niraula, A., Godbout, J., & Bailey, M. T. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.06.025 · Cited by 127 · see citing works
Environmental enrichment decreases the rewarding but not the activating effects of heroin
El Rawas, R., Thiriet, N., Lardeux, V., Jaber, M., & Solinas, M. (2009) · Psychopharmacology · doi:10.1007/s00213-008-1402-6 · Cited by 121 · see citing works
Champagne, F. A. (2010) · Perspectives on Psychological Science · doi:10.1177/1745691610383494 · Cited by 110 · see citing works
Sze, Y., & Brunton, P. J. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14615 · Cited by 85 · see citing works
Kofink, D., Boks, M. P. M., Timmers, H. T. M., & Kas, M. J. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.020 · Cited by 83 · see citing works
Sadeghi, M., Peeri, M., & Hosseini, M.-J. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.05.017 · Cited by 83 · see citing works
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64 · see citing works
Environmental intervention as a therapy for adverse programming by ancestral stress
McCreary, J. K., Erickson, Z. T., Hao, Y., Ilnytskyy, Y., Kovalchuk, I., & Metz, G. A. S. (2016) · Scientific Reports · doi:10.1038/srep37814 · Cited by 59 · see citing works
Reynolds, S., Lane, S. J., & Richards, L. (2010) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-010-9053-4 · Cited by 54 · see citing works
Walker, S. E., Papilloud, A., Huzard, D., & Sandi, C. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.10.008 · Cited by 49 · see citing works
Opioid addiction: who are your real friends?
Eitan, S., Emery, M. A., Bates, M. L. S., & Horrax, C. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.05.017 · Cited by 42 · see citing works
Kentrop, J., Smid, C. R., Achterberg, E. J. M., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Joëls, M., & van der Veen, R. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00193 · Cited by 41 · see citing works
Schmidt, M., Lax, E., Zhou, R., Cheishvili, D., Ruder, A. M., Ludiro, A., Lapert, F., Macedo da Cruz, A., Sandrini, P., Calzoni, T., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-018-0348-7 · Cited by 37 · see citing works
Sahafi, E., Peeri, M., Hosseini, M.-J., & Azarbyjani, M. A. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.10.022 · Cited by 32 · see citing works
- Authors
- Morley‐Fletcher, S., Rea, M., Maccari, S., & Laviola, G.
- Affiliations
- Université de Lille (FR)
- Istituto Superiore di Sanità (IT)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2003-12
- Volume
- 18
- Issue
- 12
- Pages
- 3367-3374
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2006578440
- Cited by
- 373
- References
- 9
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 9 · 2023: 9 · 2022: 11 · 2021: 15 · 2020: 14 · 2019: 22 · 2018: 23 · 2017: 24 · 2016: 23 · 2015: 25 · 2014: 24 · 2013: 19 · 2012: 21
- FWCI
- 3.51
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- 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
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- prenatal stress, environmental enrichment, HPA axis reactivity, corticosterone, restraint stress, periadolescence, behavioural disorders, rats
- MeSH terms
- Adolescent, Aging, Animals, Behavior, Animal, Corticosterone, Environment, Controlled, Female, Humans, Hypothalamo-Hypophyseal System, Male, Pituitary-Adrenal System, Pregnancy, Prenatal Exposure Delayed Effects, Social Behavior, Stress, Physiological, Rats, Sprague-Dawley, Rats
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