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Early Life Stress: Consequences for the Development of the Brain

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This literature review demonstrates the importance and consequences of early life stress for the development of the brain and its role in the formation of neurological and mental illnesses (particularly depression). The most dangerous is chronic early life stress during the neonatal period of development in the first days after birth, when the effects on the development of the brain, neuro-, synapto-, and glio-, and angiogenesis are the most stable. Among all the neuropsychological effects of early life stress, the most common are apparent as depressive disorders in humans and animals, and this constitutes a widely used model of experimental depression in rodents.

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References

  • Aisa, B., Elizalde, N., Tordera, R., et al., “Effects of neonatal stress on markers of synaptic plasticity in the hippocampus: implications for spatial memory,” Hippocampus, 19, No. 12, 1222–1231 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Ali, I., O’Brien, P., Kumar, G., et al., “Enduring effects of early life stress on firing patterns of hippocampal and thalamocortical neurons in rats: implications for limbic epilepsy,” PLoS One, 8, No. 6, e66962 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avishai-Eliner, S., Gilles, E. E., Eghbal-Ahmadi, M., et al., “Altered regulation of gene and protein expression of hypothalamic-pituitary-adrenal axis components in an immature rat model of chronic stress,” J. Neuroendocrinol., 13, No. 9, 799–807 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baek, S. B., Bahn, G., Moon, S. J., et al., “The phosphodiesterase type-5 inhibitor, tadalafil, improves depressive symptoms, ameliorates memory impairment, as well as suppresses apoptosis and enhances cell proliferation in the hippocampus of maternal-separated rat pups,” Neurosci. Lett., 488, No. 1, 26–30 (2011).

    Article  CAS  PubMed  Google Scholar 

  • Baek, S. S., Jun T. W., Kim, K. J., et al., “Effects of postnatal treadmill exercise on apoptotic neuronal cell death and cell proliferation of maternal-separated rat pups,” Brain Dev., 34, No. 1, 45–56 (2012).

    Article  PubMed  Google Scholar 

  • Bagot, R. C., van Hasselt, E. N., Champagne, D. L., et al., “Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus,” Neurobiol. Learn. Mem., 92, No. 3, 292–300 (2009).

    Article  PubMed  Google Scholar 

  • Bakos, J., Duncko, R., Makatsori, A., et al., “Prenatal immune challenge affects growth, behavior, and brain, dopamine in offspring,” Ann. N. Y. Acad. Sci., 1018, 281–287 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Bale, T. L., “Epigenetic and transgenerational reprogramming of brain development,” Nat. Rev. Neurosci., 16, No. 6, 332–344 (2015).

    Article  CAS  PubMed  Google Scholar 

  • Bayer, S. A., Altman, J., Russo, R. J., and Zhang, X., “Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat,” Neurotoxicology, 14, No. 1, 83–144 (1993).

    CAS  PubMed  Google Scholar 

  • Beck, S. L. and Gavin D. L., “Susceptibility of mice to audiogenic seizures is increased by handling their dams during gestation,” Science, 193, No. 4251, 427–428 (1976).

    Article  CAS  PubMed  Google Scholar 

  • Bilbo, S. D. and Schwarz J. M., “Early-life programming of later-life brain and behavior: a critical role for the immune system,” Front. Behav. Neurosci., 3, 1–14 (2009).

    Article  Google Scholar 

  • Boersma, G. J. and Tamashiro K. L., “Individual differences in the effects of prenatal stress exposure in rodents,” Neurobiol. Stress, 1, 100–108 (2015).

    Article  PubMed  Google Scholar 

  • Boisse, L., Spencer, S. J., Mouihate, A., et al., “Neonatal immune challenge alters nociception in the adult rat,” Pain, 119, No. 1–3, 133–141 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Boldrini, M., Hen, R., Underwood, M. D., et al., “Hippocampal angiogenesis and progenitor cell proliferation are increased with antidepressant use in major depression,” Biol. Psychiatry, 72, No. 7, 562–571 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunson, K. L., Kramar, E., Lin, B., et al., “Mechanisms of late-onset cognitive decline after early-life stress,” J. Neurosci., 25, No. 41, 9328–9338 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunton, P. J., “Programming the brain and behaviour by early-life stress: a focus on neuroactive steroids,” J. Neuroendocrinol., 27, No. 6, 468–480 (2015).

    Article  CAS  PubMed  Google Scholar 

  • Carr, C. P., Martins, C. M., Stingel, A. M., et al., “The role of early life stress in adult psychiatric disorders: a systematic review according to childhood trauma subtypes,” J. Nerv. Ment. Dis., 201. No. 12, 1007–1020 (2013).

    Article  PubMed  Google Scholar 

  • Clancy, B., Finlay, B. L., Darlington, R. B., and Anand, K. J., “Extrapolating brain development from experimental species to humans,” Neurotoxicology, 28, No. 5, 931–937 (2007).

    Article  PubMed  Google Scholar 

  • Cohen, R. A., Grieve, S., Hoth, K. E., et al., “Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei,” Biol. Psychiatry, 59, No. 10, 975–982 (2006).

    Article  PubMed  Google Scholar 

  • Comasco, E., Todkar, A., Granholm, L., et al., “Alpha 2a-adrenoceptor gene expression and early life stress-mediated propensity to alcohol drinking in outbred rats,” Int. J. Environ. Res. Public Health, 12, No. 7, 7154–7171 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coyle, P., Tran, N., Fung, J. N., et al., “Maternal dietary zinc supplementation prevents aberrant behaviour in an object recognition task in mice offspring exposed to LPS in early pregnancy,” Behav. Brain Res., 197, No. 1, 210–218 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Cui, K., Ashdown, H., Luheshi, G. N., and Boksa, P., “Effects of prenatal immune activation on hippocampal neurogenesis in the rat,” Schizophr. Res., 113, No. 2–3, 288–297 (2009).

    Article  PubMed  Google Scholar 

  • Dalle Molle, R., Portella, A. K., Goldani, M. Z., et al., “Associations between parenting behavior and anxiety in a rodent model and a clinical sample: relationship to peripheral BDNF levels,” Transl. Psychiatry, 2, el95 (2012).

    Article  Google Scholar 

  • Edwards, H. E., Dortok, D., Tam, J., et al., “Prenatal stress alters seizure thresholds and the development of kindled seizures in infant and adult rats,” Harm. Behav., 42, No. 4, 437–447 (2002).

    Article  Google Scholar 

  • Eisch, A. J. and Petrik D., “Depression and hippocampal neurogenesis: a road to remission,” Science, 338, No. 6103, 72–75 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fabricius, K., Wortwein, G., and Pakkenberg, B., “The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus,” Brain Struct. Funct., 212, No. 5, 403–416 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  • Favre, M. R., Barkat, T. R., Lamendola, D., et al., “General developmental health in the VPA-rat model of autism,” Front Behav. Neurosci., 7: 1–11 (2013).

    Article  Google Scholar 

  • Fortier, M. E., Joober, R., Luheshi, G. N., and Boksa, P., “Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamine-induced locomotion and startle responses in adult rat offspring,” J. Psychiatr Res., 38, No. 3, 335–345 (2004).

    Article  PubMed  Google Scholar 

  • Gilles, E. E., Schultz, L., and Baram, T. Z., “Abnormal corticosterone regulation in an immature rat model of continuous chronic stress,” Pediatr. Neurol., 15, No. 2, 114–119 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Girardi, C. E., Zanta, N. C., and Suchecki, D., “Neonatal stress-induced affective changes in adolescent Wistar rats: early signs of schizophrenia-like behavior,” Front Behav. Neurosci., 8, 1–9 (2014).

    Article  Google Scholar 

  • Golan, H. M., Lev, V. Hallak, M., et al., “Specific neurodevelopmental damage in mice offspring following maternal inflammation during pregnancy,” Neuropharmacology, 48, No. 6, 903–917 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Gonzalez, B. and Escobar A., “Altered functional development of the blood-brain barrier after early life stress in the rat,” Brain Res. Bull., 79, No. 6, 376–387 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Gunn, B. G., Cunningham, L., Cooper, M. A., et al., “Dysfunctional astrocytic and synaptic regulation of hypothalamic glutamatergic transmission in a mouse model of early-life adversity: relevance to neurosteroids and programming of the stress response,” J. Neurosci., 33, No. 50: 19534–19554 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutman, D. A. and Nemeroff C. B., “Neurobiology of early life stress: rodent studies,” Semin. Clin. Neuropsychiatry, 7, No. 2, 89–95 (2002).

    Article  PubMed  Google Scholar 

  • Hanson, J. L., Nacewicz, B. M., Sutterer, M. J., et al., “Behavioral problems after early life stress: contributions of the hippocampus and amygdala,” Biol. Psychiatry, 77, No. 4, 314–323 (2015).

    Article  PubMed  Google Scholar 

  • Hara, Y., Maeda, Y., Kataoka, S., et al., “Effect of prenatal valproic acid exposure on cortical morphology in female mice,” J. Pharmacol. Sci., 118, No. 4, 543–546 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Harrison, E. L. and Baune B. T., “Modulation of early stress-induced neurobiological changes: a review of behavioural and pharmacological interventions in animal models,” Transl. Psychiatry, 4, 1–18 (2014).

    Article  Google Scholar 

  • Hava, G., Vered, L., Yael, M., et al., “Alterations in behavior in adult offspring mice following maternal inflammation during pregnancy,” Dev. Psychobiol., 48, No. 2, 162–168 (2006).

    Article  PubMed  Google Scholar 

  • Hellemans, K. G., Sliwowska, J. H., Verma, P., and Weinberg, J., “Prenatal alcohol exposure: Fetal programming and later life vulnerability to stress, depression and anxiety disorders,” Neurosci. Biobehav. Rev., 34, No. 6, 791–807 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Hornig, M., Solbrig, M., Horscroft, N., et al., “Boma disease virus infection of adult and neonatal rats: models for neuropsychiatric disease,” Curr. Top Microbiol. Immunol., 253, 157–177 (2001).

    CAS  PubMed  Google Scholar 

  • Huang, L. T., “Early-life stress impacts the developing hippo-campus and primes seizure occurrence: cellular, molecular, and epigenetic, mechanisms,” Front. Mol. Neurosci., 7, 1–15 (2014).

    Article  Google Scholar 

  • Huishof, H. J., Novati, A., Sgoifo, A., et al., “Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effect on stress sensitivity and anxiety in adult Wistar rats,” Behav. Brain Res., 216, No. 2, 552–560 (2011).

    Article  Google Scholar 

  • Huot, R. L., Plotsky, P. M., Lenox, R. H., and McNamara, R. K., “Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats,” Brain Res., 950, No. 1–2, 52–63 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Jasarevic, E., Rodgers, A. B., and Bale, T. L., “A novel role for maternal stress and microbial transmission in early life programming and neurodevelopment,” Neurobiol. Stress, No. 1, 81–88 (2015).

  • Karalcal, P., Bozkir, M. G., Dere, E., et al., “The effects of maternal deprivation on the hippocampal structure in adult rats,” Can. J. Neurol. Sci., 36, No. 3, 356–362 (2009).

    Article  Google Scholar 

  • Kikusui, T. and Mori, Y., “Behavioural and neurochemical consequences of early weaning in rodents,” J. Neuroendocrinol., 21, No. 4, 427–431 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Kinast, K., Peeters, D., Kolk, S. M., et al., “Genetic and pharmacological manipulations of the serotonergic system in early life: neurodevelopmental underpinnings of autism-related behavior,” Front Cell. Neurosci., 7, 1–17 (2013).

    Article  Google Scholar 

  • Kohman, R. A., Tarr, A. J., Sparkman, N. L., et al., “Neonatal endotoxin exposure impairs avoidance learning and attenuates endotoxin-induced sickness behavior and central IL-1beta gene transcription in adulthood,” Behav. Brain Res., 194, No. 1, 25–31 (2008).

    Article  CAS  PubMed  Google Scholar 

  • Korosi, A., Naninck, E. E., Oomen, C. A., et al., “Early-life stress mediated modulation of adult neurogenesis and behavior,” Behav. Brain Res., 227, No. 2, 400–409 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Krivoruchenko, V. K., “Child abuse: occurrence and prevention,” www.zpu-journal.ru/e-zpu/2012/3/Krivoruchenko_Child-Abuse/ (2012), acc. Feb. 2, 2016.

  • Kuipers, S. D., Bramham, C. R., Cameron, H. A., et al., “Environmental control of adult neurogenesis: from hippocampal homeostasis to behavior and disease,” Neural Plast., 2014, 1–3 (2014).

    Article  Google Scholar 

  • Kumar, G., Jones, N. C., Morris, M. J., et al., “Early life stress enhancement of limbic epileptogenesis in adult rats: mechanistic insights,” PLoS One, 6, No. 9, e24033 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lajud, N. and Tomer L., “Early life stress and hippocampal neurogenesis in the neonate: sexual dimorphism, long term consequences and possible mediators,” Front. Mol. Neurosci., 8, 1–10 (2015).

    Article  Google Scholar 

  • Lajud, N., Roque, A., Cajero, M., et al., “Periodic maternal separation decreases hippocampal neurogenesis without affecting basal corticosterone during the stress hyporesponsive period, but alters HPA axis and coping behavior in adulthood,” Psychoneuroendocrinology, 37, No. 3, 410–420 (2012).

    Article  CAS  PubMed  Google Scholar 

  • Lewis, A. J., Galbally, M., Gannon, T., and Symeonides, C., “Early life programming as a target for prevention of child and adolescent mental disorders,” BMC Med., 12, 33: 1–15 (2014).

    Google Scholar 

  • Loi, M., Koricka, S., Lucassen, P. J., and Joels, M., “Age- and sex-dependent effects of early life stress on hippocampal neurogenesis,” Front. Endocrinol. (Lausanne), 5, 1–11 (2014).

  • Lyons, D. M., Parker, K. J., and Schatzberg, A. E., “Animal models of early life stress: implications for understanding resilience,” Dev. Psychobiol., 52, No. 7, 616–624 (2010).

    Article  PubMed  Google Scholar 

  • Malter Cohen, M., Jing, D., Yang, R. R., et al., “Early-life stress has persistent effects on amygdala function and development in mice and humans,” Proc. Natl. Acad. Sci. USA, 110, No. 45, 18274–18278 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  • Marmendal, M., Roman, E., Eriksson, C. J., et al., “Maternal separation alters maternal care, but has minor effects on behavior and brain opioid peptides in adult offspring,” Dev. Psychobiol., 45, No. 3, 140–152 (2004).

    Article  CAS  PubMed  Google Scholar 

  • McEwen, B. S., “Understanding the potency of stressful early life experiences on brain and body function,” Metabolism, 57, Suppl. 2, S11–S15 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKinney, W. T., “Overview of the past contributions of animal models and their changing place in psychiatry,” Semin. Clin. Neuropsychiatry, 6, No. 1, 68–78 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Meyer, U. and Feldon J., “Neural basis of psychosis-related behaviour in the infection model of schizophrenia,” Behav. Brain Res., 204, No. 2, 322–334 (2009).

    Article  CAS  PubMed  Google Scholar 

  • Meyer, U., Feldon, J., Schedlowski, M., and Yee, B. K., “Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia,” Neurosci. Biobehav. Rev., 29, No. 6, 913–947 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Migunova, Yu. V., “Abuse of children in families as a subject of sociological analysis,” Current Problems in Science and Edu cation, www.science-education.ru/Russia/article/view?id=12905, acc. Feb. 10, 2016.

  • Mirescu, C., Peters, J. D., and Gould, E., “Early life experience alters response of adult neurogenesis to stress,” Nat. Neurosci., 7, No. 8, 841–846 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Molet, J., Maras, P. M., Avishai-Eliner, S., and Baram, T. Z., “Naturalistic rodent models of chronic early-life stress,” Dev. Psychobiol., 56, No. 8, 1675–1688 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  • Moriceau, S., Shionoya, K., Jakubs, K., and Sullivan, R. M., “Early-life stress disrupts attachment learning: the role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine,” J. Neurosci., 29, No. 50: 15745–15755 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naninck, E. E., Hoemakers, L., Kakava-Georgiadou, N., et al., “Chronic early life stress alters developmental and adult neurogenesis and impairs cognitive function in mice,” Hippocampus, 25, No. 3, 309–328 (2015).

    Article  CAS  PubMed  Google Scholar 

  • Neigh, G. N., Owens, M. J., Taylor, W. R., and Nemeroff, C. B., “Changes in the vascular area fraction of the hippocampus and amygdala are induced by prenatal dexamethasone and/or adult stress,” J. Cereb. Blood Flow Metabolism., 30, No. 6, 1100–1104 (2010).

    Article  CAS  Google Scholar 

  • Nugent, N. R., Tyrka, A. R., Carpenter, L. L., and Price, L. H., “Gene-environment interactions: early life stress and risk for depressive and anxiety disorders,” Psychopharmacology (Berl.), 214, No. 1, 175–196 (2011).

    Article  CAS  Google Scholar 

  • Numbers of Minors Falling Victim to Criminal Assault, Federal State Statistics Service (Rosstat) (2000–2013), www.science-education.ru/Russia/article/view?id=12905, acc. Feb. 10, 2016.

  • Oomen, C. A., Girardi, C. E., Cahyadi, R., et al., “Opposite effects of early maternal deprivation on neurogenesis in male versus female rats,” PLoS One, 4, No. 1, e3675 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  • Oomen, C. A., Soeters, H., Audureau, N., et al., “Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood,” J. Neurosci., 30, No. 19, 6635–6645 (2010).

    Article  CAS  PubMed  Google Scholar 

  • Oomen, C. A., Soeters, H., Audureau, N., et al., “Early maternal deprivation affects dentate gyrus structure and emotional learning in adult female rats,” Psychopharmacology (Berl.), 214, No. 1, 249–260 (2011).

    Article  CAS  Google Scholar 

  • Orefice, L. L. and Heinrichs, S. C., “Paternal care paradoxically increases offspring seizure susceptibility in the El mouse model of epilepsy,” Epilepsy Behav., 12, No. 1, 234–241 (2008).

    Article  PubMed  Google Scholar 

  • Pechtel, P. and Pizzagalli, D. A., “Effects of early life stress on cognitive and affective function: an integrated review of human literature,” Psychopharmacology (Berl.), 214, No. 1, 55–70 (2011).

    Article  CAS  Google Scholar 

  • Pryce, C. R. and Seifritz, E., “A translational research framework for enhanced validity of mouse models of psychopathological states in depression,” Psychoneuroendocrinology, 36, No. 3, 308–329 (2011).

    Article  PubMed  Google Scholar 

  • Raceková, E., Lievajová, K., Danko, I., et al., “Maternal separation induced alterations of neurogenesis in the rat rostral migratory stream,” Cell. Mol. Neurobiol., 29, No. 6–7, 811–819 (2009).

    Article  PubMed  Google Scholar 

  • Raineki, C., Cortés, M. R., Belnoue, L., and Sullivan, R. M., “Effects of early-life abuse differ across development: infant social behavior deficits are followed by adolescent depressive-like behaviors mediated by the amygdala,” J. Neurosci., 32, No. 22: 7758–7765 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raineki, C., Moriceau, S., and Sullivan, R. M., “Developing a neurobehavioral animal model of infant attachment to an abusive caregiver,” Biol. Psychiatry, 67, No. 12: 1137–1145 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  • Rice, C. J., Sandman, C. A., Lenjavi, M. R., and Baram, T. Z., “A novel mouse model for acute and long-lasting consequences of early life stress,” Endocrinology, 149, No. 10, 4892–4900 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romero, E., Ali, C., Molina-Holgado, E., et al., “Neurobehavioral and immunological consequences of prenatal immune activation in rats. Influence of antipsychotics,” Neuropsychopharmacology, 32, No. 8, 1791–1804 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Salmina, A. B., Komleva, Yu. K., Kuvacheva, N. V., et al., “Molecular mechanisms of impairments to the development of the brain in preand neonatal period,” Vopr. Sovrem. Ped., No. 6, 15–20 (2012).

  • Salzberg, M., Kumar, G., Supit, L., et al., “Early postnatal stress confers enduring vulnerability to limbic epileptogenesis,” Epilepsia, 48, No. 11, 2079–2085 (2007).

    Article  PubMed  Google Scholar 

  • Schmidt, M. V., Wang, X. D., and Meijer, O. C., “Early life stress paradigms in rodents: potential animal models of depression?” Psychophar macology (Berl.), 214, No. 1, 131–140 (2011).

    Article  CAS  Google Scholar 

  • Schneider, T., Turczak, J., and Przewtocki, R., “Environmental enrichment reverses behavioral alterations in rats prenatally exposed to valproic acid: issues for a therapeutic approach in autism,” Neuropsychophar macology, 31, No. 1, 36–46 (2006).

    Article  CAS  Google Scholar 

  • Shanks, N., Windle R. J., Perks P. A., et al., “Early-life exposure to endotoxin alters hypothalamic-pituitary-adrenal function and predisposition to inflammation,” Proc. Natl Acad. Sci. USA, 97, No. 10: 5645–5650 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi, L., Fatemi, S. H., Sidwell, R. W., and Patterson, P. H., “Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring,” J. Neurosci., 23, No. 1, 297–302 (2003).

    PubMed  Google Scholar 

  • Suri, D., Veenit, V., Sarkar, A., et al., “Early stress evokes age-dependent biphasic changes in hippocampal neurogenesis, BDNF expression, and cognition,” Biol. Psychiatry, 73, No. 7, 658–666 (2013).

    Article  CAS  PubMed  Google Scholar 

  • Tanapat, P., Galea, L. A., and Gould, E., “Stress inhibits the proliferation of granule cell precursors in the developing dentate gyms,” Int. J. Dev. Neurosci., 16, No. 3–4, 235–239 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Tarry-Adkins, J. L. and Ozanne, S. E., “Mechanisms of early life programming: current knowledge and future directions,” Am. J. Clin. Nutr., 94, No. 6, Supplement, 1765S–1771S (2011).

  • Velíšek L., “Prenatal corticosteroid exposure alters early developmental seizures and behavior,” Epilepsy Res., 95, No. 1–2, 9–19 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, H. and Gondre-Lewis, M. C., “Prenatal nicotine and maternal deprivation stress de-regulate the development of CAL CA3, and dentate, gyrus neurons in hippocampus of infant rats,” PLoS One, 8, No. 6, e65517 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, X. D., Laivimaier, C., Holsboer, E., et al., “Early-life stress-induced anxiety-related behavior in adult mice partially requires forebrain corticotropin-releasing hormone receptor 1,” Eur. J. Neurosci., 36, No. 3, 2360–2367 (2012).

    Article  PubMed  Google Scholar 

  • Wolff, A. R. and Bilkey, D. K., “Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring,” Behav. Brain Res., 190, No. 1, 156–159 (2008).

    Article  CAS  PubMed  Google Scholar 

  • Yauzina, N. A., Cherepanov, S. M., Komleva, Yu. K., et al., “The effects of early life stress on behavior, neurogenesis, and apoptosis of brain cells in rats,” Sib. Med. Obozr., No. 5, 3–10 (2013b).

  • Yauzina, N. A., Komleva, Yu. K., Salmina, A. B., et al., “Current experimental models of depression,” Biomeditsina, No. 1, 61–71 (2013a).

  • Young, N. A., Teskey, G. C., Henry, L. C., and Edwards, H. E., “Exogenous antenatal glucocorticoid treatment reduces susceptibility for hippocampal kindled and maximal electroconvulsive seizures in infant rats,” Exp. Neurol., 198, No. 2, 303–312 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Yum, M. S., Chachua, T., Velíšková, J., and Velíšek, L., “Prenatal stress promotes development of spasms in infant rats,” Epilepsia, 53, No. 3, e46–e49 (2012).

    Article  CAS  PubMed  Google Scholar 

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Correspondence to N. A. Malinovskaya.

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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 66, No. 6, pp. 643–668, November–December, 2016.

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Malinovskaya, N.A., Morgun, A.V., Lopatina, O.L. et al. Early Life Stress: Consequences for the Development of the Brain. Neurosci Behav Physi 48, 233–250 (2018). https://doi.org/10.1007/s11055-018-0557-9

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