Различные экспериментальные модели в изучении влияния пренатальной гипоксии на развитие мозга

Авторы

DOI:

https://doi.org/10.33910/2687-1270-2022-3-4-432-454

Ключевые слова:

онтогенез, пренатальная гипоксия/ишемия, мозг, поведение, обучение

Аннотация

Проблема пренатальной гипоксии и отдаленных ее последствий является чрезвычайно актуальной с точки зрения механизмов развития различных патологических состояний. Исследования молекулярно-клеточных и эпигенетических механизмов, лежащих в основе нарушений поведения и способности к обучению, возникающих в результате действия повреждающих воздействий в критические периоды пренатального онтогенеза, невозможны без использования модельных экспериментов на животных, которые могут воспроизводить эмбриональное развитие человека, особенно развитие мозга плода. При изучении влияния пренатальной гипоксии-ишемии на животных используется большое количество протоколов, различающихся по виду и возрасту животных, по применяемому воздействию, его степени и продолжительности, а также по возрасту, когда происходит тестирование изучаемых параметров. В обзоре представлены различные модели на животных создания гипоксии/ишемии в различные периоды пре- и перинатального онтогенеза. Практически во всех рассматриваемых моделях показано отставание в развитии мозга, нарушения поведения и способности к обучению. Как правило, они связаны не столько с потерей нейронов у взрослых животных, как с изменениями их функциональной активности. Степень и направленность изменений на молекулярно-клеточном уровне зачастую бывает различной в зависимости от типа и сроков воздействия. Несмотря на большое количество исследований в этом направлении, полного понимания молекулярно-клеточных механизмов, лежащих в основе нарушений развития мозга вследствие воздействия пренатальной гипоксии, еще нет.

Библиографические ссылки

СПИСОК ЛИТЕРАТУРЫ

Аршавский, И. А. (1982) Физиологические механизмы и закономерности индивидуального развития. М.: Наука, 270 с.

Барашнев, Ю. И. (2000) Клинико-морфологическая характеристика и исходы церебральных расстройств при гипоксически-ишемических энцефалопатиях. Акушерство и гинекология, № 5, c. 39–42.

Васильев, Д. С., Туманова, Н. Л., Журавин, И. А. (2008) Структурные изменения в нервной ткани новой коры в онтогенезе крыс после гипоксии на разных сроках эмбриогенеза. Журнал эволюционной биохимии и физиологии, т. 44, № 3, c. 258–267.

Ватаева, Л. А., Тюлькова, Е. И., Алехин, А. Н., Стратилов, В. А. (2018) Влияние гипоксии или дексаметазона в различные сроки гестации на проявление условно-рефлекторного страха у взрослых крыс. Журнал эволюционной биохимии и физиологии, т. 54, № 6, с. 392–398. https://doi.org/10.1134/S0044452918060037

Ветровой, О. В., Нимирицкий, П. П., Тюлькова, Е. И., Рыбникова, Е. А. (2020) Содержание и активность гипоксия-индуцируемого фактора HIF1α увеличены в гиппокампе новорожденных крысят, переживших пренатальную гипоксию на 14–16 сутки эмбриогенеза. Нейрохимия, т. 37, № 3, с. 228–232. https://doi.org/10.31857/S1027813320030127

Дубровская, Н. М., Журавин, И. А. (2008) Онтогенетические особенности поведения крыс, перенесших гипоксию на 14-е или 18-е сутки эмбриогенеза. Журнал высшей нервной деятельности им. И. П. Павлова, т. 58, № 6, с. 718–727.

Журавин, И. А., Туманова, Н. Л., Васильев, Д. С. (2009) Структурные изменения нервной ткани гиппокампа в онтогенезе крыс после пренатальной гипоксии. Журнал эволюционной биохимии и физиологии, т. 45, № 1, с. 138–140.

Отеллин, В. А. (2003) Формирование патологий головного мозга в эмбриональный период. Природа, № 9, с. 30–35.

Отеллин, В. А., Хожай, Л. И., Ватаева, Л. А. (2012) Влияние гипоксии в раннем пренатальном онтогенезе на поведение и структурные характеристики головного мозга. Журнал эволюционной биохимии и физиологии, т. 48, № 5, с. 467–473.

Отеллин, В. А., Хожай, Л. И., Шишко, Т. Т., Вершинина, Е. А. (2021) Ультраструктура ядрышек нейронов сенсомоторной области неокортекса крыс в неонатальный период после воздействия перинатальной гипоксии и фармакологической коррекции. Журнал эволюционной биохимии и физиологии, т. 57, № 6, с. 494–499. https://doi.org/10.31857/S0044452921050065

Резников, К. Ю. (1981) Пролиферация клеток мозга позвоночных в условиях нормального развития мозга и при его травме. М.: Наука, 149 с.

Стратилов, В. А., Ветровой, О. В., Ватаева, Л. А., Тюлькова, Е. И. (2021) Ассоциированные с возрастом изменения в исследовательской активности в тесте «Открытое поле» у крыс, переживших пренатальную гипоксию. Журнал высшей нервной деятельности им. И. П. Павлова, т. 71, № 3, с. 428–436. https://doi.org/10.31857/S0044467721030102

Тюлькова, Е. И., Ватаева, Л. А., Ветровой, О. В., Романовский, Д. Ю. (2015) Пренатальная гипоксия модифицирует рабочую память и активность полифосфоинозитидной системы гиппокампа крыс. Журнал эволюционной биохимии и физиологии, т. 51, № 2, с. 115–121.

Тюлькова, Е. И., Ватаева, Л. А., Стратилов, В. А. и др. (2020) Особенности метилирования ДНК и гистона Н3 в гиппокампе и неокортексе крыс, переживших патологические воздействия в пренатальном периоде развития. Нейрохимия, т. 37, № 1, с. 64–74. https://doi.org/10.31857/S1027813320010197

Barker, D. J. (2004) Developmental origins of adult health and disease. Journal of Epidemiology and Community Health, vol. 58, no. 2, pp. 114–115. https://doi.org/10.1136/jech.58.2.114

Barker, D. J., Osmond, C., Kajantie, E., Eriksson, J. G. (2009) Growth and chronic disease: Findings in the Helsinki birth cohort. Annals of Human Biology, vol. 36, no. 5, pp. 445–458. https://doi.org/10.1080/03014460902980295

Baud, O., Daire, J.-L., Dalmaz, Y. et al. (2004) Gestational hypoxia induces white matter damage in neonatal rats: A new model of periventricular leukomalacia. Brain Pathology, vol. 14, no. 1, pp. 1–10. https://doi.org/10.1111/j.1750-3639.2004.tb00492.x

Bayer, S. A. (1980) Development of the hippocampal region in the rat I. Neurogenesis examined with 3H-thymidine autoradiography. The Journal of Comparative Neurology, vol. 190, no. 1, pp. 87–114. https://doi.org/10.1002/cne.901900107

Bayer, S. A., Altman, J., Russo, R. J., Zhang, X. (1993) Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology, vol. 14, no. 1, pp. 83–144. https://pubmed.ncbi.nlm.nih.gov/8361683

Bennet, L., Davidson, J. O., Koome, M., Gunn, A. J. (2012) Glucocorticoids and preterm hypoxic-ischemic brain injury: The good and the bad. Journal of Pregnancy, vol. 2012, article 751694. https://doi.org/10.1155/2012/751694

Blutstein, T., Castello, M. A., Viechweg, S. S. et al. (2013) Differential responses of hippocampal neurons and astrocytes to nicotine and hypoxia in the fetal guinea pig. Neurotoxic Research, vol. 24, no. 1, pp. 80–93. https://doi.org/10.1007/s12640-012-9363-2

Buss, C., Davis, E. P., Shahbaba, B. et al. (2012) Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 20, pp. E1312–E1319. https://doi.org/10.1073/pnas.1201295109

Cai, Z., Xiao, F., Lee, B. et al. (1999) Prenatal hypoxia-ischemia alters expression and activity of nitric oxide synthase in the young rat brain and causes learning deficits. Brain Research Bulletin, vol. 49, no. 5, pp. 359–365. https://doi.org/10.1016/s0361-9230(99)00076-3

Calkins, K., Devaskar, S. U. (2011) Fetal origins of adult disease. Current Problems in Pediatric and Adolescent Health Care, vol. 41, no. 6, pp. 158–176. https://doi.org/10.1016/j.cppeds.2011.01.001

Camm, E. J., Cross, C. M., Kane, A. D. et al. (2021) Maternal antioxidant treatment protects adult offspring against memory loss and hippocampal atrophy in a rodent model of developmental hypoxia. The FASEB Journal, vol. 35, article e21477. https://doi.org/10.1096/fj.202002557RR

Camm, E. J., Gibbs, M. E., Harding, R. (2001) Restriction of prenatal gas exchange impairs memory consolidation in the chick. Developmental Brain Research, vol. 132, no. 2, pp. 141–150. https://doi.org/10.1016/s0165-3806(01)00305-4

Camm, E. J., Gibbs, M. E., Harding, R. et al. (2005) Prenatal hypoxia impairs memory function but does not result in overt structural alterations in the postnatal chick brain. Developmental Brain Research, vol. 160, no. 1, pp. 9–18. https://doi.org/10.1016/j.devbrainres.2005.07.015

Chen, Q., Zhang, F., Wang, Y. et al. (2015) The transcription factor c-Myc suppresses MiR-23b and MiR-27b transcription during fetal distress and increases the sensitivity of neurons to hypoxia-induced apoptosis. PLoS One, vol. 10, no. 3, article e0120217. https://doi.org/10.1371%2Fjournal.pone.0120217

Chung, Y., So, K., Kim, E. et al. (2015) Immunoreactivity of neurogenic factor in the guinea pig brain after prenatal hypoxia. Annals of Anatomy, vol. 200, pp. 66–72. https://doi.org/10.1016/j.aanat.2015.02.003

Coq, J.-O., Delcour, M., Massicotte, V. S. et al. (2016) Prenatal ischemia deteriorates white matter, brain organization, and function: Implications for prematurity and cerebral palsy. Developmental Medicine & Child Neurology, vol. 58, no. 4, pp. 7–11. https://doi.org/10.1111/dmcn.13040

De Boo, H. A., Harding, J. E. (2006) The developmental origins of adult disease (Barker) hypothesis. Australian and New Zealand Journal of Obstetrics and Gynaecology, vol. 46, no. 1, pp. 4–14. https://doi.org/10.1111/j.1479-828X.2006.00506.x

De Courten-Myers, G. M., Xi, G., Hwang, J. H. al. (2000) Hypoglycemic brain injury: Potentiation from respiratory depression and injury aggravation from hyperglycemic treatment overshoots. Journal of Cerebral Blood Flow & Metabolism, vol. 20, no. 1, pp. 82–92. https://doi.org/10.1097/00004647-200001000-00012

Dehay, C., Kennedy, H. (2007) Cell-cycle control and cortical development. Nature Reviews Neuroscience, vol. 8, no. 6, pp. 438–450. https://doi.org/10.1038/nrn2097

Delcour, M., Olivier, P., Chambon, C. et al. (2012a) Neuroanatomical, sensorimotor and cognitive deficits in adult rats with white matter injury following prenatal ischemia. Brain Pathology, vol. 22, no. 1, pp. 1–16. https://doi.org/10.1111/j.1750-3639.2011.00504.x

Delcour, M., Russier, M., Amin, M. et al. (2012b) Impact of prenatal ischemia on behavior, cognitive abilities and neuroanatomy in adult rats with white matter damage. Behavioural Brain Research, vol. 232, no. 1, pp. 233–244. https://doi.org/10.1016/j.bbr.2012.03.029

Delcour, M., Russier, M., Xin, D. L. et al. (2011) Mild musculoskeletal and locomotor alterations in adult rats with white matter injury following prenatal ischemia. International Journal of Developmental Neuroscience, vol. 29, no. 6, pp. 593–607. https://doi.org/10.1016/j.ijdevneu.2011.02.010

Derrick, M., Luo, N. L., Bregman, J. C. et al. (2004) Preterm fetal hypoxia-ischemia causes hypertonia and motor deficits in the neonatal rabbit: A model for human cerebral palsy? Journal of Neuroscience, vol. 24, no. 1, pp. 24–34. https://doi.org/10.1523/jneurosci.2816-03.2004

Dobbing, J. (1968) Vulnerable periods in developing brain. In: A. N. Davison, J. Dobbing (eds.). Applied neurochemistry. Oxford: Blackwell Publ., pp. 287–316.

Du Plessis, A. J., Volpe, J. J. (2002) Perinatal brain injury in the preterm and term newborn. Current Opinion in Neurology, vol. 15, no. 2, pp. 151–157. https://doi.org/10.1097/00019052-200204000-00005

Dudley, K. J., Li, X., Kobor, M. S. et al. (2011) Epigenetic mechanisms mediating vulnerability and resilience to psychiatric disorders. Neuroscience & Biobehavioral Reviews, vol. 35, no. 7, pp. 1544–1551. https://doi.org/10.1016/j.neubiorev.2010.12.016

Eskild, A., Strøm-Roum, E. M., Haavaldsen, C. (2016) Does the biological response to fetal hypoxia involve angiogenesis, placental enlargement and preeclampsia? Paediatric and Perinatal Epidemiology, vol. 30, no. 3, pp. 305–309. https://doi.org/10.1111/ppe.12283

Getahun, D., Rhoads, G. G., Demissie, K. et al. (2013) In utero exposure to ischemic-hypoxic conditions and attention-deficit/hyperactivity disorder. Pediatrics, vol. 131, no. 1, pp. e53–e61. https://doi.org/10.1542/peds.2012-1298

Giannopoulou, I., Pagida, M. A., Briana, D. D., Panayotacopoulou, M. T. (2018) Perinatal hypoxia as a risk factor for psychopathology later in life: The role of dopamine and neurotrophins. Hormones, vol. 17, no. 1, pp. 25–32. https://doi.org/10.1007/s42000-018-0007-7

Gilbert, J. S., Babcock, S. A., Granger, J. P. (2007) Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension, vol. 50, no. 6, pp. 1142–1147. https://doi.org/10.1161/HYPERTENSIONAHA.107.096594

Gluckman, P. D., Hanson, M. A. (2004) Living with the past: Evolution, development, and patterns of disease. Science, vol. 305, no. 5691, pp. 1733–1736. https://doi.org/10.1126/science.1095292

Gluckman, P. D., Hanson, M. A., Cooper, C., Thornburg, K. L. (2008) Effect of in utero and early-life conditions on adult health and disease. New England Journal of Medicine, vol. 359, no. 1, pp. 61–73. https://doi.org/10.1056/NEJMra0708473

Golan, H., Huleihel, M. (2006) The effect of prenatal hypoxia on brain development: Short- and long-term consequences demonstrated in rodent models. Developmental Science, vol. 9, no. 4, pp. 338–349. https://doi.org/10.1111/j.1467-7687.2006.00498.x

Golan, H., Kashtuzki, I., Hallak, M. et al. (2004) Maternal hypoxia during pregnancy induces fetal neurodevelopmental brain damage: Partial protection by magnesium sulfate. Journal of Neuroscience Research, vol. 78, no. 3, pp. 430–441. https://doi.org/10.1002/jnr.20269

Golan, M. H., Mane, R., Molczadzki, G. et al. (2009) Impaired migration signaling in the hippocampus following prenatal hypoxia. Neuropharmacology, vol. 57, no. 5-6, pp. 511–522. https://doi.org/10.1016/j.neuropharm.2009.07.028

Gonzalez-Rodriguez, P. J., Xiong, F., Li, Y. et al. (2014) Fetal hypoxia increases vulnerability of hypoxic-ischemic brain injury in neonatal rats: Role of glucocorticoid receptors. Neurobiology of Disease, vol. 65, pp. 172–179. https://doi.org/10.1016/j.nbd.2014.01.020

Gopagondanahalli, K. R., Li, J., Fahey, M. C. et al. (2016) Preterm hypoxic-ischemic encephalopathy. Frontiers in Pediatrics, vol. 4, article 114. https://doi.org/10.3389/fped.2016.00114

Graf, A. V., Maslova, M. V., Artiukhov, A. V. et al. (2022) Acute prenatal hypoxia in rats affects physiology and brain metabolism in the offspring, dependent on sex and gestational. International Journal of Molecular Sciences, vol. 23, no. 5, article 2579. https://doi.org/10.3390/ijms23052579

Granger, J. P., LaMarca, B. B. D., Cockrell, K. et al. (2006) Reduced uterine perfusion pressure (RUPP) model for studying cardiovascular-renal dysfunction in response to placental ischemia. In: M. J. Soares, J. S. Hunt (eds.). Placenta and Trophoblast. Methods in Molecular Medicine. Vol. 122. Totowa: Humana Press Publ., pp. 383–392. https://doi.org/10.1385/1-59259-989-3:381

Harris, A., Seckl, J. (2011) Glucocorticoids, prenatal stress and the programming of disease. Hormones and Behavior, vol. 59, no. 3, pp. 279–289. https://doi.org/10.1016/j.yhbeh.2010.06.007

Herlenius, E., Lagercrantz, H. (2004) Development of neurotransmitter systems during critical periods. Experimental Neurology, vol. 190, no. 1, pp. S8–S21. https://doi.org/10.1016/j.expneurol.2004.03.027

Hompes, T., Vrieze, E., Fieuws, S. et al. (2012) The influence of maternal cortisol and emotional state during pregnancy on fetal intrauterine growth. Pediatric Research, vol. 72, no. 3, pp. 305–315. https://doi.org/10.1038/pr.2012.70

Inder, T. E., Volpe, J. J. (2000) Mechanisms of perinatal brain injury. Seminars in Neonatology, vol. 5, no. 1, pp. 3–16. https://doi.org/10.1053/siny.1999.0112

Jansson, T., Powell, T. L. (2007) Role of the placenta in fetal programming: Underlying mechanisms and potential interventional approaches. Clinical Science, vol. 113, no. 1, pp. 1–13. https://doi.org/10.1042/CS20060339

Jantzie, L. L., Corbett, C. J., Firl, D. J., Robinson, S. (2015) Postnatal erythropoietin mitigates impaired cerebral cortical development following subplate loss from prenatal hypoxia-ischemia. Cerebral Cortex, vol. 25, no. 9, pp. 2683–2695. https://doi.org/10.1093/cercor/bhu066

Jia, L., Wang, J., Cao, H. et al. (2020) Activation of PGC-1α and mitochondrial biogenesis protects against prenatal hypoxicischemic. Brain Injury. Neuroscience, vol. 432, pp. 63–72. https://doi.org/10.1016/j.neuroscience.2020.02.035

Katz, J. M., Pacia, S. V., Devinsky, O. (2001) Current management of epilepsy and pregnancy: Fetal outcome, congenital malformations, and developmental delay. Epilepsy & Behavior, vol. 2, no. 2, pp. 119–123. https://doi.org/10.1006/ebeh.2001.0158

Kimball, R., Wayment, M., Merrill, D. et al. (2015) Hypoxia reduces placental mTOR activation in a hypoxia-induced model of intrauterine growth restriction (IUGR). Physiological Reports, vol. 3, no. 12, article e12651. https://doi.org/10.14814/phy2.12651

Kubo, K. I., Deguchi, K., Nagai, T. et al. (2017) Association of impaired neuronal migration with cognitive deficits in extremely preterm infants. JCI Insight, vol. 2, no. 10, article e88609. https://doi.org/10.1172/jci.insight.88609

Langley-Evans, S. C., McMullen, S. (2010) Developmental origins of adult disease. Medical Principles and Practice, vol. 19, no. 2, pp. 87–98. https://doi.org/10.1159/000273066

Lawrence, K. M., McGovern, P. E., Mejaddam, A. et al. (2019) Chronic intrauterine hypoxia alters neurodevelopment in fetal sheep. Journal of Thoracic and Cardiovascular Surgery, vol. 157, no. 5, pp. 1982–1991. https://doi.org/10.1016%2Fj.jtcvs.2018.12.093

Leonard, C. T., Goldberger, M. E. (1987) Consequences of damage to the sensomotor cortex in neonatal and adult cats. I. Sparing and recovery of function. Developmental Brain Research, vol. 32, no. 1, pp. 1–14. https://doi.org/10.1016/0165-3806(87)90133-7

Li, Y., Gonzalez, P., Zhang, L. (2012) Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: Mechanisms and possible interventions. Progress in Neurobiology, vol. 98, no. 2, pp. 145–165. https://doi.org/10.1016/j.pneurobio.2012.05.010

Louzoun-Kaplan, V., Zuckerman, M., Perez-Polo, J. R., Golan, H. M. (2008) Prenatal hypoxia down regulates the GABA pathway in newborn mice cerebral cortex; partial protection by MgSO4. International Journal of Developmental Neuroscience, vol. 26, no. 1, pp. 77–85. https://doi.org/10.1016/j.ijdevneu.2007.09.002

Ma, Q., Zhang, L. (2015) Epigenetic programming of hypoxic-ischemic encephalopathy in response to fetal hypoxia. Progress in Neurobiology, vol. 124, pp. 28–48. https://doi.org/10.1016/j.pneurobio.2014.11.001

Mach, M., Dubovicky, M., Navarová, J. et al. (2006) Vitamin E supplementation in phenytoin induced developmental toxicity in rats: Postnatal study. Neuro Endocrinology Letters, vol. 27, no. 2, pp. 69–73. https://pubmed.ncbi.nlm.nih.gov/17159783

Maresová, D., Valkounová, I., Jandová, K. et al. (2001) Excitability changes of cortical neurons during the postnatal period in rats exposed to prenatal hypobaric hypoxia. Physiological Research, vol. 50, no. 2, pp. 215–219. https://pubmed.ncbi.nlm.nih.gov/11522050

Mazur, M., Miller, R. H., Robinson, S. (2010) Postnatal erythropoietin treatment mitigates neural cell loss after systemic prenatal hypoxic-ischemic injury. Journal of Neurosurgery: Pediatrics, vol. 6, no. 3, pp. 206–221. https://doi.org/10.3171/2010.5.PEDS1032

McClendon, E., Shaver, D. C., Degener-O’Brien, K. et al. (2017) Transient hypoxemia chronically disrupts maturation of preterm fetal ovine subplate neuron arborization and activity. Journal of Neuroscience, vol. 37, no. 49, pp. 11912–11929. https://doi.org/10.1523/JNEUROSCI.2396-17.2017

McGovern, P. E., Lawrence, K., Baumgarten, H. et al. (2020) Ex utero extracorporeal support as a model for fetal hypoxia and brain dysmaturity. The Annals of Surgery, vol. 109, no. 3, pp. 810–819. https://doi.org/10.1016/j.athoracsur.2019.08.021

Miller, S. L., Huppi, P. S., Mallard, C. (2016) The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome. The Journal of Physiology, vol. 594, no. 4, pp. 807–823. https://doi.org/10.1113/jp271402

Miranda, A., Sousa, N. (2018) Maternal hormonal milieu influence on fetal brain development. Brain and Behavior, vol. 8, no. 2, article e00920. https://doi.org/10.1002/brb3.920

Moisiadis, V. G., Matthews, S. G. (2014a) Glucocorticoids and fetal programming part 1: Outcomes. Nature Reviews Endocrinology, vol. 10, no. 7, pp. 391–402. https://doi.org/10.1038/nrendo.2014.73

Moisiadis, V. G., Matthews, S. G. (2014b) Glucocorticoids and fetal programming part 2: Mechanisms. Nature Reviews Endocrinology, vol. 10, no. 7, pp. 403–411. https://doi.org/10.1038/nrendo.2014.74

Mujsce, D. J., Christensen, M. A., Vannucci, R. C. (1990) Cerebral blood flow and edema in perinatal hypoxic-ischemic brain damage. Pediatric Research, vol. 27, no. 5, pp. 450–453. https://doi.org/10.1203/00006450-199005000-00007

Nalivaeva, N. N., Turner, A. J., Zhuravin, I. A. (2018) Role of prenatal hypoxia in brain development, cognitive functions, and neurodegeneration. Frontiers in Neuroscience, vol. 12, article 825. https://doi.org/10.3389/fnins.2018.00825

Nardozza, L. M. M., Caetano, A. C. R., Zamarian, A. C. P. et al. (2017) Fetal growth restriction: Current knowledge. Archives of Gynecology and Obstetrics, vol. 295, no. 5, pp. 1061–1077. https://doi.org/10.1007/s00404-017-4341-9

Nyakas, C., Buwalda, B., Luiten, P. G. M. (1996) Hypoxia and brain development. Progress in Neurobiology, vol. 49, no. 1, pp. 1–51. https://doi.org/10.1016/0301-0082(96)00007-x

Ohshima, M., Coq, J.-O., Otani, K. et al. (2016) Mild intrauterine hypoperfusion reproduces neurodevelopmental disorders observed in prematurity. Scientific Reports, vol. 6, article 39377. https://doi.org/10.1038/srep39377

Olivier, P., Baud, O., Evrard, P. et al. (2005) Prenatal ischemia and white matter damage in rats. Journal of Neuropathology & Experimental Neurology, vol. 64, no. 11, pp. 998–1006. https://doi.org/10.1097/01.jnen.0000187052.81889.57

Owens, E. B., Hinshaw, S. P. (2013) Perinatal problems and psychiatric comorbidity among children with ADHD. Journal of Clinical Child & Adolescent Psychology, vol. 42, no. 6, pp. 762–768. https://doi.org/10.1080/15374416.2013.785359

Patterson, A. J., Zhang, L. (2010) Hypoxia and fetal heart development. Current Molecular Medicine, vol. 10, no. 7, pp. 653–666. https://doi.org/10.2174/156652410792630643

Peyronnet, J., Roux, J. C., Géloën, A. et al. (2000) Prenatal hypoxia impairs the postnatal development of neural and functional chemoafferent pathway in rat. Journal of Physiology, vol. 524, no. 2, pp. 525–537. https://doi.org/10.1111/j.1469-7793.2000.00525.x

Phillips, T. J., Scott, H., Menassa, D. A. et al. (2017) Treating the placenta to prevent adverse effects of gestational hypoxia on fetal brain development. Scientific Reports, vol. 7, article 9079. https://doi.org/10.1038/s41598-017-06300-1

Piešová, M., Mach, M. (2020) Impact of perinatal hypoxia on the developing brain. Physiological Research, vol. 69, no. 2, pp. 199–213. https://doi.org/10.33549/physiolres.934198

Pryce, C. R. (2008) Postnatal ontogeny of expression of the corticosteroid receptor genes in mammalian brains: Inter-species and intra-species differences. Brain Research Reviews, vol. 57, no. 2, pp. 596–605. https://doi.org/10.1016/j.brainresrev.2007.08.005

Rice, D., Barone, S. (2000) Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environmental Health Perspectives, vol. 108, no. 3, pp. 511–533. https://doi.org/10.1289/ehp.00108s3511

Rice, J. E., Vannucci, R. C., Brierley, J. B. (1981) The influence of immaturity on hypoxic-ischemic brain damage in the rat. Annals of Neurology, vol. 9, no. 2, pp. 131–141. https://doi.org/10.1002/ana.410090206

Robinson, S., Petelenz, K., Li, Q. et al. (2005) Developmental changes induced by graded prenatal systemic hypoxic-ischemic insults in rats. Neurobiology of Disease, vol. 18, no. 3, pp. 568–581. https://doi.org/10.1016/j.nbd.2004.10.024

Roland, E. H., Poskitt, K., Rodriguez, E. et al. (1998) Perinatal hypoxic-ischemic thalamic injury: Clinical features and neuroimaging. Annals of Neurology, vol. 44, no. 2, pp. 161–166. https://doi.org/10.1002/ana.410440205

Sab, I. M., Ferraz, M. M., Amaral, T. A. et al. (2013) Prenatal hypoxia, habituation memory and oxidative stress. Pharmacology Biochemistry & Behavior, vol. 107, pp. 24–28. https://doi.org/10.1016/j.pbb.2013.04.004

Shchelchkova, N. A., Kokaya, A. A., Bezhenar’, V. F. et al. (2020) The role of brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor in chronic fetal oxygen deprivation. Modern Technologies in Medicine, vol. 12, no. 1, pp. 25–31. https://doi.org/10.17691/stm2020.12.1.03

Sheldon, R. A., Sedik, C., Ferriero, D. M. (1998) Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Research, vol. 810, no. 1-2, pp. 114–122. https://doi.org/10.1016/s0006-8993(98)00892-0

Shen, G., Hu, S., Zhao, Z. et al. (2020) Antenatal hypoxia accelerates the onset of Alzheimer’s disease pathology in 5xFAD mouse model. Frontiers in Aging Neuroscience, vol. 12, article 251. https://doi.org/10.3389/fnagi.2020.00251

Skogen, J. C., Øverland, S. (2012) The fetal origins of adult disease: A narrative review of the epidemiological literature. JRSM Short Reports, vol. 3, no. 8, pp. 1–7. https://doi.org/10.1258/shorts.2012.012048

So, K., Chung, Y., Yu, S.-K., Jun, Y. (2017) Regional immunoreactivity of Pax6 in the neurogenic zone after chronic prenatal hypoxia. In Vivo, vol. 31, no. 6, pp. 1125–1129. https://doi.org/10.21873/invivo.11178

Sosedova, L. M., Vokina, V. A., Kapustina, E. A. (2019) Contribution of fetal programming in the formation of cognitive impairments induced by lead poisoning in white rats. Bulletin of Experimental Biology and Medicine, vol. 166, no. 5, pp. 617–621. https://doi.org/10.1007/s10517-019-04404-4

Togher, K. L., O’Keeffe, M. M., Khashan, A. S. et al. (2014) Epigenetic regulation of the placental HSD11B2 barrier and its role as a critical regulator of fetal development. Epigenetics, vol. 9, no. 6. pp. 816–822. https://doi.org/10.4161/epi.28703

Towfighi, J., Zec, N., Yager, J. et al. (1995) Temporal evolution of neuropathologic changes in an immature rat model of cerebral hypoxia: A light microscopic study. Acta Neuropathologica, vol. 90, no. 4, pp. 375–386. https://doi.org/10.1007/BF00315011

Tuor, U. I., Del Bigio, M. R., Chumas, P. D. (1996) Brain damage due to cerebral hypoxia/ischemia in the neonate: Pathology and pharmacological modification. Cerebrovascular & Brain Metabolism Review, vol. 8, no. 2, pp. 159–193. https://pubmed.ncbi.nlm.nih.gov/8727185

Ujhazy, E., Dubovicky, M., Navarova, J. et al. (2013) Subchronic perinatal asphyxia in rats: Embryo-foetal assessment of a new model of oxidative stress during critical period of development. Food and Chemical Toxicology, vol. 61, pp. 233–239. https://doi.org/10.1016/j.fct.2013.07.023

Vannucci, R. C. (2000) Hypoxic-ischemic encephalopathy. American Journal of Perinatology, vol. 17, no. 3, pp. 113–120. https://doi.org/10.1055/s-2000-9293

Vannucci, R. C., Connor, J. R., Mauger, D. T. et al. (1999) Rat model of perinatal hypoxic-ischemic brain damage. Journal of Neuroscience Research, vol. 55, no. 2, pp. 158–163. https://doi.org/10.1002/(SICI)1097-4547(19990115)55:2<158::AID-JNR3>3.0.CO;2-1

Vannucci, C. R., Perlman, J. M. (1997) Interventions for perinatal hypoxic-ischemic encephalopathy. Pediatrics, vol. 100, no. 6, pp. 1004–1014. https://doi.org/10.1542/peds.100.6.1004

Vannucci, R. C., Vannucci, S. J. (2005) Perinatal hypoxic-ischemic brain damage: Evolution of an animal model. Developmental Neuroscience, vol. 27, no. 2-4, pp. 81–86. https://doi.org/10.1159/000085978

Vasilev, D. S., Dubrovskaya, N. M., Tumanova, N. L., Zhuravin, I. A. (2016) Prenatal hypoxia in different periods of embryogenesis differentially affects cell migration, neuronal plasticity, and rat behavior in postnatal ontogenesis. Frontiers in Neuroscience, vol. 10, article 126. https://doi.org/10.3389/fnins.2016.00126

Vetrovoy, O., Stratilov, V., Nimiritsky, P. et al. (2021) Prenatal hypoxia induces premature aging accompanied by disturbed function of glutamatergic system in rat hippocampus. Neurochemical Research, vol. 46, no. 3, pp. 550–563. https://doi.org/10.1007/s11064-020-03191-z

Vetrovoy, O., Tyulkova, E., Stratilov, V. et al. (2020) Long-term effects of prenatal severe hypoxia on central and peripheral components of the glucocorticoid system in rats. Developmental Neuroscience, vol. 42, no. 2-4, pp. 145–158. https://doi.org/10.1159/000512223

Volpe, J. J. (1992) Brain injury in the premature infant—current concepts of pathogenesis and prevention. Biology of the Neonate, vol. 62, no. 4, pp. 231–242. https://doi.org/10.1159/000243876

Waffarn, F., Davis, E. P. (2012) Effects of antenatal corticosteroids on the hypothalamic-pituitary-adrenocortical axis of the fetus and newborn: Experimental findings and clinical considerations. American Journal of Obstetrics and Gynecology, vol. 207, no. 6, pp. 446–454. https://doi.org/10.1016/j.ajog.2012.06.012

Wang, X., Meng, F.-S., Liu, Z.-Y. et al. (2013) Gestational hypoxia induces sex-differential methylation of Crhr1 linked to anxiety-like behavior. Molecular Neurobiology, vol. 48, no. 3, pp. 544–555. https://doi.org/10.1007/s12035-013-8444-4

Wang, W.-T., Lee, P., Dong, Y. et al. (2016) In vivo neurochemical characterization of developing guinea pigs and the effect of chronic fetal hypoxia. Neurochemical Research, vol. 41, no. 7, pp. 1831–1843. https://doi.org/10.1007/s11064-016-1924-y

Warner, M. J., Ozanne, S. E. (2010) Mechanisms involved in the developmental programming of adulthood disease. Biochemical Journal, vol. 427, no. 3, pp. 333–347. https://doi.org/10.1042/bj20091861

Wei, B., Li, L., He, A. et al. (2016) Hippocampal NMDAR-Wnt-Catenin signaling disrupted with cognitive deficits in adolescent offspring exposed to prenatal hypoxia. Brain Research, vol. 1631, pp. 157–164. https://doi.org/10.1016/j.brainres.2015.11.041

Xiong, F., Zhang, L. (2013) Role of the hypothalamic-pituitary-adrenal axis in developmental programming of health and disease. Frontiers in Neuroendocrinology, vol. 34, no. 1, pp. 27–46. https://doi.org/doi:10.1016/j.yfrne.2012.11.002

Zamudio, S. (2003) The placenta at high altitude. High Altitude Medicine & Biology, vol. 4, no. 2, pp. 171–191. https://doi.org/10.1089/152702903322022785

Zhao, T., Zhang, C. P., Liu, Z. H. et al. (2008) Hypoxia-driven proliferation of embryonic neural stem⁄progenitor cells—role of hypoxia-inducible transcription factor-1α. FEBS Journal, vol. 275, no. 8, pp. 1824–1834. https://doi.org/10.1111/j.1742-4658.2008.06340.x

Zhuravin, I. A., Dubrovskaya, N. M., Vasilev, D. S. et al. (2019). Prenatal hypoxia produces memory deficits associated with impairment of long-term synaptic plasticity in young rats. Neurobiology of Learning and Memory, vol. 164, article 107066. https://doi.org/10.1016/j.nlm.2019.107066

REFERENCES

Arshavskij, I. A. (1982) Fiziologicheskie mekhanizmy i zakonomernosti individual’nogo razvitiya [Physiological mechanisms and patterns of individual development]. Moscow: Nauka Publ., 270 p. (In Russian)

Barashnev, Yu. I. (2000) Kliniko-morfologicheskaya kharakteristika i iskhody tserebral’nykh rasstrojstv pri gipoksicheski-ishemicheskikh entsefalopatiyakh [Clinical and morphological characteristics and outcomes of cerebral disorders in hypoxic-ischemic encephalopathies]. Akusherstvo i ginekologiya — Obstetrics and Gynecology, no. 5, pp. 39–42. (In Russian)

Barker, D. J. (2004) Developmental origins of adult health and disease. Journal of Epidemiology and Community Health, vol. 58, no. 2, pp. 114–115. https://doi.org/10.1136/jech.58.2.114 (In English)

Barker, D. J., Osmond, C., Kajantie, E., Eriksson, J. G. (2009) Growth and chronic disease: Findings in the Helsinki birth cohort. Annals of Human Biology, vol. 36, no. 5, pp. 445–458. https://doi.org/10.1080/03014460902980295 (In English)

Baud, O., Daire, J.-L., Dalmaz, Y. et al. (2004) Gestational hypoxia induces white matter damage in neonatal rats: A new model of periventricular leukomalacia. Brain Pathology, vol. 14, no. 1, pp. 1–10. https://doi.org/10.1111/j.1750-3639.2004.tb00492.x (In English)

Bayer, S. A. (1980) Development of the hippocampal region in the rat I. Neurogenesis examined with 3H-thymidine autoradiography. The Journal of Comparative Neurology, vol. 190, no. 1, pp. 87–114. https://doi.org/10.1002/cne.901900107 (In English)

Bayer, S. A., Altman, J., Russo, R. J., Zhang, X. (1993) Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology, vol. 14, no. 1, pp. 83–144. https://pubmed.ncbi.nlm.nih.gov/8361683 (In English)

Bennet, L., Davidson, J. O., Koome, M., Gunn, A. J. (2012) Glucocorticoids and preterm hypoxic-ischemic brain injury: The good and the bad. Journal of Pregnancy, vol. 2012, article 751694. https://doi.org/10.1155/2012/751694 (In English)

Blutstein, T., Castello, M. A., Viechweg, S. S. et al. (2013) Differential responses of hippocampal neurons and astrocytes to nicotine and hypoxia in the fetal guinea pig. Neurotoxic Research, vol. 24, no. 1, pp. 80–93. https://doi.org/10.1007/s12640-012-9363-2 (In English)

Buss, C., Davis, E. P., Shahbaba, B. et al. (2012) Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 20, pp. E1312–E1319. https://doi.org/10.1073/pnas.1201295109 (In English)

Cai, Z., Xiao, F., Lee, B. et al. (1999) Prenatal hypoxia-ischemia alters expression and activity of nitric oxide https://doi.org/10.1016/s0361-9230(99)00076-3 (In English)

Calkins, K., Devaskar, S. U. (2011) Fetal origins of adult disease. Current Problems in Pediatric and Adolescent Health Care, vol. 41, no. 6, pp. 158–176. https://doi.org/10.1016/j.cppeds.2011.01.001 (In English)

Camm, E. J., Cross, C. M., Kane, A. D. et al. (2021) Maternal antioxidant treatment protects adult offspring against memory loss and hippocampal atrophy in a rodent model of developmental hypoxia. The FASEB Journal, vol. 35, article e21477. https://doi.org/10.1096/fj.202002557RR (In English)

Camm, E. J., Gibbs, M. E., Harding, R. (2001) Restriction of prenatal gas exchange impairs memory consolidation in the chick. Developmental Brain Research, vol. 132, no. 2, pp. 141–150. https://doi.org/10.1016/s0165-3806(01)00305-4 (In English)

Camm, E. J., Gibbs, M. E., Harding, R. et al. (2005) Prenatal hypoxia impairs memory function but does not result in overt structural alterations in the postnatal chick brain. Developmental Brain Research, vol. 160, no. 1, pp. 9–18. https://doi.org/10.1016/j.devbrainres.2005.07.015 (In English)

Chen, Q., Zhang, F., Wang, Y. et al. (2015) The transcription factor c-Myc suppresses MiR-23b and MiR-27b transcription during fetal distress and increases the sensitivity of neurons to hypoxia-induced apoptosis. PLoS One, vol. 10, no. 3, article e0120217. https://doi.org/10.1371%2Fjournal.pone.0120217 (In English)

Chung, Y., So, K., Kim, E. et al. (2015) Immunoreactivity of neurogenic factor in the guinea pig brain after prenatal hypoxia. Annals of Anatomy, vol. 200, pp. 66–72. https://doi.org/10.1016/j.aanat.2015.02.003 (In English)

Coq, J.-O., Delcour, M., Massicotte, V. S. et al. (2016) Prenatal ischemia deteriorates white matter, brain organization, and function: Implications for prematurity and cerebral palsy. Developmental Medicine & Child Neurology, vol. 58, no. 4, pp. 7–11. https://doi.org/10.1111/dmcn.13040 (In English)

De Boo, H. A., Harding, J. E. (2006) The developmental origins of adult disease (Barker) hypothesis. Australian and New Zealand Journal of Obstetrics and Gynaecology, vol. 46, no. 1, pp. 4–14. https://doi.org/10.1111/j.1479-828X.2006.00506.x (In English)

De Courten-Myers, G. M., Xi, G., Hwang, J. H. al. (2000) Hypoglycemic brain injury: Potentiation from respiratory depression and injury aggravation from hyperglycemic treatment overshoots. Journal of Cerebral Blood Flow & Metabolism, vol. 20, no. 1, pp. 82–92. https://doi.org/10.1097/00004647-200001000-00012 (In English)

Dehay, C., Kennedy, H. (2007) Cell-cycle control and cortical development. Nature Reviews Neuroscience, vol. 8, no. 6, pp. 438–450. https://doi.org/10.1038/nrn2097 (In English)

Delcour, M., Olivier, P., Chambon, C. et al. (2012a) Neuroanatomical, sensorimotor and cognitive deficits in adult rats with white matter injury following prenatal ischemia. Brain Pathology, vol. 22, no. 1, pp. 1–16. https://doi.org/10.1111/j.1750-3639.2011.00504.x (In English)

Delcour, M., Russier, M., Amin, M. et al. (2012b) Impact of prenatal ischemia on behavior, cognitive abilities and neuroanatomy in adult rats with white matter damage. Behavioural Brain Research, vol. 232, no. 1, pp. 233–244. https://doi.org/10.1016/j.bbr.2012.03.029 (In English)

Delcour, M., Russier, M., Xin, D. L. et al. (2011) Mild musculoskeletal and locomotor alterations in adult rats with white matter injury following prenatal ischemia. International Journal of Developmental Neuroscience, vol. 29, no. 6, pp. 593–607. https://doi.org/10.1016/j.ijdevneu.2011.02.010 (In English)

Derrick, M., Luo, N. L., Bregman, J. C. et al. (2004) Preterm fetal hypoxia-ischemia causes hypertonia and motor deficits in the neonatal rabbit: A model for human cerebral palsy? Journal of Neuroscience, vol. 24, no. 1, pp. 24–34. https://doi.org/10.1523/jneurosci.2816-03.2004 (In English)

Dobbing, J. (1968) Vulnerable periods in developing brain. In: A. N. Davison, J. Dobbing (eds.). Applied neurochemistry. Oxford: Blackwell Publ., pp. 287–316. (In English)

Du Plessis, A. J., Volpe, J. J. (2002) Perinatal brain injury in the preterm and term newborn. Current Opinion in Neurology, vol. 15, no. 2, pp. 151–157. https://doi.org/10.1097/00019052-200204000-00005 (In English)

Dubrovskaya, N. M., Zhuravin, I. A. (2008) Ontogeneticheskie osobennosti povedeniya krys, perenesshikh gipoksiyu na 14-e ili 18-e sutki embriogeneza [Specificity of ontogenetic development of behavior of rats subjected to prenatal hypoxia on the 14-th or 18-th days of embryogenesis]. Zhurnal vysshej nervnoj deyatel’nosti im. I. P. Pavlova — I. P. Pavlov Journal of Higher Nervous Activity, vol. 58, no. 6, pp. 718–727. (In Russian)

Dudley, K. J., Li, X., Kobor, M. S. et al. (2011) Epigenetic mechanisms mediating vulnerability and resilience to psychiatric disorders. Neuroscience & Biobehavioral Reviews, vol. 35, no. 7, pp. 1544–1551. https://doi.org/10.1016/j.neubiorev.2010.12.016 (In English)

Eskild, A., Strøm-Roum, E. M., Haavaldsen, C. (2016) Does the biological response to fetal hypoxia involve angiogenesis, placental enlargement and preeclampsia? Paediatric and Perinatal Epidemiology, vol. 30, no. 3, pp. 305–309. https://doi.org/10.1111/ppe.12283 (In English)

Getahun, D., Rhoads, G. G., Demissie, K. et al. (2013) In utero exposure to ischemic-hypoxic conditions and attention-deficit/hyperactivity disorder. Pediatrics, vol. 131, no. 1, pp. e53–e61. https://doi.org/10.1542/peds.2012-1298 (In English)

Giannopoulou, I., Pagida, M. A., Briana, D. D., Panayotacopoulou, M. T. (2018) Perinatal hypoxia as a risk factor for psychopathology later in life: The role of dopamine and neurotrophins. Hormones, vol. 17, no. 1, pp. 25–32. https://doi.org/10.1007/s42000-018-0007-7 (In English)

Gilbert, J. S., Babcock, S. A., Granger, J. P. (2007) Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension, vol. 50, no. 6, pp. 1142–1147. https://doi.org/10.1161/HYPERTENSIONAHA.107.096594 (In English)

Gluckman, P. D., Hanson, M. A. (2004) Living with the past: Evolution, development, and patterns of disease. Science, vol. 305, no. 5691, pp. 1733–1736. https://doi.org/10.1126/science.1095292 (In English)

Gluckman, P. D., Hanson, M. A., Cooper, C., Thornburg, K. L. (2008) Effect of in utero and early-life conditions on adult health and disease. New England Journal of Medicine, vol. 359, no. 1, pp. 61–73. https://doi.org/10.1056/NEJMra0708473 (In English)

Golan, H., Huleihel, M. (2006) The effect of prenatal hypoxia on brain development: Short- and long-term consequences demonstrated in rodent models. Developmental Science, vol. 9, no. 4, pp. 338–349. https://doi.org/10.1111/j.1467-7687.2006.00498.x (In English)

Golan, H., Kashtuzki, I., Hallak, M. et al. (2004) Maternal hypoxia during pregnancy induces fetal neurodevelopmental brain damage: Partial protection by magnesium sulfate. Journal of Neuroscience Research, vol. 78, no. 3, pp. 430–441. https://doi.org/10.1002/jnr.20269 (In English)

Golan, M. H., Mane, R., Molczadzki, G. et al. (2009) Impaired migration signaling in the hippocampus following prenatal hypoxia. Neuropharmacology, vol. 57, no. 5-6, pp. 511–522. https://doi.org/10.1016/j.neuropharm.2009.07.028 (In English)

Gonzalez-Rodriguez, P. J., Xiong, F., Li, Y. et al. (2014) Fetal hypoxia increases vulnerability of hypoxic-ischemic brain injury in neonatal rats: Role of glucocorticoid receptors. Neurobiology of Disease, vol. 65, pp. 172–179. https://doi.org/10.1016/j.nbd.2014.01.020 (In English)

Gopagondanahalli, K. R., Li, J., Fahey, M. C. et al. (2016) Preterm hypoxic-ischemic encephalopathy. Frontiers in Pediatrics, vol. 4, article 114. https://doi.org/10.3389/fped.2016.00114 (In English)

Graf, A. V., Maslova, M. V., Artiukhov, A. V. et al. (2022) Acute prenatal hypoxia in rats affects physiology and brain metabolism in the offspring, dependent on sex and gestational. International Journal of Molecular Sciences, vol. 23, no. 5, article 2579. https://doi.org/10.3390/ijms23052579 (In English)

Granger, J. P., LaMarca, B. B. D., Cockrell, K. et al. (2006) Reduced uterine perfusion pressure (RUPP) model for studying cardiovascular-renal dysfunction in response to placental ischemia. In: M. J. Soares, J. S. Hunt (eds.). Placenta and Trophoblast. Methods in Molecular Medicine. Vol. 122. Totowa: Humana Press Publ., pp. 383–392. https://doi.org/10.1385/1-59259-989-3:381 (In English)

Harris, A., Seckl, J. (2011) Glucocorticoids, prenatal stress and the programming of disease. Hormones and Behavior, vol. 59, no. 3, pp. 279–289. https://doi.org/10.1016/j.yhbeh.2010.06.007 (In English)

Herlenius, E., Lagercrantz, H. (2004) Development of neurotransmitter systems during critical periods. Experimental Neurology, vol. 190, no. 1, pp. S8–S21. https://doi.org/10.1016/j.expneurol.2004.03.027 (In English)

Hompes, T., Vrieze, E., Fieuws, S. et al. (2012) The influence of maternal cortisol and emotional state during pregnancy on fetal intrauterine growth. Pediatric Research, vol. 72, no. 3, pp. 305–315. https://doi.org/10.1038/pr.2012.70 (In English)

Inder, T. E., Volpe, J. J. (2000) Mechanisms of perinatal brain injury. Seminars in Neonatology, vol. 5, no. 1, pp. 3–16. https://doi.org/10.1053/siny.1999.0112 (In English)

Jansson, T., Powell, T. L. (2007) Role of the placenta in fetal programming: Underlying mechanisms and potential interventional approaches. Clinical Science, vol. 113, no. 1, pp. 1–13. https://doi.org/10.1042/CS20060339 (In English)

Jantzie, L. L., Corbett, C. J., Firl, D. J., Robinson, S. (2015) Postnatal erythropoietin mitigates impaired cerebral cortical development following subplate loss from prenatal hypoxia-ischemia. Cerebral Cortex, vol. 25, no. 9, pp. 2683–2695. https://doi.org/10.1093/cercor/bhu066 (In English)

Jia, L., Wang, J., Cao, H. et al. (2020) Activation of PGC-1α and mitochondrial biogenesis protects against prenatal hypoxicischemic. Brain Injury. Neuroscience, vol. 432, pp. 63–72. https://doi.org/10.1016/j.neuroscience.2020.02.035 (In English)

Katz, J. M., Pacia, S. V., Devinsky, O. (2001) Current management of epilepsy and pregnancy: Fetal outcome, congenital malformations, and developmental delay. Epilepsy & Behavior, vol. 2, no. 2, pp. 119–123. https://doi.org/10.1006/ebeh.2001.0158 (In English)

Kimball, R., Wayment, M., Merrill, D. et al. (2015) Hypoxia reduces placental mTOR activation in a hypoxia-induced model of intrauterine growth restriction (IUGR). Physiological Reports, vol. 3, no. 12, article e12651. https://doi.org/10.14814/phy2.12651 (In English)

Kubo, K. I., Deguchi, K., Nagai, T. et al. (2017) Association of impaired neuronal migration with cognitive deficits in extremely preterm infants. JCI Insight, vol. 2, no. 10, article e88609. https://doi.org/10.1172/jci.insight.88609 (In English)

Langley-Evans, S. C., McMullen, S. (2010) Developmental origins of adult disease. Medical Principles and Practice, vol. 19, no. 2, pp. 87–98. https://doi.org/10.1159/000273066 (In English)

Lawrence, K. M., McGovern, P. E., Mejaddam, A. et al. (2019) Chronic intrauterine hypoxia alters neurodevelopment in fetal sheep. Journal of Thoracic and Cardiovascular Surgery, vol. 157, no. 5, pp. 1982–1991. https://doi.org/10.1016%2Fj.jtcvs.2018.12.093 (In English)

Leonard, C. T., Goldberger, M. E. (1987) Consequences of damage to the sensomotor cortex in neonatal and adult cats. I. Sparing and recovery of function. Developmental Brain Research, vol. 32, no. 1, pp. 1–14. https://doi.org/10.1016/0165-3806(87)90133-7 (In English)

Li, Y., Gonzalez, P., Zhang, L. (2012) Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: Mechanisms and possible interventions. Progress in Neurobiology, vol. 98, no. 2, pp. 145–165. https://doi.org/10.1016/j.pneurobio.2012.05.010 (In English)

Louzoun-Kaplan, V., Zuckerman, M., Perez-Polo, J. R., Golan, H. M. (2008) Prenatal hypoxia down regulates the GABA pathway in newborn mice cerebral cortex; partial protection by MgSO4. International Journal of Developmental Neuroscience, vol. 26, no. 1, pp. 77–85. https://doi.org/10.1016/j.ijdevneu.2007.09.002 (In English)

Ma, Q., Zhang, L. (2015) Epigenetic programming of hypoxic-ischemic encephalopathy in response to fetal hypoxia. Progress in Neurobiology, vol. 124, pp. 28–48. https://doi.org/10.1016/j.pneurobio.2014.11.001 (In English)

Mach, M., Dubovicky, M., Navarová, J. et al. (2006) Vitamin E supplementation in phenytoin induced developmental toxicity in rats: Postnatal study. Neuro Endocrinology Letters, vol. 27, no. 2, pp. 69–73. https://pubmed.ncbi.nlm.nih.gov/17159783 (In English)

Maresová, D., Valkounová, I., Jandová, K. et al. (2001) Excitability changes of cortical neurons during the postnatal period in rats exposed to prenatal hypobaric hypoxia. Physiological Research, vol. 50, no. 2, pp. 215–219. https://pubmed.ncbi.nlm.nih.gov/11522050 (In English)

Mazur, M., Miller, R. H., Robinson, S. (2010) Postnatal erythropoietin treatment mitigates neural cell loss after systemic prenatal hypoxic-ischemic injury. Journal of Neurosurgery: Pediatrics, vol. 6, no. 3, pp. 206–221. https://doi.org/10.3171/2010.5.PEDS1032 (In English)

McClendon, E., Shaver, D. C., Degener-O’Brien, K. et al. (2017) Transient hypoxemia chronically disrupts maturation of preterm fetal ovine subplate neuron arborization and activity. Journal of Neuroscience, vol. 37, no. 49, pp. 11912–11929. https://doi.org/10.1523/JNEUROSCI.2396-17.2017 (In English)

McGovern, P. E., Lawrence, K., Baumgarten, H. et al. (2020) Ex utero extracorporeal support as a model for fetal hypoxia and brain dysmaturity. The Annals of Surgery, vol. 109, no. 3, pp. 810–819. https://doi.org/10.1016/j.athoracsur.2019.08.021 (In English)

Miller, S. L., Huppi, P. S., Mallard, C. (2016) The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome. The Journal of Physiology, vol. 594, no. 4, pp. 807–823. https://doi.org/10.1113/jp271402 (In English)

Miranda, A., Sousa, N. (2018) Maternal hormonal milieu influence on fetal brain development. Brain and Behavior, vol. 8, no. 2, article e00920. https://doi.org/10.1002/brb3.920 (In English)

Moisiadis, V. G., Matthews, S. G. (2014a) Glucocorticoids and fetal programming part 1: Outcomes. Nature Reviews Endocrinology, vol. 10, no. 7, pp. 391–402. https://doi.org/10.1038/nrendo.2014.73 (In English)

Moisiadis, V. G., Matthews, S. G. (2014b) Glucocorticoids and fetal programming part 2: Mechanisms. Nature Reviews Endocrinology, vol. 10, no. 7, pp. 403–411. https://doi.org/10.1038/nrendo.2014.74 (In English)

Mujsce, D. J., Christensen, M. A., Vannucci, R. C. (1990) Cerebral blood flow and edema in perinatal hypoxic-ischemic brain damage. Pediatric Research, vol. 27, no. 5, pp. 450–453. https://doi.org/10.1203/00006450-199005000-00007 (In English)

Nalivaeva, N. N., Turner, A. J., Zhuravin, I. A. (2018) Role of prenatal hypoxia in brain development, cognitive functions, and neurodegeneration. Frontiers in Neuroscience, vol. 12, article 825. https://doi.org/10.3389/fnins.2018.00825 (In English)

Nardozza, L. M. M., Caetano, A. C. R., Zamarian, A. C. P. et al. (2017) Fetal growth restriction: Current knowledge. Archives of Gynecology and Obstetrics, vol. 295, no. 5, pp. 1061–1077. https://doi.org/10.1007/s00404-017-4341-9 (In English)

Nyakas, C., Buwalda, B., Luiten, P. G. M. (1996) Hypoxia and brain development. Progress in Neurobiology, vol. 49, no. 1, pp. 1–51. https://doi.org/10.1016/0301-0082(96)00007-x (In English)

Ohshima, M., Coq, J.-O., Otani, K. et al. (2016) Mild intrauterine hypoperfusion reproduces neurodevelopmental disorders observed in prematurity. Scientific Reports, vol. 6, article 39377. https://doi.org/10.1038/srep39377 (In English)

Olivier, P., Baud, O., Evrard, P. et al. (2005) Prenatal ischemia and white matter damage in rats. Journal of Neuropathology & Experimental Neurology, vol. 64, no. 11, pp. 998–1006. https://doi.org/10.1097/01.jnen.0000187052.81889.57 (In English)

Otellin, V. A. (2003) Formirovanie patologij golovnogo mozga v embrional’nyj period [Formation of brain pathologies in the embryonic period]. Priroda, no. 9, pp. 30–35. (In Russian)

Otellin, V. A., Khozhaj, L. I., Shishko, T. T., Vershinina, E. A. (2021) Ul’trastruktura yadryshek nejronov sensomotornoj oblasti neokorteksa krys v neonatal’nyj period posle vozdejstviya perinatal’noj gipoksii i farmakologicheskoj korrektsii [Nucleolar ultrastructure in neurons of the rat neocortical sensorimotor area during the neonatal period after perinatal hypoxic exposure and its pharmacological correction]. Zhurnal evolyutsionnoj biokhimii i fiziologii — Journal of Evolutionary Biochemistry and Physiology, vol. 57, no. 6, pp. 494–499. https://doi.org/10.31857/S0044452921050065 (In Russian)

Otellin, V. A., Khozhaj, L. I., Vataeva, L. A. (2012) Vliyanie gipoksii v rannem prenatal’nom ontogeneze na povedenie i strukturnye kharakteristiki golovnogo mozga [Effect of hypoxia in early perinatal ontogenesis on behavior and structural characteristics of the rat brain]. Zhurnal evolyutsionnoj biokhimii i fiziologii — Journal of Evolutionary Biochemistry and Physiology, vol. 48, no. 5, pp. 467–473. (In Russian)

Owens, E. B., Hinshaw, S. P. (2013) Perinatal problems and psychiatric comorbidity among children with ADHD. Journal of Clinical Child & Adolescent Psychology, vol. 42, no. 6, pp. 762–768. https://doi.org/10.1080/15374416.2013.785359 (In English)

Patterson, A. J., Zhang, L. (2010) Hypoxia and fetal heart development. Current Molecular Medicine, vol. 10, no. 7, pp. 653–666. https://doi.org/10.2174/156652410792630643 (In English)

Peyronnet, J., Roux, J. C., Géloën, A. et al. (2000) Prenatal hypoxia impairs the postnatal development of neural and functional chemoafferent pathway in rat. Journal of Physiology, vol. 524, no. 2, pp. 525–537. https://doi.org/10.1111/j.1469-7793.2000.00525.x (In English)

Phillips, T. J., Scott, H., Menassa, D. A. et al. (2017) Treating the placenta to prevent adverse effects of gestational hypoxia on fetal brain development. Scientific Reports, vol. 7, article 9079. https://doi.org/10.1038/s41598-017-06300-1 (In English)

Piešová, M., Mach, M. (2020) Impact of perinatal hypoxia on the developing brain. Physiological Research, vol. 69, no. 2, pp. 199–213. https://doi.org/10.33549/physiolres.934198 (In English)

Pryce, C. R. (2008) Postnatal ontogeny of expression of the corticosteroid receptor genes in mammalian brains: Inter-species and intra-species differences. Brain Research Reviews, vol. 57, no. 2, pp. 596–605. https://doi.org/10.1016/j.brainresrev.2007.08.005 (In English)

Reznikov, K. Yu. (1981) Proliferatsiya kletok mozga pozvonochnykh v usloviyakh normal’nogo razvitiya mozga i pri ego travme [Proliferation of vertebrate brain cells in normal brain development and injury]. Moscow: Nauka Publ., 149 p. (In Russian)

Rice, D., Barone, S. (2000) Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environmental Health Perspectives, vol. 108, no. 3, pp. 511–533. https://doi.org/10.1289/ehp.00108s3511 (In English)

Rice, J. E., Vannucci, R. C., Brierley, J. B. (1981) The influence of immaturity on hypoxic-ischemic brain damage in the rat. Annals of Neurology, vol. 9, no. 2, pp. 131–141. https://doi.org/10.1002/ana.410090206 (In English)

Robinson, S., Petelenz, K., Li, Q. et al. (2005) Developmental changes induced by graded prenatal systemic hypoxic-ischemic insults in rats. Neurobiology of Disease, vol. 18, no. 3, pp. 568–581. https://doi.org/10.1016/j.nbd.2004.10.024 (In English)

Roland, E. H., Poskitt, K., Rodriguez, E. et al. (1998) Perinatal hypoxic-ischemic thalamic injury: Clinical features and neuroimaging. Annals of Neurology, vol. 44, no. 2, pp. 161–166. https://doi.org/10.1002/ana.410440205 (In English)

Rong, G., Weijian, H., Yaffing, D. et al. (2010) Brain injury caused by chronic fetal hypoxemia is mediated by inflammatory cascade activation. Reproductive Sciences, vol. 17, no. 6, pp. 540–548. https://doi.org/10.1177/1933719110364061 (In English)

Sab, I. M., Ferraz, M. M., Amaral, T. A. et al. (2013) Prenatal hypoxia, habituation memory and oxidative stress. Pharmacology Biochemistry & Behavior, vol. 107, pp. 24–28. https://doi.org/10.1016/j.pbb.2013.04.004 (In English)

Shchelchkova, N. A., Kokaya, A. A., Bezhenar’, V. F. et al. (2020) The role of brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor in chronic fetal oxygen deprivation. Modern Technologies in Medicine, vol. 12, no. 1, pp. 25–31. https://doi.org/10.17691/stm2020.12.1.03 (In English)

Sheldon, R. A., Sedik, C., Ferriero, D. M. (1998) Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Research, vol. 810, no. 1-2, pp. 114–122. https://doi.org/10.1016/s0006-8993(98)00892-0 (In English)

Shen, G., Hu, S., Zhao, Z. et al. (2020) Antenatal hypoxia accelerates the onset of Alzheimer’s disease pathology in 5xFAD mouse model. Frontiers in Aging Neuroscience, vol. 12, article 251. https://doi.org/10.3389/fnagi.2020.00251 (In English)

Skogen, J. C., Øverland, S. (2012) The fetal origins of adult disease: A narrative review of the epidemiological literature. JRSM Short Reports, vol. 3, no. 8, pp. 1–7. https://doi.org/10.1258/shorts.2012.012048 (In English)

So, K., Chung, Y., Yu, S.-K., Jun, Y. (2017) Regional immunoreactivity of Pax6 in the neurogenic zone after chronic prenatal hypoxia. In Vivo, vol. 31, no. 6, pp. 1125–1129. https://doi.org/10.21873/invivo.11178 (In English)

Sosedova, L. M., Vokina, V. A., Kapustina, E. A. (2019) Contribution of fetal programming in the formation of cognitive impairments induced by lead poisoning in white rats. Bulletin of Experimental Biology and Medicine, vol. 166, no. 5, pp. 617–621. https://doi.org/10.1007/s10517-019-04404-4 (In English)

Stratilov, V. A., Vetrovoj, O. V., Vataeva, L. A., Tyul’kova, E. I. (2021) Assotsiirovannye s vozrastom izmeneniya v issledovatelskoj aktivnosti v teste “Otkrytoe pole” u krys, perezhivshikh prenatal’nuyu gipoksiyu [Age-associated changes in exploratory activity in the open field test in rats surviving prenatal hypoxia]. Zhurnal vysshej nervnoj deyatel’nosti im. I. P. Pavlova — I. P. Pavlov Journal of Higher Nervous Activity, vol. 71, no. 3, pp. 428–436. https://doi.org/10.31857/S0044467721030102 (In Russian)

Togher, K. L., O’Keeffe, M. M., Khashan, A. S. et al. (2014) Epigenetic regulation of the placental HSD11B2 barrier and its role as a critical regulator of fetal development. Epigenetics, vol. 9, no. 6. pp. 816–822. https://doi.org/10.4161/epi.28703 (In English)

Towfighi, J., Zec, N., Yager, J. et al. (1995) Temporal evolution of neuropathologic changes in an immature rat model of cerebral hypoxia: A light microscopic study. Acta Neuropathologica, vol. 90, no. 4, pp. 375–386. https://doi.org/10.1007/BF00315011 (In English)

Tuor, U. I., Del Bigio, M. R., Chumas, P. D. (1996) Brain damage due to cerebral hypoxia/ischemia in the neonate: Pathology and pharmacological modification. Cerebrovascular & Brain Metabolism Review, vol. 8, no. 2, pp. 159–193. https://pubmed.ncbi.nlm.nih.gov/8727185 (In English)

Tyul’kova, E. I., Vataeva, L. A., Vetrovoj, O. V., Romanovskij, D. Yu. (2015) Prenatal’naya gipoksiya modifitsiruet rabochuyu pamyat’ i aktivnost’ polifosfoinozitidnoj sistemy gippokampa krys [Prenatal hypoxia modifies working memory and the activity of hippocampal polyphosphoinositide system in rats]. Zhurnal evolyutsionnoj biokhimii i fiziologii — Journal of Evolutionary Biochemistry and Physiology, vol. 51, no. 2, pp. 115–121. (In Russian)

Tyul’kova, E. I., Vataeva, L. A., Stratilov, V. A. et al. (2020) Osobennosti metilirovaniya DNK i gistona H3 v gippokampe i neokortekse krys, perezhivshikh patologicheskie vozdejstviya v prenatal’nom periode razvitiya [Peculiarities of DNA and histone H3 methylation in the hippocampus and neocortex of rats subjected to pathological treatments during the prenatal period]. Neyrokhimiya — Neurochemical Journal, vol. 37, no. 1, pp. 64–74. https://doi.org/10.31857/S1027813320010197 (In Russian)

Ujhazy, E., Dubovicky, M., Navarova, J. et al. (2013) Subchronic perinatal asphyxia in rats: Embryo-foetal assessment of a new model of oxidative stress during critical period of development. Food and Chemical Toxicology, vol. 61, pp. 233–239. https://doi.org/10.1016/j.fct.2013.07.023 (In English)

Vannucci, R. C. (2000) Hypoxic-ischemic encephalopathy. American Journal of Perinatology, vol. 17, no. 3, pp. 113–120. https://doi.org/10.1055/s-2000-9293 (In English)

Vannucci, R. C., Connor, J. R., Mauger, D. T. et al. (1999) Rat model of perinatal hypoxic-ischemic brain damage. Journal of Neuroscience Research, vol. 55, no. 2, pp. 158–163. https://doi.org/10.1002/(SICI)1097-4547(19990115)55:2<158::AID-JNR3>3.0.CO;2-1 (In English)

Vannucci, C. R., Perlman, J. M. (1997) Interventions for perinatal hypoxic-ischemic encephalopathy. Pediatrics, vol. 100, no. 6, pp. 1004–1014. https://doi.org/10.1542/peds.100.6.1004 (In English)

Vannucci, R. C., Vannucci, S. J. (2005) Perinatal hypoxic-ischemic brain damage: Evolution of an animal model. Developmental Neuroscience, vol. 27, no. 2-4, pp. 81–86. https://doi.org/10.1159/000085978 (In English)

Vasilev, D. S., Dubrovskaya, N. M., Tumanova, N. L., Zhuravin, I. A. (2016) Prenatal hypoxia in different periods of embryogenesis differentially affects cell migration, neuronal plasticity, and rat behavior in postnatal ontogenesis. Frontiers in Neuroscience, vol. 10, article 126. https://doi.org/10.3389/fnins.2016.00126 (In English)

Vasil’ev, D. S., Tumanova, N. L., Zhuravin, I. A. (2008) Strukturnye izmeneniya v nervnoj tkani novoj kory v ontogeneze krys posle gipoksii na raznykh srokakh embriogeneza [Structural changes in the neocortex nervous tissue in rat ontogenesis after hypoxia at various terms of embryogenesis]. Zhurnal evolyutsionnoj biokhimii i fiziologii — Journal of Evolutionary Biochemistry and Physiology, vol. 44, no. 3. pp. 258–267. (In Russian)

Vataeva, L. A., Tyul’kova, E. I., Alekhin, A. N., Stratilov, V. A. (2018) Vliyanie gipoksii ili deksametazona v razlichnye sroki gestatsii na proyavlenie uslovno-reflektornogo strakha u vzroslykh krys [Effects of hypoxia or dexamethasone at different gestation periods on fear conditioning in adult rats]. Zhurnal evolyutsionnoy biokhimii i fiziologii — Journal of Evolutionary Biochemistry and Physiology, vol. 54, no. 6, pp. 392–398. https://doi.org/10.1134/S0044452918060037 (In Russian)

Vetrovoj, O. V., Nimiritskij, P. P., Tyul’kova, E. I., Rybnikova, E. A. (2020) Soderzhanie i aktivnost’ gipoksiya-indutsiruemogo faktora HIF1α uvelicheny v gippokampe novorozhdennykh krysyat, perezhivshikh prenatalnuyu gipoksiyu na 14–16 sutki embriogeneza [The content and activity of the hypoxia-inducible factor HIF1α increases in the hippocampus of newborn rats that were subjected to the prenatal hypoxia on 14–16 days of embryogenesis]. Nejrokhimiya — Neurochemical Journal, vol. 37, no. 3, pp. 228–232. https://doi.org/10.31857/S1027813320030127 (In Russian)

Vetrovoy, O., Stratilov, V., Nimiritsky, P. et al. (2021) Prenatal hypoxia induces premature aging accompanied by disturbed function of glutamatergic system in rat hippocampus. Neurochemical Research, vol. 46, no. 3, pp. 550–563. https://doi.org/10.1007/s11064-020-03191-z (In English)

Vetrovoy, O., Tyulkova, E., Stratilov, V. et al. (2020) Long-term effects of prenatal severe hypoxia on central and peripheral components of the glucocorticoid system in rats. Developmental Neuroscience, vol. 42, no. 2-4, pp. 145–158. https://doi.org/10.1159/000512223 (In English)

Volpe, J. J. (1992) Brain injury in the premature infant—current concepts of pathogenesis and prevention. Biology of the Neonate, vol. 62, no. 4, pp. 231–242. https://doi.org/10.1159/000243876 (In English)

Waffarn, F., Davis, E. P. (2012) Effects of antenatal corticosteroids on the hypothalamic-pituitary-adrenocortical axis of the fetus and newborn: Experimental findings and clinical considerations. American Journal of Obstetrics and Gynecology, vol. 207, no. 6, pp. 446–454. https://doi.org/10.1016/j.ajog.2012.06.012 (In English)

Wang, X., Meng, F.-S., Liu, Z.-Y. et al. (2013) Gestational hypoxia induces sex-differential methylation of Crhr1 linked to anxiety-like behavior. Molecular Neurobiology, vol. 48, no. 3, pp. 544–555. https://doi.org/10.1007/s12035-013-8444-4 (In English)

Wang, W.-T., Lee, P., Dong, Y. et al. (2016) In vivo neurochemical characterization of developing guinea pigs and the effect of chronic fetal hypoxia. Neurochemical Research, vol. 41, no. 7, pp. 1831–1843. https://doi.org/10.1007/s11064-016-1924-y (In English)

Warner, M. J., Ozanne, S. E. (2010) Mechanisms involved in the developmental programming of adulthood disease. Biochemical Journal, vol. 427, no. 3, pp. 333–347. https://doi.org/10.1042/bj20091861 (In English)

Wei, B., Li, L., He, A. et al. (2016) Hippocampal NMDAR-Wnt-Catenin signaling disrupted with cognitive deficits in adolescent offspring exposed to prenatal hypoxia. Brain Research, vol. 1631, pp. 157–164. https://doi.org/10.1016/j.brainres.2015.11.041 (In English)

Xiong, F., Zhang, L. (2013) Role of the hypothalamic-pituitary-adrenal axis in developmental programming of health and disease. Frontiers in Neuroendocrinology, vol. 34, no. 1, pp. 27–46. https://doi.org/doi:10.1016/j.yfrne.2012.11.002 (In English)

Zamudio, S. (2003) The placenta at high altitude. High Altitude Medicine & Biology, vol. 4, no. 2, pp. 171–191. https://doi.org/10.1089/152702903322022785 (In English)

Zhao, T., Zhang, C. P., Liu, Z. H. et al. (2008) Hypoxia-driven proliferation of embryonic neural stem⁄progenitor cells—role of hypoxia-inducible transcription factor-1α. FEBS Journal, vol. 275, no. 8, pp. 1824–1834. https://doi.org/10.1111/j.1742-4658.2008.06340.x (In English)

Zhuravin, I. A., Dubrovskaya, N. M., Vasilev, D. S. et al. (2019). Prenatal hypoxia produces memory deficits associated with impairment of long-term synaptic plasticity in young rats. Neurobiology of Learning and Memory, vol. 164, article 107066. https://doi.org/10.1016/j.nlm.2019.107066 (In English)

Zhuravin, I. A., Tumanova, N. L., Vasil’ev, D. S. (2009) Strukturnye izmeneniya nervnoj tkani gippokampa v ontogeneze krys posle prenatal’noj gipoksii [Structural changes of the hippocampus nervous tissue in rat ontogenesis after prenatal hypoxia]. Zhurnal evolyutsionnoj biokhimii i fiziologii — Journal of Evolutionary Biochemistry and Physiology, vol. 45, no. 1, pp. 138–140. (In Russian)

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