Patterns of development and formation of the fetal central nervous system integrative function in the antenatal period

Abstract

The development of the fetal central nervous system and the formation of its integrative functions have been studied for a long time. In the middle of the 20^th century, researchers paid attention to structural changes and in the 1980s to the sequence of formation of functional relationships in the fetal body and the possibilities of their assessment. Further development of technology (accumulation of knowledge in the field of embryology, better resolution of ultrasound diagnostic devices, introduction and improvement of magnetic resonance imaging methods) allowed for not only receiving more detailed data on structural patterns in the fetal brain during pregnancy, but also presenting new opportunities for expanding knowledge about its functional condition. The review is devoted to the generalization of knowledge about the development of the fetal central nervous system, the brain vascular network formation and the brain circulation, as well as possibilities of assessing the formation of the fetal central nervous system integrative function during the entire period of pregnancy.

Keywords

embryology / perinatology / normal physiology / brain / morphophysiology / central nervous system / fetal circulation / circle of Willis / myocardial reflex / ultrasound diagnostics / magnetic resonance imaging

References

[1] Konkel L. The brain before birth: using fMRI to explore the secrets of fetal neurodevelopment. Environ. Health Perspect. 2018;126(11). DOI: 10.1289/EHP2268

[2] Konkel L. The brain before birth: using fMRI to explore the secrets of fetal neurodevelopment // Environ. Health Perspect. 2018. Vol. 126. No. 11. DOI: 10.1289/EHP2268

[3] Stiles J, Jernigan TL. The basics of brain development. Neuropsychol Rev. 2010;20(4):327–348. DOI: 10.1007/s11065-010-9148-4

[4] Stiles J., Jernigan T.L. The basics of brain development // Neuropsychol. Rev. 2010. Vol. 20. No. 4. P. 327–348. DOI: 10.1007/s11065-010-9148-4

[5] San-Jose LM, Roulin A. On the potential role of the neural crest cells in integrating pigmentation into behavioral and physiological syndromes. Front Ecol Evol. 2020;8. DOI: 10.3389/fevo.2020.00278

[6] San-Jose L.M., Roulin A. On the potential role of the neural crest cells in integrating pigmentation into behavioral and physiological syndromes // Front. Ecol. Evol. 2020. Vol. 8. DOI: 10.3389/fevo.2020.00278

[7] Bystron I, Blakemore C, Rakic P. Development of the human cerebral cortex: boulder bommittee revisited. Nat Rev Neurosci. 2008;9(2):110–122. DOI: 10.1038/nrn2252

[8] Bystron I., Blakemore C., Rakic P. Development of the human cerebral cortex: Boulder Committee revisited // Nat. Rev. Neurosci. 2008. Vol. 9. No. 2. P. 110–122. DOI: 10.1038/nrn2252

[9] Quezada S, Castillo-Melendez M, Walker DW, et al. Development of the cerebral cortex and the effect of the intrauterine environment. J Physiol. 2018;596(23):5665–5674. DOI: 10.1113/JP277151

[10] Quezada S., Castillo-Melendez M., Walker D.W., et al. Development of the cerebral cortex and the effect of the intrauterine environment // J. Physiol. 2018. Vol. 596. No. 23. P. 5665–5674. DOI: 10.1113/JP277151

[11] Fernández V, Llinares-Benadero C, Borrell V. Cerebral cortex expansion and folding: what have we learned? EMBO J. 2016;35(10):1021–1044. DOI: 10.15252/embj.201593701

[12] Fernández V., Llinares-Benadero C., Borrell V. Cerebral cortex expansion and folding: what have we learned? // EMBO J. 2016. Vol. 35. No. 10. P. 1021–1044. DOI: 10.15252/embj.201593701

[13] Blaas HG, Eik-Nes SH, Kiserud T, et al. Early development of the forebrain and midbrain: a longitudinal ultrasound study from 7 to 12 weeks of gestation. Ultrasound Obstet Gynecol. 1994;4(3):183–192. DOI: 10.1046/j.1469-0705.1994.04030183.x

[14] Blaas H.G., Eik-Nes S.H., Kiserud T., et al. Early development of the forebrain and midbrain: a longitudinal ultrasound study from 7 to 12 weeks of gestation // Ultrasound Obstet. Gynecol. 1994. Vol. 4. No. 3. P. 183–192. DOI: 10.1046/j.1469-0705.1994.04030183.x

[15] Blaas HG, Eik-Nes SH, Kiserud T, et al. Early development of the hindbrain: a longitudinal ultrasound study from 7 to 12 weeks of gestation. Ultrasound Obstet Gynecol. 1995;5(3):151–160. DOI: 10.1046/j.1469-0705.1995.05030151.x

[16] Blaas H.G., Eik-Nes S.H., Kiserud T., et al. Early development of the hindbrain: a longitudinal ultrasound study from 7 to 12 weeks of gestation. // Ultrasound Obstet. Gynecol. 1995. Vol. 5. No. 3. P. 151–160. DOI: 10.1046/j.1469-0705.1995.05030151.x

[17] Barkovich AJ, Raybaud C, editors. Pediatric neuroimaging. 5th ed. Philadelphia; 2012.

[18] Pediatric neuroimaging / Ed. by A.J. Barkovich, C. Raybaud. 5th ed. Philadelphia, 2012.

[19] Barkovich MJ, Barkovich AJ. MR imaging of normal brain development. Neuroimaging Clin N Am. 2019;29(3):325–337. DOI: 10.1016/j.nic.2019.03.007

[20] Barkovich M.J., Barkovich A.J. MR Imaging of normal brain development // Neuroimaging Clin. N. Am. 2019. Vol. 29. No. 3. P. 325–337. DOI: 10.1016/j.nic.2019.03.007

[21] Studholme C. Mapping fetal brain development in utero using magnetic resonance imaging: the big bang of brain mapping. Annu Rev Biomed Eng. 2011;13(1):345–368. DOI: 10.1146/annurev-bioeng-071910-124654

[22] Studholme C. Mapping fetal brain development in utero using magnetic resonance imaging: the big bang of brain mapping // Annu. Rev. Biomed. Eng. 2011. Vol. 13. No. 1. P. 345–368. DOI: 10.1146/annurev-bioeng-071910-124654

[23] Dubois J, Dehaene-Lambertz G, Kulikova S, et al. The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience. 2014;276:48–71. DOI: 10.1016/j.neuroscience.2013.12.044

[24] Dubois J., Dehaene-Lambertz G., Kulikova S., et al. The early development of brain white matter: A review of imaging studies in fetuses, newborns and infants // Neuroscience. 2014. Vol. 276. P. 48–71. DOI: 10.1016/j.neuroscience.2013.12.044

[25] Ouyang M, Dubois J, Yu Q, et al. Delineation of early brain development from fetuses to infants with diffusion MRI and beyond. Neuroimage. 2019;185:836–850. DOI: 10.1016/j.neuroimage.2018.04.017

[26] Ouyang M., Dubois J., Yu Q., et al. Delineation of early brain development from fetuses to infants with diffusion MRI and beyond // Neuroimage. 2019. Vol. 185. P. 836–850. DOI: 10.1016/j.neuroimage.2018.04.017

[27] Studholme C. Mapping the developing human brain in utero using quantitative MR imaging techniques. Semin Perinatol. 2015;39(2):105–112. DOI: 10.1053/j.semperi.2015.01.003

[28] Studholme C. Mapping the developing human brain in utero using quantitative MR imaging techniques // Semin. Perinatol. 2015. Vol. 39. No. 2. P. 105–112. DOI: 10.1053/j.semperi.2015.01.003

[29] Wright R, Makropoulos A, Kyriakopoulou V, et al. Construction of a fetal spatio-temporal cortical surface atlas from in utero MRI: application of spectral surface matching. Neuroimage. 2015;120:467–480. DOI: 10.1016/j.neuroimage.2015.05.087

[30] Wright R., Makropoulos A., Kyriakopoulou V., et al. Construction of a fetal spatio-temporal cortical surface atlas from in utero MRI: Application of spectral surface matching // Neuroimage. 2015. Vol. 120. P. 467–480. DOI: 10.1016/j.neuroimage.2015.05.087

[31] Moltoni G, Talenti G, Righini A. Brain fetal neuroradiology: a beginner’s guide. Transl Pediatr. 2021;10(4):1065–1077. DOI: 10.21037/tp-20-293

[32] Moltoni G., Talenti G., Righini A. Brain fetal neuroradiology: a beginner’s guide // Transl. Pediatr. 2021. Vol. 10. No. 4. P. 1065–1077. DOI: 10.21037/tp-20-293

[33] Hill J, Dierker D, Neil J, et al. A surface-based analysis of hemispheric asymmetries and folding of cerebral cortex in term-born human infants. J Neurosci. 2010;30(6):2268–2276. DOI: 10.1523/JNEUROSCI.4682-09.2010

[34] Hill J., Dierker D., Neil J., et al. A surface-based analysis of hemispheric asymmetries and folding of cerebral cortex in term-born human infants // J. Neurosci. 2010. Vol. 30. No. 6. P. 2268–2276. DOI: 10.1523/JNEUROSCI.4682-09.2010

[35] Kim K, Habas PA, Rousseau F, et al. Intersection based motion correction of multislice MRI for 3-D in utero fetal brain image formation. IEEE Trans Med Imaging. 2010;29(1):146–158. DOI: 10.1109/TMI.2009.2030679

[36] Kim K., Habas P.A., Rousseau F., et al. Intersection based motion correction of multislice MRI for 3-D in utero fetal brain image formation // IEEE Trans. Med. Imaging. 2010. Vol. 29, No. 1. P. 146–158. DOI: 10.1109/TMI.2009.2030679

[37] Habas PA, Scott JA, Roosta A, et al. Early folding patterns and asymmetries of the normal human brain detected from in utero MRI. Cereb Cortex. 2012;22(1):13–25. DOI: 10.1093/cercor/bhr053

[38] Habas P.A., Scott J.A., Roosta A., et al. Early folding patterns and asymmetries of the No.rmal human brain detected from in utero MRI // Cereb. Cortex. 2012. Vol. 22. No. 1. P. 13–25. DOI: 10.1093/cercor/bhr053

[39] Clouchoux C, Kudelski D, Gholipour A, et al. Quantitative in vivo MRI measurement of cortical development in the fetus. Brain Struct Funct. 2012;217(1):127–139. DOI: 10.1007/s00429-011-0325-x

[40] Clouchoux C., Kudelski D., Gholipour A., et al. Quantitative in vivo MRI measurement of cortical development in the fetus // Brain Struct. Funct. 2012. Vol. 217. No. 1. P. 127–139. DOI: 10.1007/s00429-011-0325-x

[41] Dubois J, Benders M, Borradori-Tolsa C, et al. Primary cortical folding in the human newborn: an early marker of later functional development. Brain. 2008;131(8):2028–2041. DOI: 10.1093/brain/awn137

[42] Dubois J., Benders M., Borradori-Tolsa C., et al. Primary cortical folding in the human newborn: an early marker of later functional development // Brain. 2008. Vol. 131. No. 8. P. 2028–2041. DOI: 10.1093/brain/awn137

[43] Geva R, Eshel R, Leitner Y, et al. Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study. Pediatrics. 2006;118(1):91–100. DOI: 10.1542/peds.2005-2343

[44] Geva R., Eshel R., Leitner Y., et al. Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study // Pediatrics. 2006. Vol. 118. No. 1. P. 91–100. DOI: 10.1542/peds.2005-2343

[45] Garel C, Chantrel E, Elmaleh M, et al. Fetal MRI: normal gestational landmarks for cerebral biometry, gyration and myelination. Childs Nerv Syst. 2003;19(7–8):422–425. DOI: 10.1007/s00381-003-0767-4

[46] Garel C., Chantrel E., Elmaleh M., et al. Fetal MRI: Normal gestational landmarks for cerebral biometry, gyration and myelination. // Childs. Nerv. Syst. 2003. Vol. 19. No. 7–8. P. 422–425. DOI: 10.1007/s00381-003-0767-4

[47] Kyriakopoulou V, Vatansever D, Davidson A, et al. Normative biometry of the fetal brain using magnetic resonance imaging. Brain Struct Funct. 2017;222(5):2295–2307. DOI: 10.1007/s00429-016-1342-6

[48] Kyriakopoulou V., Vatansever D., Davidson A., et al. Normative biometry of the fetal brain using magnetic resonance imaging // Brain Struct. Funct. 2017. Vol. 222. No. 5. P. 2295–2307. DOI: 10.1007/s00429-016-1342-6

[49] Conte G, Milani S, Palumbo G, et al. Prenatal brain MR imaging: reference linear biometric centiles between 20 and 24 gestational weeks. Am J Neuroradiol. 2018;39(5):963–967. DOI: 10.3174/ajnr.A5574

[50] Conte G., Milani S., Palumbo G., et al. Prenatal brain MR imaging: reference linear biometric centiles between 20 and 24 gestational weeks // Am. J. Neuroradiol. 2018. Vol. 39. No. 5. P. 963–967. DOI: 10.3174/ajnr.A5574

[51] Yoshida R, Ishizu K, Yamada S, et al. Dynamics of gyrification in the human cerebral cortex during development. Congenit Anom (Kyoto). 2017;57(1):8–14. DOI: 10.1111/cga.12179

[52] Yoshida R., Ishizu K., Yamada S., et al. Dynamics of gyrification in the human cerebral cortex during development // Congenit. ANom. 2017. Vol. 57. No. 1. P. 8–14. DOI: 10.1111/cga.12179

[53] Wobrock T, Gruber O, McIntosh AM, et al. Reduced prefrontal gyrification in obsessive–compulsive disorder. Eur Arch Psychiatry Clin Neurosci. 2010;260(6):455–464. DOI: 10.1007/s00406-009-0096-z

[54] Wobrock T., Gruber O., McIntosh A.M., et al. Reduced prefrontal gyrification in obsessive–compulsive disorder // Eur. Arch. Psychiatry Clin. Neurosci. 2010. Vol. 260. No. 6. P. 455–464. DOI: 10.1007/s00406-009-0096-z

[55] Auzias G, Viellard M, Takerkart S, et al. Atypical sulcal anatomy in young children with autism spectrum disorder. NeuroImage Clin. 2014;4:593–603. DOI: 10.1016/j.nicl.2014.03.008

[56] Auzias G., Viellard M., Takerkart S., et al. Atypical sulcal anatomy in young children with autism spectrum disorder // NeuroImage Clin. 2014. Vol. 4. P. 593–603. DOI: 10.1016/j.nicl.2014.03.008

[57] Budday S, Raybaud C, Kuhl E. A mechanical model predicts morphological abnormalities in the developing human brain. Sci Rep. 2015;4(1). DOI: 10.1038/srep05644

[58] Budday S., Raybaud C., Kuhl E. A mechanical model predicts morphological abnormalities in the developing human brain // Sci. Rep. 2015. Vol. 4. No. 1. DOI: 10.1038/srep05644

[59] Sidman RL, Rakic P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 1973;62(1):1–35. DOI: 10.1016/0006-8993(73)90617-3

[60] Sidman R.L., Rakic P. Neuronal migration, with special reference to developing human brain: a review // Brain Res. 1973. Vol. 62. No. 1. P. 1–35. DOI: 10.1016/0006-8993(73)90617-3

[61] Mrzljak L, Uylings HB, Van Eden CG, et al. Neuronal development in human prefrontal cortex in prenatal and postnatal stages. Prog Brain Res. 1990;85:185–222. DOI: 10.1016/s0079-6123(08)62681-3

[62] Mrzljak L., Uylings H.B., Van Eden C.G., et al. Neuronal development in human prefrontal cortex in prenatal and postnatal stages // Prog. Brain Res. 1990. Vol. 85. P. 185–222. DOI: 10.1016/s0079-6123(08)62681-3

[63] Huttenlocher PR, Dabholkar AS. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol. 1997;387(2):167–178. DOI: 10.1002/(SICI)1096-9861(19971020)387:2<167::AID-CNE1>3.0.CO;2-Z

[64] Huttenlocher P.R., Dabholkar A.S. Regional differences in synaptogenesis in human cerebral cortex // J. Comp. Neurol. 1997. Vol. 387. No. 2. P. 167–178. DOI: 10.1002/(SICI)1096-9861(19971020)387:2<167::AID-CNE1>3.0.CO;2-Z

[65] Thomason ME. Structured spontaneity: building circuits in the human prenatal brain. Trends Neurosci. 2018;41(1):1–3. DOI: 10.1016/j.tins.2017.11.004

[66] Thomason M.E. Structured spontaneity: building circuits in the human prenatal brain // Trends Neurosci. 2018. Vol. 41. No. 1. P. 1–3. DOI: 10.1016/j.tins.2017.11.004

[67] Kostović I, Jovanov-Milošević N. The development of cerebral connections during the first 20–45 weeks’ gestation. Semin Fetal Neonatal Med. 2006;11(6):415–422. DOI: 10.1016/j.siny.2006.07.001

[68] Kostović I., JovaNo.v-Milošević N. The development of cerebral connections during the first 20–45 weeks’ gestation // Semin. Fetal Neonatal Med. 2006. Vol. 11. No. 6. P. 415–422. DOI: 10.1016/j.siny.2006.07.001

[69] Vasung L, Huang H, Jovanov-Milošević N, et al. Development of axonal pathways in the human fetal fronto-limbic brain: histochemical characterization and diffusion tensor imaging. J Anat. 2010;217(4):400–417. DOI: 10.1111/j.1469-7580.2010.01260.x

[70] Vasung L., Huang H., Jovanov-Milošević N., et al. Development of axonal pathways in the human fetal fronto-limbic brain: histochemical characterization and diffusion tensor imaging // J. Anat. 2010. Vol. 217. No. 4. P. 400–417. DOI: 10.1111/j.1469-7580.2010.01260.x

[71] Collin G, van den Heuvel MP. The ontogeny of the human connectome. Neurosci. 2013;19(6):616–628. DOI: 10.1177/1073858413503712

[72] Collin G., van den Heuvel M.P. The ontogeny of the human connectome // Neurosci. 2013. Vol. 19. No. 6. P. 616–628. DOI: 10.1177/1073858413503712

[73] Hoff GE, Van den Heuvel MP, Benders MJ, et al. On development of functional brain connectivity in the young brain. Front Hum Neurosci. 2013;7:650. DOI: 10.3389/fnhum.2013.00650

[74] Hoff G.E., Van den Heuvel M.P., Benders M.J., et al. On development of functional brain connectivity in the young brain // Front. Hum. Neurosci. 2013. Vol. 7. P. 650. DOI: 10.3389/fnhum.2013.00650

[75] Turk E, van den Heuvel MI, Benders MJ, et al. Functional connectome of the fetal brain. J Neurosci. 2019;39(49):9716–9724. DOI: 10.1523/JNEUROSCI.2891-18.2019

[76] Turk E., van den Heuvel M.I., Benders M.J., et al. Functional connectome of the fetal brain // J. Neurosci. 2019. Vol. 39. No. 49. P. 9716–9724. DOI: 10.1523/JNEUROSCI.2891-18.2019

[77] Krontira AC, Cruceanu C. The fetal functional connectome offers clues for early maturing networks and implications for neurodevelopmental disorders. J Neurosci. 2020;40(23):4436–4438. DOI: 10.1523/JNEUROSCI.0260-20.2020

[78] Krontira A.C., Cruceanu C. The fetal functional connectome offers clues for early maturing networks and implications for neurodevelopmental disorders // J. Neurosci. 2020. Vol. 40. No. 23. P. 4436–4438. DOI: 10.1523/JNEUROSCI.0260-20.2020

[79] Larsen WJ. Human embryology. 3rd ed. Philadelphia: Churchill Livingstone; 2001.

[80] Larsen W.J. Human embryology. 3rd ed. Philadelphia: Churchill Livingstone, 2001.

[81] Marín-Padilla M. The human brain intracerebral microvascular system: development and structure. Front Neuroanat. 2012;6:38. DOI: 10.3389/fnana.2012.00038

[82] Marín-Padilla M. The human brain intracerebral microvascular system: development and structure // Front. Neuroanat. 2012. Vol. 6. P. 38. DOI: 10.3389/fnana.2012.00038

[83] Vasung L, Abaci Turk E, Ferradal SL, et al. Exploring early human brain development with structural and physiological neuroimaging. Neuroimage. 2019;187:226–254. DOI: 10.1016/j.neuroimage.2018.07.041

[84] Vasung L., Abaci Turk E., Ferradal S.L., et al. Exploring early human brain development with structural and physiological neuroimaging // Neuroimage. 2019. Vol. 187. P. 226–254. DOI: 10.1016/j.neuroimage.2018.07.041

[85] Raghunathan R, Liu C-H, Singh M, et al. A comparison of microvasculature changes in the fetal brain and maternal extremities due to prenatal alcohol exposure using optical coherence angiography. In: Proceedings of the SPIE. Dynamics and Fluctuations in Biomedical Photonics XVIII. Ed. by V.V. Tuchin, M.J. Leahy, R.K. Wang. 2021:11641. DOI: 10.1117/12.2583340

[86] Raghunathan R., Liu C.-H., Singh M., et al. A comparison of microvasculature changes in the fetal brain and maternal extremities due to prenatal alcohol exposure using optical coherence angiography // Proceedings of the SPIE. Dynamics and Fluctuations in Biomedical Photonics XVIII. Tuchin V.V., Leahy M.J., Wang R.K., editors. 2021. Vol. 11641. DOI: 10.1117/12.2583340

[87] Bautch VL, James JM. Neurovascular development. Cell Adh Migr. 2009;3(2):199–204. DOI: 10.4161/cam.3.2.8397

[88] Bautch V.L., James J.M. Neurovascular development // Cell Adh. Migr. 2009. Vol. 3. No. 2. P. 199–204. DOI: 10.4161/cam.3.2.8397

[89] Willie CK, Tzeng Y-C, Fisher JA, et al. Integrative regulation of human brain blood flow. J Physiol. 2014;592(5):841–859. DOI: 10.1113/jphysiol.2013.268953

[90] Willie C.K. Yu-Chieh T., Joseph A F. et al. Integrative regulation of human brain blood flow // J. Physiol. 2014. Vol. 592. No. 5. P. 841–859. DOI: 10.1113/jphysiol.2013.268953

[91] Nasretdinov AR, Khazipov RN. Early activity patterns and thalamocortical synaptic plasticity during the “brain spurt” period. Uchenye zapiski kazanskogo universiteta Seriya estestvennye nauki. 2018;160(4):677–685

[92] Насретдинов А.Р., Хазипов Р.Н. Паттерны ранней активности и синаптическая пластичность соматосенсорных таламокортикальных карт во время критического периода развития // Ученые записки казанского университета. Серия естественные науки. 2018. Т. 160, № 4. C. 677–685.

[93] Haynes RL, Borenstein NS, Desilva TM, et al. Axonal development in the cerebral white matter of the human fetus and infant. J Comp Neurol. 2005;484(2):156–167. DOI: 10.1002/cne.20453

[94] Haynes R.L., Borenstein N.S., Desilva T.M., et al. Axonal development in the cerebral white matter of the human fetus and infant // J. Comp. Neurol. 2005. Vol. 484. No. 2. P. 156–167. DOI: 10.1002/cne.20453

[95] Akhmetshina DR, Valeeva GR, Colonnese M, et al. Brain activity at the embryonic stages of development. Uchenye zapiski Kazanskogo universiteta. Seriya Estestvennye nauki. 2015;157(2):5–34.

[96] Ахметшина Д.Р., Валеева Г.Р., Колоннезе М., и др. Активность мозга на эмбриональных этапах развития // Ученые записки Казанского университета. Серия Естественные науки. 2015. Т. 157, № 2. C. 5–34

[97] Vrselja Z, Brkic H, Mrdenovic S, et al. Function of circle of willis. J Cereb Blood Flow Metab. 2014;34(4):578–584. DOI: 10.1038/jcbfm.2014.7

[98] Vrselja Z. Brkic H., Mrdenovic S., et al. Function of circle of willis // J. Cereb. Blood Flow Metab. 2014. Vol. 34. No. 4. P. 578–584. DOI: 10.1038/jcbfm.2014.7

[99] Vanderah T. Nolte’s essentials of the human brain. 1st ed. 2009.

[100] Pooh RK, Kurjak A. Fetal brain vascularity visualized by conventional 2D and 3D power doppler technology. Donald Sch J Ultrasound Obstet Gynecol. 2010;4(3):249–258. DOI: 10.5005/jp-journals-10009-1147

[101] Pooh R.K., Kurjak A. Fetal brain vascularity visualized by conventional 2D and 3D power doppler technology // Donald Sch. J. Ultrasound Obstet. Gynecol. 2010. Vol. 4. No. 3. P. 249–258. DOI: 10.5005/jp-journals-10009-1147

[102] Ageeva MI. Dopplerograficheskoe issledovanie gemodinamiki ploda: posobie dlya vrachey. 2006.

[103] Агеева М.И. Допплерографическое исследование гемодинамики плода: пособие для врачей. Москва, 2006.

[104] Burlev VA, Zaydieva S, Il’yasova NA. Regulyatsiya angiogeneza gestatsionnogo perioda. Problemy reproduktsii. 2008;3:15–22.

[105] Бурлев В.А., Зайдиева С., Ильясова Н.А. Регуляция ангиогенеза гестационного периода // Проблемы репродукции. 2008. № 3. C. 15–22.

[106] Cipolla MJ. The cerebral circulation. Colloq Ser Integr Syst Physiol From Mol to Funct. 2009;1(1):1–59. DOI: 10.4199/C00005ED1V01Y200912ISP002

[107] Cipolla M.J. The cerebral circulation // Colloq. Ser. Integr. Syst. Physiol. From Mol. to Funct. 2009. Vol. 1. No. 1. P. 1–59. DOI: 10.4199/C00005ED1V01Y200912ISP002

[108] Pooh RK, Pooh KH. Fetal neuroimaging. Fetal Matern Med Rev. 2008;19(1):1–31. DOI: 10.1017/S0965539508002106

[109] Pooh R.K., Pooh K.H. Fetal neuroimaging // Fetal Matern. Med. Rev. 2008. Vol. 19. No. 1. P. 1–31. DOI: 10.1017/S0965539508002106

[110] Barashnev YuI. Perinatal’naya nevrologiya. Moscow: Triada-Kh; 2005. (in Russ.)

[111] Барашнев Ю.И. Перинатальная неврология. Москва: Триада-Х, 2005.

[112] Polyanin AA, Kogan IYu. Venoznoe krovoobrashchenie ploda pri normal’nom protekayushchey i oslozhnennoy beremennosti. Saint Petersburg; 2002. (in Russ.)

[113] Полянин А.А., Коган И.Ю. Венозное кровообращение плода при нормально протекающей и осложненной беременности. Санкт-Петербург, 2002.

[114] Lees CC, Stampalija T, Baschat AA, et al. ISUOG practice guidelines: diagnosis and management of small-for-gestational-age fetus and fetal growth restriction. Ultrasound Obstet Gynecol. 2020;56(2):298–312. DOI: 10.1002/uog.22134

[115] Lees C.C. Stampalija T., Baschat A., et al. ISUOG Practice Guidelines: diagnosis and management of small-for-gestational-age fetus and fetal growth restriction // Ultrasound Obstet. Gynecol. 2020. Vol. 56. No. 2. P. 298–312. DOI: 10.1002/uog.22134

[116] Bhide A, Acharya G, Baschat A, et al. ISUOG practice guidelines (updated): use of doppler velocimetry in obstetrics. Ultrasound Obstet Gynecol. 2021;58(2):331–339. DOI: 10.1002/uog.23698

[117] Bhide A., Acharya G., Baschat A., et al. ISUOG Practice guidelines (updated): use of doppler velocimetry in obstetrics // Ultrasound Obstet. Gynecol. 2021. Vol. 58. No. 2. P. 331–339. DOI: 10.1002/uog.23698

[118] Belich AI. Evolutionary approach to the study of central nervous system foundation of the fetus. Journal of Obstetrics and Women’s Diseases. 2010;59(5):12–16.

[119] Белич А.И. Эволюционный подход к изучению становления центральной нервной системы плода // Журнал акушерства и женских болезней. 2010. Т. 59. № 5. C. 12–16.

[120] Jakab A, Schwartz E, Kasprian G, et al. Fetal functional imaging portrays heterogeneous development of emerging human brain networks. Front Hum Neurosci. 2014;8:852. DOI: 10.3389/fnhum.2014.00852

[121] Jakab A., Schwartz E., Kasprian G., et al. Fetal functional imaging portrays heterogeneous development of emerging human brain networks // Front. Hum. Neurosci. 2014. Vol. 8. P. 852. DOI: 10.3389/fnhum.2014.00852

[122] Canini M, Cavoretto P, Scifo P, et al. Subcortico-cortical functional connectivity in the fetal brain: a cognitive development blueprint. Cereb Cortex Commun. 2020;1(1). DOI: 10.1093/texcom/tgaa008

[123] Canini M., Cavoretto P., Scifo P., et al. Subcortico-cortical functional connectivity in the fetal brain: a cognitive development blueprint // Cereb. Cortex Commun. 2020. Vol. 1. No. 1. DOI: 10.1093/texcom/tgaa008

[124] Pavlova NG. Antenatal’naya diagnostika, profilaktika i lechenie funktsional’nykh narusheniy razvitiya TsNS ploda. [dissertation abstract]. Saint Petersburg; 2000. (In Russ.). [cited 2022 Oct 10]. Available from: https://viewer.rusneb.ru/ru/000200_000018_RU_NLR_bibl_246393?page=1&rotate=0&theme=white

[125] Павлова Н.Г. Антенатальная диагностика, профилактика и лечение функциональных нарушений развития ЦНС плода: автореф. дис. д-ра мед.наук. Санкт-Петербург, 2000. [дата обращения 10.10.2022]. Доступ по ссылке: https://viewer.rusneb.ru/ru/000200_000018_RU_NLR_bibl_246393?page=1&rotate=0&theme=white

[126] Garmasheva NL, Konstantinova NN. Vvedenie v perinatal’nuyu meditsinu. Moscow: 1978. (In Russ.)

[127] Гармашева Н.Л., Константинова Н.Н. Введение в перинатальную медицину. Москва, 1978.

[128] Brändle J, Preissl H, Draganova R, et al. Heart rate variability parameters and fetal movement complement fetal behavioral states detection via magnetography to monitor neurovegetative development. Front Hum Neurosci. 2015;9. DOI: 10.3389/fnhum.2015.00147

[129] Brändle J., Preissl H., Draganova R., et al. Heart rate variability parameters and fetal movement complement fetal behavioral states detection via magnetography to monitor neurovegetative development // Front. Hum. Neurosci. 2015. Vol. 9. P. 147. DOI: 10.3389/fnhum.2015.00147

[130] Belich AI, Natsvishvili VV. Stanovlenie tsikla “aktivnost’-pokoy” ploda cheloveka. Vestnik AMN SSSR. 1989;(3):35–42. (In Russ.)

[131] Белич А. И., Нацвишвили В.В. Становление цикла «активность-покой» плода человека // Вестник АМН СССР. 1989. № 3. P. 35–42

[132] Garmasheva NL, Konstantinova NN, Belich AI. K voprosu o mekhanizmakh stanovleniya reflektornoy deyatel’nosti. Zh evol biokhim i fiziol. 1998;34(1):96–106. (In Russ.)

[133] Гармашева Н.Л., Константинова Н.Н., Белич А.И. К вопросу о механизмах становления рефлекторной деятельности // Журнал эволюционной биохимии и физиологии. 1998. Т. 34. № 1. С. 96–106.

[134] Nijhuis JG, Prechtl HF, Martin CB, et al. Are there behavioural states in the human fetus? Early Hum Dev. 1982;6(2):177–195. DOI: 10.1016/0378-3782(82)90106-2

[135] Nijhuis J.G., Prechtl H.F., Martin C.B., et al. Are there behavioural states in the human fetus? // Early Hum. Dev. 1982. Vol. 6. No. 2. P. 177–195. DOI: 10.1016/0378-3782(82)90106-2

[136] Belich AI, Konstantinova NN, Natslishvili VV, et al. Morfofiziologicheskiy analiz formirovaniya mekhanizmov tsikla “aktivnost’-pokoy” v ontogeneze cheloveka. Vestnik RAMN. 1996;(3):55–61. (In Russ.)

[137] Белич А.И., Константинова Н.Н., Нацлишвили В.В., и др. Морфофизиологический анализ формирования механизмов цикла «активность-покой» в онтогенезе человека // Вестник РАМН. 1996. № 3. C. 55–61.

[138] Groome L, Gotlieb S, Neely C, et al. Developmental trends in fetal habituation to vibroacoustic stimulation. Am J Perinatol. 1993;10(01):46–49. DOI: 10.1055/s-2007-994700

[139] Groome L., Gotlieb S.J., Neely C.L., et al. Developmental trends in fetal habituation to vibroacoustic stimulation // Am. J. Perinatol. 1993. Vol. 10. No. 1. P. 46–49. DOI: 10.1055/s-2007-994700

[140] Morokuma S, Fukushima K, Kawai N, et al. Fetal habituation correlates with functional brain development. Behav Brain Res. 2004;153(2):459–463. DOI: 10.1016/j.bbr.2004.01.002

[141] Morokuma S., Fukushima K., Kawai N., et al. Fetal habituation correlates with functional brain development // Behav. Brain Res. 2004. Vol. 153. No. 2. P. 459–463. DOI: 10.1016/j.bbr.2004.01.002

[142] Thompson RF, Spencer WA. Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev. 1966;73(1):16–43. DOI: 10.1037/h0022681

[143] Thompson R.F., Spencer W.A. Habituation: a model phenomenon for the study of neuronal substrates of behavior // Psychol. Rev. 1966. Vol. 73. No. 1. P. 16–43. DOI: 10.1037/h0022681

[144] Robinson DA. The use of control systems analysis in the neurophysiology of eye movements. Annu Rev Neurosci. 1981;4(1):463–503. DOI: 10.1146/annurev.ne.04.030181.002335

[145] Robinson D.A. The use of control systems analysis in the neurophysiology of eye movements // Annu. Rev. Neurosci. 1981. Vol. 4. No. 1. P. 463–503. DOI: 10.1146/annurev.ne.04.030181.002335

[146] Maehara K, Morokuma S, Nakahara K, et al. A study on the association between eye movements and regular mouthing movements (RMMs) in normal fetuses between 24 to 39 weeks of gestation. Ed. by M.Y. Oncel. PLoS One. 2020;15(5). DOI: 10.1371/journal.pone.0233909

[147] Maehara K., Morokuma S., Nakahara K., et al. A study on the association between eye movements and regular mouthing movements (RMMs) in normal fetuses between 24 to 39 weeks of gestation // PLoS One. 2020. Vol. 15. No. 5. DOI: 10.1371/journal.pone.0233909

[148] Krueger C, Holditch-Davis D, Quint S, et al. Recurring auditory experience in the 28- to 34-week-old fetus. Infant Behav Dev. 2004;27(4):537–543. DOI: 10.1016/j.infbeh.2004.03.001

[149] Krueger C., Holditch-Davis D., Quint S., et al. Recurring auditory experience in the 28- to 34-week-old fetus // Infant Behav. Dev. 2004. Vol. 27. No. 4. P. 537–543. DOI: 10.1016/j.infbeh.2004.03.001

[150] James DK, Spencer CJ, Stepsis BW. Fetal learning: a prospective randomized controlled study. Ultrasound Obstet Gynecol. 2002;20(5):431–438. DOI: 10.1046/j.1469-0705.2002.00845.x

[151] James D.K., Spencer C.J., Stepsis B.W. Fetal learning: a prospective randomized controlled study // Ultrasound Obstet. Gynecol. 2002. Vol. 20. No. 5. P. 431–438. DOI: 10.1046/j.1469-0705.2002.00845.x

[152] Otera Y, Morokuma S, Fukushima K, et al. Correlation between regular mouthing movements and heart rate patterns during non-rapid eye movement periods in normal human fetuses between 32 and 40 weeks of gestation. Early Hum Dev. 2013;89(6):381–386. DOI: 10.1016/j.earlhumdev.2012.12.007

[153] Otera Y., Morokuma S., Fukushima K., et al. Correlation between regular mouthing movements and heart rate patterns during non-rapid eye movement periods in normal human fetuses between 32 and 40 weeks of gestation // Early Hum. Dev. 2013. Vol. 89. No. 6. P. 381–386. DOI: 10.1016/j.earlhumdev.2012.12.007

[154] Al-Qahtani NH. Foetal response to music and voice. Aust New Zeal J Obstet Gynaecol. 2005;45(5):414–417. DOI: 10.1111/j.1479-828X.2005.00458.x

[155] Al-Qahtani N.H. Foetal response to music and voice // Aust. New Zeal. J. Obstet. Gynaecol. 2005. Vol. 45. No. 5. P. 414–417. DOI: 10.1111/j.1479-828X.2005.00458.x

RIGHTS & PERMISSIONS

Eсо-Vector