Patterns of development and formation of the fetal central nervous system integrative function in the antenatal period
- Authors: Yusenko S.R.1, Nagorneva S.V.1, Kogan I.Y.1
-
Affiliations:
- The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O.Ott
- Issue: Vol 71, No 5 (2022)
- Pages: 97-110
- Section: Reviews
- URL: https://journals.rcsi.science/jowd/article/view/125964
- DOI: https://doi.org/10.17816/JOWD107183
- ID: 125964
Cite item
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 20th 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.
Full Text
##article.viewOnOriginalSite##About the authors
Sofya R. Yusenko
The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O.Ott
Author for correspondence.
Email: iusenko.sr@gmail.com
Russian Federation, Saint Petersburg
Stanislava V. Nagorneva
The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O.Ott
Email: stanislava_n@bk.ru
ORCID iD: 0000-0003-0402-5304
SPIN-code: 5109-7613
ResearcherId: К-3723-2018
MD, Cand. Sci. (Med.)
Russian Federation, Saint PetersburgIgor Yu. Kogan
The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O.Ott
Email: ikogan@mail.ru
ORCID iD: 0000-0002-7351-6900
SPIN-code: 6572-6450
Scopus Author ID: 56895765600
ResearcherId: P-4357-2017
MD, Dr. Sci. (Med.), Professor, Corresponding Member of the Russian Academy of Sciences
Russian Federation, Saint-PetersburgReferences
- 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
- Stiles J, Jernigan TL. The basics of brain development. Neuropsychol Rev. 2010;20(4):327–348. doi: 10.1007/s11065-010-9148-4
- 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
- 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
- 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
- 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
- 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
- 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
- Barkovich AJ, Raybaud C, editors. Pediatric neuroimaging. 5th ed. Philadelphia; 2012.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Collin G, van den Heuvel MP. The ontogeny of the human connectome. Neurosci. 2013;19(6):616–628. doi: 10.1177/1073858413503712
- 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
- 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
- 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
- Larsen WJ. Human embryology. 3rd ed. Philadelphia: Churchill Livingstone; 2001.
- Marín-Padilla M. The human brain intracerebral microvascular system: development and structure. Front Neuroanat. 2012;6:38. doi: 10.3389/fnana.2012.00038
- 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
- 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
- Bautch VL, James JM. Neurovascular development. Cell Adh Migr. 2009;3(2):199–204. doi: 10.4161/cam.3.2.8397
- 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
- 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
- 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
- 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.
- 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
- Vanderah T. Nolte’s essentials of the human brain. 1st ed. 2009.
- 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
- Ageeva MI. Dopplerograficheskoe issledovanie gemodinamiki ploda: posobie dlya vrachey. 2006.
- Burlev VA, Zaydieva S, Il’yasova NA. Regulyatsiya angiogeneza gestatsionnogo perioda. Problemy reproduktsii. 2008;3:15–22.
- Cipolla MJ. The cerebral circulation. Colloq Ser Integr Syst Physiol From Mol to Funct. 2009;1(1):1–59. doi: 10.4199/C00005ED1V01Y200912ISP002
- Pooh RK, Pooh KH. Fetal neuroimaging. Fetal Matern Med Rev. 2008;19(1):1–31. doi: 10.1017/S0965539508002106
- Barashnev YuI. Perinatal’naya nevrologiya. Moscow: Triada-Kh; 2005. (in Russ.)
- Polyanin AA, Kogan IYu. Venoznoe krovoobrashchenie ploda pri normal’nom protekayushchey i oslozhnennoy beremennosti. Saint Petersburg; 2002. (in Russ.)
- 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
- 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
- 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.
- 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
- 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
- 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
- Garmasheva NL, Konstantinova NN. Vvedenie v perinatal’nuyu meditsinu. Moscow: 1978. (In Russ.)
- 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
- Belich AI, Natsvishvili VV. Stanovlenie tsikla “aktivnost’-pokoy” ploda cheloveka. Vestnik AMN SSSR. 1989;(3):35–42. (In Russ.)
- 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.)
- 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
- 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.)
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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