In vitro MRI of brain development
Abstract
In this review, we demonstrate the developmental appearance, structural features, and reorganization of transient cerebral zones and structures in the human fetal brain using a correlative histological and MRI analysis. The analysis of postmortem aldehyde-fixed specimens (age range: 10 postovulatory weeks to term) revealed that, at 10 postovulatory weeks, the cerebral wall already has a trilaminar appearance and consists of: (1) a ventricular zone of high cell-packing density; (2) an intermediate zone; (3) the cortical plate (in a stage of primary consolidation) with high MRI signal intensity. The anlage of the hippocampus is present as a prominent bulging in the thin limbic telencephalon. The early fetal telencephalon impar also contains the first commissural fibers and fornix bundles in the septal area. The ganglionic eminence is clearly visible as an expanded continuation of the proliferative ventricular zone. The basal ganglia showed an initial aggregation of cells. The most massive fiber system is in the hemispheric stalk, which is in continuity with thalamocortical fibers. During the mid-fetal period (15-22 postovulatory weeks), the typical fetal lamination pattern develops and the cerebral wall consists of the following zones: (a) a marginal zone (visible on MRI exclusively in the hippocampus); (b) the cortical plate with high cell-packing density and high MRI signal intensity; (c) the subplate zone, which is the most prominent zone rich in extracellular matrix and with a very low MRI signal intensity; (d) the intermediate zone (fetal "white matter"); (e) the subventricular zone; (f) the periventricular fiber-rich zone; (g) the ventricular zone. The ganglionic eminence is still a very prominent structure with an intense proliferative activity. During the next period (22-26 postovulatory weeks), there is the developmental peak of transient MRI features, caused by the high content of hydrophyllic extracellular matrix in the subplate zone and the accumulation of waiting afferent axons. The period between 27 and 30 postovulatory weeks is characterized by gradual blurring of the laminar structure in parallel with the formation of cerebral convolutions. In near-term preterm infants, T2-weighted MR images showed better contrast resolution than T1-weighted images. We conclude that transient fetal zones and subcortical structures display characteristic MRI features due to the high content of extracellular matrix in the subplate zone, higher MRI signal intensity of zones with high cell-packing intensity, and the presence of growing fibers.
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Ontogenesis follows the phylogenetic axis: histological and MRI analyses of normal foetal brain development have highlighted the early maturation of the hippocampus and thalamus.
“Ontogenesis follows the phylogenetic axis: histological and MRI analyses [60,62] of normal foetal brain development have highlighted the early maturation of the hippocampus and thalamus (see also [82]).”
From Voxel-based mapping of brain gray matter volume and glucose metabolism profiles in normal aging (2009) · cites this paper as [62]
Cites
(2005) · Choice Reviews Online · doi:10.5860/choice.43-0626 · Cited by 4,726 · see citing works
Kostović, I., & RAKIC, P. T. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902970309 · Cited by 912 · see citing works
Self-citationAbnormal Cerebral Structure Is Present at Term in Premature Infants
Inder, T. E., Warfield, S. K., Wang, H., Hüppi, P. S., & Volpe, J. J. (2005) · PEDIATRICS · doi:10.1542/peds.2004-0326 · Cited by 883 · see citing works
Kostović, I. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.5.536 · Cited by 408 · see citing works
Self-citationThe development of synapses in cerebral cortex of the human fetus
Molliver, M. E., Kostović, I., & der Loos, H. V. (1973) · Brain Research · doi:10.1016/0006-8993(73)90741-5 · Cited by 385 · see citing works
Self-citationSelective Vulnerability of Subplate Neurons after Early Neonatal Hypoxia-Ischemia
McQuillen, P. S., Sheldon, R. A., Shatz, C. J., & Ferriero, D. M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03308.2003 · Cited by 381 · see citing works
Hüppi, P. S., Murphy, B. P., Maier, S. E., Zientara, G. P., Inder, T. E., Barnes, P. D., Kikinis, R., Jolesz, F. A., & Volpe, J. J. (2001) · PEDIATRICS · doi:10.1542/peds.107.3.455 · Cited by 362 · see citing works
Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging.
Garel, C., Chantrel, E., Brisse, H. J., Elmaleh, M., Luton, D., Oury, J., Sebag, G. H., & Hassan, M. (2001) · PubMed Central · Cited by 286 · see citing works
Kostovic, I., & Rakic, P. (1984) · The Journal of Neuroscience · doi:10.1523/jneurosci.04-01-00025.1984 · Cited by 270 · see citing works
Kostović, I., & Judáš, M. (2002) · The Anatomical Record · doi:10.1002/ar.10069 · Cited by 215 · see citing works
Self-citationJudáš, M., Radoš, M., Milošević, N. J., Hrabač, P., Štern-Padovan, R., & Kostović, I. (2005) · PubMed Central · Cited by 190 · see citing works
Self-citationMagnetic resonance imaging of preterm brain injury
Counsell, S. J., Rutherford, M. A., Cowan, F. M., et al. (2003) · Archives of Disease in Childhood Fetal & Neonatal · doi:10.1136/fn.88.4.f269 · Cited by 166 · see citing works
Maas, L., Mukherjee, P., Carballido-Gamio, J., Veeraraghavan, S., Miller, S. P., Partridge, S., Henry, R. G., Barkovich, A., & Vigneron, D. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.02.035 · Cited by 148 · see citing works
de Vries, L. S., Groenendaal, F., van Haastert, I. C., Eken, P., Rademaker, K. J., & Meiners, L. C. (1999) · Neuropediatrics · doi:10.1055/s-2007-973511 · Cited by 133 · see citing works
Brisse, H. J., Fallet‐Bianco, C., Sebag, G. H., Nessmann, C., Blot, P., & Hassan, M. (1997) · PubMed Central · Cited by 101 · see citing works
Melhem, E. R., Hoon, A. H., Ferrucci, J. T., Quinn, C. B., Reinhardt, E. M., Demetrides, S., Freeman, B. M., & Johnston, M. V. (2000) · Radiology · doi:10.1148/radiology.214.1.r00dc35199 · Cited by 97 · see citing works
Kostović, I., Lukinović, N., Judáš, M., Bogdanović, N., Mrzljak, L., Zečević, N., & Kubat, M. (1989) · Metabolic Brain Disease · doi:10.1007/bf00999489 · Cited by 95 · see citing works
Self-citationMR imaging of fetal brain malformations
Raybaud, C., Levrier, O., Brunel, H., et al. (2003) · Child s Nervous System · doi:10.1007/s00381-003-0769-2 · Cited by 85 · see citing works
Childs, A. M., Ramenghi, L. A., Evans, D., et al. (1998) · PubMed · Cited by 71 · see citing works
Regional Size Reduction in the Human Corpus Callosum Following Pre- and Perinatal Brain Injury
Moses, P. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.12.1200 · Cited by 57 · see citing works
Early areal differentiation of the human cerebral cortex: Entorhinal area
Kostović, I., Petanjek, Z., & Judáš, M. (1993) · Hippocampus · doi:10.1002/hipo.450030406 · Cited by 56 · see citing works
Self-citationNikolić, I., & Kostović, I. (1986) · Anatomy and Embryology · doi:10.1007/bf00698785 · Cited by 48 · see citing works
Self-citationContinuing Education in Neurometabolic Disorders - Serine Deficiency Disorders
de Koning, T., Poll‐The, B. T., & Jaeken, J. (1999) · Neuropediatrics · doi:10.1055/s-2007-973447 · Cited by 30 · see citing works
Cerebral cortex three‐dimensional profiling in human fetuses by magnetic resonance imaging
Sbarbati, A., Pizzini, F. B., Fabene, P. F., Nicolato, E., Marzola, P., Calderan, L., Simonati, A., Longo, L., Osculati, A. M. M., & Beltramello, A. (2004) · Journal of Anatomy · doi:10.1111/j.0021-8782.2004.00301.x · Cited by 18 · see citing works
MR appearance of the internal architecture of Ammon's horn.
Miller, M. J., Mark, L. P., Ho, K., & Haughton, V. M. (1996) · PubMed Central · Cited by 11 · see citing works
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Dubois, J., Dehaene-Lambertz, G., Kulikova, S., Poupon, C., Hüppi, P. S., & Hertz-Pannier, L. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.044 · Cited by 851 · see citing works
Voxel-based mapping of brain gray matter volume and glucose metabolism profiles in normal aging
Kalpouzos, G., Chételat, G., Baron, J.-C., Landeau, B., Mevel, K., Godeau, C., Barré, L., Constans, J.-M., Viader, F., Eustache, F., et al. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.05.019 · Cited by 392 · see citing works
MRI of normal fetal brain development
Prayer, D., Kasprian, G., Krampl, E., Ulm, B., Witzani, L., Prayer, L., & Brugger, P. C. (2006) · European Journal of Radiology · doi:10.1016/j.ejrad.2005.11.020 · Cited by 240 · see citing works
Exploring early human brain development with structural and physiological neuroimaging
Vasung, L., Abaci Turk, E., Ferradal, S. L., Sutin, J., Stout, J. N., Ahtam, B., Lin, P.-Y., & Grant, P. E. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2018.07.041 · Cited by 177 · see citing works
Watching the fetal brain at ‘rest’
Schöpf, V., Kasprian, G., Brugger, P. C., & Prayer, D. (2012) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.10.006 · Cited by 137 · see citing works
Douet, V., & Chang, L. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00343 · Cited by 122 · see citing works
- Authors
- Radoš, M., Judaš, M., & Kostović, I.
- Affiliations
- University Hospital Centre Zagreb (HR)
- University of Zagreb (HR)
- Corresponding author
- Kostović, Ivica
- Venue
- European Journal of Radiology
- Publisher
- Elsevier BV
- Published
- 2006-02
- Volume
- 57
- Issue
- 2
- Pages
- 187-198
- ISSN
- 0720-048X (ISSN-L)
- OpenAlex
- W1965271433
- Cited by
- 152
- References
- 25
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 6 · 2023: 7 · 2022: 6 · 2021: 10 · 2020: 8 · 2019: 7 · 2018: 4 · 2017: 5 · 2016: 3 · 2015: 6 · 2014: 7 · 2013: 10 · 2012: 8
- FWCI
- 8.06
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Radiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Keywords
- fetal brain development, fetal brain MRI, extracellular matrix, cortical lamination, ventricular zone, ganglionic eminence, hippocampus, basal ganglia, commissural fibers, fornix, T2-weighted imaging, T1-weighted imaging, cerebral convolutions, histopathological correlation, human fetal brain, preterm infants, MRI signal intensity
- MeSH terms
- Brain, Fetus, Humans, Magnetic Resonance Imaging, Fetal Development, In Vitro Techniques
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