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Quantitative in vivo MRI measurement of cortical development in the fetus
Abstract
Normal brain development is associated with expansion and folding of the cerebral cortex following a highly orchestrated sequence of gyral-sulcal formation. Although several studies have described the evolution of cerebral cortical development ex vivo or ex utero, to date, very few studies have characterized and quantified the gyrification process for the in vivo fetal brain. Recent advances in fetal magnetic resonance imaging and post-processing computational methods are providing new insights into fetal brain maturation in vivo. In this study, we investigate the in vivo fetal cortical folding pattern in healthy fetuses between 25 and 35 weeks gestational age using 3-D reconstructed fetal cortical surfaces. We describe the in vivo fetal gyrification process using a robust feature extraction algorithm applied directly on the cortical surface, providing an explicit delineation of the sulcal pattern during fetal brain development. We also delineate cortical surface measures, including surface area and gyrification index. Our data support an exuberant third trimester gyrification process and suggest a non-linear evolution of sulcal development. The availability of normative indices of cerebral cortical developing in the living fetus may provide critical insights on the timing and progression of impaired cerebral development in the high-risk fetus.
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“A study of healthy fetuses at 25–35 GW shows an exuberant third-trimester gyrification process and suggests a non-linear evolution of sulcal development [53].”
From Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy (2024) · cites this paper as [53]
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Cites
A Coefficient of Agreement for Nominal Scales
Cohen, J. (1960) · Educational and Psychological Measurement · doi:10.1177/001316446002000104 · Cited by 42,398
Measures of the Amount of Ecologic Association Between Species
Dice, L. R. (1945) · Ecology · doi:10.2307/1932409 · Cited by 12,187
Zhang, Y., Brady, M., & Smith, S. M. (2001) · IEEE Transactions on Medical Imaging · doi:10.1109/42.906424 · Cited by 7,628
Fundamentals of digital image processing
Jain, A. K. (1988) · Cited by 7,000
Cortical Surface-Based Analysis
Fischl, B., Sereno, M. I., & Dale, A. M. (1999) · NeuroImage · doi:10.1006/nimg.1998.0396 · Cited by 6,147
A nonparametric method for automatic correction of intensity nonuniformity in MRI data
Sled, J. G., Zijdenbos, A. P., & Evans, A. C. (1998) · IEEE Transactions on Medical Imaging · doi:10.1109/42.668698 · Cited by 4,731
Self-citationSpecification of Cerebral Cortical Areas
Rakic, P. (1988) · Science · doi:10.1126/science.3291116 · Cited by 3,127 · cited 3×
“2010a), and is believed to be the result of a strong genetic influence (Rakic 1988; Regis et al. 2005).”
BackgroundA tension-based theory of morphogenesis and compact wiring in the central nervous system
Essen, D. C. V. (1997) · Nature · doi:10.1038/385313a0 · Cited by 1,668
Gyral development of the human brain
Je, G., Dooling, E. C., & Gilles, F. H. (1977) · Annals of Neurology · doi:10.1002/ana.410010109 · Cited by 1,099
Automated 3-D Extraction of Inner and Outer Surfaces of Cerebral Cortex from MRI
MacDonald, D. J., Kabani, N. J., Avis, D., & Evans, A. C. (2000) · NeuroImage · doi:10.1006/nimg.1999.0534 · Cited by 850
Self-citationThe human pattern of gyrification in the cerebral cortex
Zilles, K., Armstrong, E., Schleicher, A., & Hj, K. (1988) · Anatomy and Embryology · doi:10.1007/bf00304699 · Cited by 731
Limperopoulos, C., Tworetzky, W., McElhinney, D. B., Newburger, J. W., Brown, D. W., Robertson, R. L., Guizard, N., McGrath, E., Geva, J., Annese, D., et al. (2010) · Circulation · doi:10.1161/circulationaha.109.865568 · Cited by 663
Self-citationThe Ontogeny of Human Gyrification
Armstrong, E., Schleicher, A., Omran, H., Curtis, M., & Zilles, K. (1995) · Cerebral Cortex · doi:10.1093/cercor/5.1.56 · Cited by 646
Mechanical Model of Brain Convolutional Development
Richman, D. P., Stewart, R. M., Hutchinson, J. W., & Caviness, V. S. (1975) · Science · doi:10.1126/science.1135626 · Cited by 575
The NIH MRI study of normal brain development
Evans, A. C. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.09.068 · Cited by 526
Self-citationPrimary cortical folding in the human newborn: an early marker of later functional development
Dubois, J., Benders, M. J. N. L., Borradori-Tolsa, C., Cachia, A., Lazeyras, F., Leuchter, R. H., Sizonenko, S. V., Warfield, S. K., Mangin, J., & Hüppi, P. S. (2008) · Brain · doi:10.1093/brain/awn137 · Cited by 490
Self-citationMapping the Early Cortical Folding Process in the Preterm Newborn Brain
Dubois, J., Benders, M. J. N. L., Cachia, A., Lazeyras, F., Leuchter, R. H., Sizonenko, S. V., Borradori-Tolsa, C., Mangin, J., & Hüppi, P. S. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm180 · Cited by 468
An unbiased iterative group registration template for cortical surface analysis
Lyttelton, O. C., Boucher, M., Robbins, S. M., & Evans, A. C. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.10.041 · Cited by 415
Self-citationA curvature-based approach to estimate local gyrification on the cortical surface
Eileen Luders, A., Thompson, P. M., Narr, K. L., Toga, A. W., Jäncke, L., & Christian Gaser, B. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.08.049 · Cited by 375
Genetic variability of human brain size and cortical gyral patterns
Bartley, A. J. (1997) · Brain · doi:10.1093/brain/120.2.257 · Cited by 355
Gholipour, A., Estroff, J. A., & Warfield, S. K. (2010) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2010.2051680 · Cited by 351
Self-citationThree-dimensional statistical analysis of sulcal variability in the human brain
Thompson, P. M., Schwartz, C., Lin, R. T., Khan, A. A., & Toga, A. W. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-13-04261.1996 · Cited by 346
Hill, J., Dierker, D. L., Neil, J. J., Inder, T. E., Knutsen, A. K., Harwell, J., Coalson, T. S., & Essen, D. C. V. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4682-09.2010 · Cited by 294
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
Axons Pull on the Brain, But Tension Does Not Drive Cortical Folding
Xu, G., Knutsen, A. K., Dikranian, K. T., Kroenke, C. D., Bayly, P. V., & Taber, L. A. (2010) · Journal of Biomechanical Engineering · doi:10.1115/1.4001683 · Cited by 280
A novel cubic-order algorithm for approximating principal direction vectors
Goldfeather, J., & Interrante, V. (2004) · ACM Transactions on Graphics · doi:10.1145/966131.966134 · Cited by 278
Registration-Based Approach for Reconstruction of High-Resolution In Utero Fetal MR Brain Images
Rousseau, F., Glenn, O. A., Iordanova, B. E., Rodriguez-Carranza, C. E., Vigneron, D. B., Barkovich, A. J., & Studholme, C. (2006) · Academic Radiology · doi:10.1016/j.acra.2006.05.003 · Cited by 240
Régis, J. M., Mangin, J., Ochiai, T., Frouin, V., Rivière, D., Cachia, A., Tamura, M., & Samson, Y. (2005) · Neurologia medico-chirurgica · doi:10.2176/nmc.45.1 · Cited by 224
Kostović, I., & Judáš, M. (2002) · The Anatomical Record · doi:10.1002/ar.10069 · Cited by 215
Automatic recognition of cortical sulci of the human brain using a congregation of neural networks
Rivière, D., Mangin, J., Orfanos, D. P., Martinez, J., Frouin, V., & Régis, J. M. (2002) · Medical Image Analysis · doi:10.1016/s1361-8415(02)00052-x · Cited by 215
The embryonic human brain : an atlas of developmental stages
O’Rahilly, R., & Müller, F. (2006) · Cited by 203
The Prenatal Origin of Hemispheric Asymmetry: An In Utero Neuroimaging Study
Kasprian, G. J., Langs, G., Brugger, P. C., Bittner, M., Weber, M., Arantes, M., & Prayer, D. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq179 · Cited by 189
Fast and robust detection of crest lines on meshes
Yoshizawa, S., Belyaev, A. G., & Seidel, H. (2005) · ACM Symposium on Solid and Physical Modeling (SPM) · doi:10.1145/1060244.1060270 · Cited by 188
Deep Sulcal Landmarks Provide an Organizing Framework for Human Cortical Folding
Lohmann, G., von Cramon, D. Y., & Colchester, A. C. F. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm174 · Cited by 185
Local Tissue Growth Patterns Underlying Normal Fetal Human Brain Gyrification QuantifiedIn Utero
Rajagopalan, V., Scott, J. A., Habas, P. A., Kim, K., Corbett-Detig, J., Rousseau, F., Barkovich, A. J., Glenn, O. A., & Studholme, C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5458-10.2011 · Cited by 166
Habas, P. A., Kim, K., Corbett-Detig, J., Rousseau, F., Glenn, O. A., Barkovich, A. J., & Studholme, C. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.06.054 · Cited by 160
Structural asymmetries of perisylvian regions in the preterm newborn
Dubois, J., Benders, M. J. N. L., Lazeyras, F., Borradori-Tolsa, C., Leuchter, R. H., Mangin, J., & Hüppi, P. S. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.03.054 · Cited by 156
ESTIMATING CURVATURE ON TRIANGULAR MESHES
Gatzke, T., & Grimm, C. M. (2006) · International Journal of Shape Modeling · doi:10.1142/s0218654306000810 · Cited by 148
Depth potential function for folding pattern representation, registration and analysis
Boucher, M., Whitesides, S. H., & Evans, A. C. (2008) · Medical Image Analysis · doi:10.1016/j.media.2008.09.001 · Cited by 125
Self-citationDifferential growth between the fetal brain and its infratentorial part
Guihard-Costa, A.-M., & Larroche, J. (1990) · Early Human Development · doi:10.1016/0378-3782(90)90126-4 · Cited by 111
Lee, J. K., Lee, J.-M., Kim, J. S., Kim, I. Y., Evans, A. C., & Kim, S. I. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.12.044 · Cited by 108
Self-citationExtraction of Feature Lines on Triangulated Surfaces Using Morphological Operators
Rössl, C., Ossl, C. R., Kobbelt, L., Seidel, H., & Stadtwald, I. (2000) · Cited by 106
Barron, D. H. (1950) · Journal of Experimental Zoology · doi:10.1002/jez.1401130304 · Cited by 97
Quantitative MRI measurements of human fetal brain development in utero
Grossman, R., Hoffman, C., Mardor, Y., & Biegon, A. R. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.07.005 · Cited by 89
Measures of folding applied to the development of the human fetal brain
Batchelor, P. G., Smith, A. D., Hill, D., Hawkes, D. J., Cox, T. C. S., & Dean, A. F. (2002) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2002.803108 · Cited by 89
Fetal brain volumetry through MRI volumetric reconstruction and segmentation
Gholipour, A., Estroff, J. A., Barnewolt, C. E., Connolly, S. A., & Warfield, S. K. (2010) · International Journal of Computer Assisted Radiology and Surgery · doi:10.1007/s11548-010-0512-x · Cited by 78
Self-citation3D global and regional patterns of human fetal subplate growth determined in utero
Corbett-Detig, J., Habas, P. A., Scott, J. A., Kim, K., Rajagopalan, V., McQuillen, P. S., Barkovich, A. J., Glenn, O. A., & Studholme, C. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0286-5 · Cited by 72
Investigation of normal organ development with fetal MRI
Prayer, D., & Brugger, P. C. (2007) · European Radiology · doi:10.1007/s00330-007-0604-3 · Cited by 66
Shankle, W. R., Landing, B. H., Rafii, M. S., Schiano, A. V. R., Chen, J., & Hara, J. (1998) · Journal of Theoretical Biology · doi:10.1006/jtbi.1997.0570 · Cited by 60
Advancing Fetal Brain MRI: Targets for the Future
Limperopoulos, C., & Clouchoux, C. (2009) · Seminars in Perinatology · doi:10.1053/j.semperi.2009.04.002 · Cited by 52
Self-citationGeometric atlas: modeling the cortex as an organized surface
Toro, R., & Burnod, Y. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.07.008 · Cited by 49
MR Volumetry of Brain and CSF in Fetuses Referred for Ventriculomegaly
Kazan-Tannus, J. F., Dialani, V. M., Kataoka, M. L., Chiang, G. C.-Y., Feldman, H. A., Brown, J. S., & Levine, D. (2007) · American Journal of Roentgenology · doi:10.2214/ajr.07.2073 · Cited by 46
Fetal MRI: what is the future?
Garel, C. (2008) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.5249 · Cited by 37
Identification of Growth Seeds in the Neonate Brain through Surfacic Helmholtz Decomposition
Lefèvre, J., Leroy, F., Khan, S., Dubois, J., Hüppi, P. S., Baillet, S., & Mangin, J. (2009) · Lecture notes in computer science · doi:10.1007/978-3-642-02498-6_21 · Cited by 30
Model-driven parameterization of the cortical surface for localization and inter-subject matching
Clouchoux, C., Rivière, D., Mangin, J., Operto, G., Régis, J. M., & Coulon, O. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.12.048 · Cited by 27
Self-citationMorphological regionalization using fetal magnetic resonance images of normal developing brains
Hu, H., Guo, W., Chen, H., Wang, P., Hung, C., Hsieh, J., & Wu, Y. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06707.x · Cited by 26
Zhang, Z., Liu, S., Lin, X., Sun, B., Yu, T., & Geng, H. (2010) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2010.05.001 · Cited by 25
In-utero Three Dimension High Resolution Fetal Brain Diffusion Tensor Imaging
Jiang, S., Xue, H., Counsell, S. J., Anjari, M., Allsop, J. M., Rutherford, M., Rueckert, D., & Hajnal, J. V. (2007) · Springer eBooks · doi:10.1007/978-3-540-75757-3_3 · Cited by 21
Awate, S. P., Yushkevich, P. A., Song, Z., Licht, D. J., & Gee, J. C. (2009) · Lecture notes in computer science · doi:10.1007/978-3-642-02498-6_46 · Cited by 21
3D Feature Line Detection Based on Vertex Labeling and 2D Skeletonization
Kudelski, D., Mari, J.-L., & Viseur, S. (2010) · doi:10.1109/smi.2010.35 · Cited by 16
Self-citationA novel approach for high-resolution image reconstruction for in-vivo fetal brain MRI
Clouchoux, C., Pierrick Coupé, A., Manjón, J. V., Guizard, N., Bouyssi-Kobar, M., Lefebvre, M., du Plessis, A. J., Evans, A., & Limperopoulos, C. (2010) · Cited by 3
Self-citationClouchoux, C., Kudelski, D., Bouyssi-Kobar, M., Viseur, S., du Plessis, A., Evans, A. C., Mari, J.-L., & Limperopoulos, C. (2010) · Cited by 2
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Research works printed but not linked: 1
- Guizard N, Lepage C, Fonov V, Hakyemez H, Evans A, Limperopoulos C (2008) Development of fetus brain atlas from multi-axial MR acquisitions. In: Proceedings of the Sixteenth Annual Meeting of the International Society for Magnetic Resonance in Medicine 672:132
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Metadata
- Authors
- Clouchoux, C., Kudelski, D., Gholipour, A., Warfield, S. K., Viseur, S., Bouyssi-Kobar, M., Mari, J.-L., Evans, A. C., du Plessis, A. J., & Limperopoulos, C.
- Affiliations
- Children's National (US)
- Centre National de la Recherche Scientifique (FR)
- Boston Children's Hospital (US)
- Université de Provence Aix-Marseille I (FR)
- Montreal Neurological Institute and Hospital (CA)
- Corresponding author
- Limperopoulos, Catherine
- ORCID
- Venue
- Brain Structure and Function
- Published
- 2011-05-12
- Volume
- 217
- Issue
- 1
- Pages
- 127-139
- ISSN
- 1863-2653 (ISSN-L)
- 1863-2661
- OpenAlex
- W2051630621
- Cited by
- 164
- References
- 62
- Citations by year
- 2026: 11 · 2025: 8 · 2024: 10 · 2023: 7 · 2022: 15 · 2021: 23 · 2020: 14 · 2019: 12 · 2018: 14 · 2017: 8 · 2016: 11 · 2015: 11 · 2014: 5 · 2013: 4 · 2012: 8
- FWCI
- 5.61
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Brain Structure and Function (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Canadian Institutes of Health Research (81116_1)
- 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, cerebral cortex, cortical folding, fetal MRI, cortical surface reconstruction, gyrification index, cortical surface area, third trimester, fetal brain maturation
- MeSH terms
- Age Factors, Algorithms, Cerebral Cortex, Female, Fetus, Humans, Magnetic Resonance Imaging, Pregnancy, Fetal Development
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