Skip to main content
Top
Published in: Brain Structure and Function 1/2012

01-01-2012 | Original Article

Quantitative in vivo MRI measurement of cortical development in the fetus

Authors: Cédric Clouchoux, Dimitri Kudelski, Ali Gholipour, Simon K. Warfield, Sophie Viseur, Marine Bouyssi-Kobar, Jean-Luc Mari, Alan C. Evans, Adre J. du Plessis, Catherine Limperopoulos

Published in: Brain Structure and Function | Issue 1/2012

Login to get access

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.
Literature
go back to reference Armstrong E, Schleicher A, Omran H, Curtis M, Zilles K (1995) The ontogeny of human gyrification. Cereb Cortex 5:56–63PubMedCrossRef Armstrong E, Schleicher A, Omran H, Curtis M, Zilles K (1995) The ontogeny of human gyrification. Cereb Cortex 5:56–63PubMedCrossRef
go back to reference Awate SP, Yushkevich P, Song Z, Licht D, Gee JC (2009) Multivariate high-dimensional cortical folding analysis, combining complexity and shape, in neonates with congenital heart disease. Inf Process Med Imaging 21:552–563PubMedCrossRef Awate SP, Yushkevich P, Song Z, Licht D, Gee JC (2009) Multivariate high-dimensional cortical folding analysis, combining complexity and shape, in neonates with congenital heart disease. Inf Process Med Imaging 21:552–563PubMedCrossRef
go back to reference Barron DH (1950) An experimental analysis of some factors involved in the development of the fissure pattern of the cerebral cortex. J Exp Zool 113:553–581CrossRef Barron DH (1950) An experimental analysis of some factors involved in the development of the fissure pattern of the cerebral cortex. J Exp Zool 113:553–581CrossRef
go back to reference Bartley AJ, Jones DW, Weinberger DR (1997) Genetic variability of human brain size and cortical gyral patterns. Brain 120:257–269PubMedCrossRef Bartley AJ, Jones DW, Weinberger DR (1997) Genetic variability of human brain size and cortical gyral patterns. Brain 120:257–269PubMedCrossRef
go back to reference Batchelor PG, Castellano Smith AD, Hill DL, Hawkes DJ, Cox TC, Dean AF (2002) Measures of folding applied to the development of the human fetal brain. IEEE Trans Med Imaging 21(8):953–965PubMedCrossRef Batchelor PG, Castellano Smith AD, Hill DL, Hawkes DJ, Cox TC, Dean AF (2002) Measures of folding applied to the development of the human fetal brain. IEEE Trans Med Imaging 21(8):953–965PubMedCrossRef
go back to reference Boucher M, Whiteside S, Evans AC (2009) Depth potential function for folding pattern representation, registration and analysis. Med Image Anal 13(2):203–214PubMedCrossRef Boucher M, Whiteside S, Evans AC (2009) Depth potential function for folding pattern representation, registration and analysis. Med Image Anal 13(2):203–214PubMedCrossRef
go back to reference Clouchoux C, Rivière D, Mangin JF, Operto G, Régis J, Coulon O (2010a) Model-driven parameterization of the cortical surface for localization and inter-subject matching. Neuroimage 50(2):552–566PubMedCrossRef Clouchoux C, Rivière D, Mangin JF, Operto G, Régis J, Coulon O (2010a) Model-driven parameterization of the cortical surface for localization and inter-subject matching. Neuroimage 50(2):552–566PubMedCrossRef
go back to reference Clouchoux C, Coupé P, Manjon J, Guizard N, Bouyssi-Kobar M, Lefebvre M, Du Plessis AJ, Evans AC, Limperopoulos C (2010b) A novel approach for high-resolution image reconstruction for in vivo fetal brain MRI. In: Proceedings of the Sixteenth Annual Meeting of the Organization for Human Brain Mapping Clouchoux C, Coupé P, Manjon J, Guizard N, Bouyssi-Kobar M, Lefebvre M, Du Plessis AJ, Evans AC, Limperopoulos C (2010b) A novel approach for high-resolution image reconstruction for in vivo fetal brain MRI. In: Proceedings of the Sixteenth Annual Meeting of the Organization for Human Brain Mapping
go back to reference Clouchoux C, Kudelski D, Bouyssi-Kobar M, Viseur S, du Plessis A, Evans AC, Mari J-L, Limperopoulos C (2010c) Cortical pattern detection for the developing brain: a 3D vertex labeling and skeletonization approach. J Med Inform Technol 16:161–166 Clouchoux C, Kudelski D, Bouyssi-Kobar M, Viseur S, du Plessis A, Evans AC, Mari J-L, Limperopoulos C (2010c) Cortical pattern detection for the developing brain: a 3D vertex labeling and skeletonization approach. J Med Inform Technol 16:161–166
go back to reference Cohen J (1960) A coefficient for agreement for nominal scales. Educ Psychol Measur 20(1):37–46CrossRef Cohen J (1960) A coefficient for agreement for nominal scales. Educ Psychol Measur 20(1):37–46CrossRef
go back to reference Corbett-Detig JM, Habas PA, Scott JA, Kim K, Rajagopalan V, McQuillen PS, Barkovich AJ, Glenn OA, Studholme C (2011) 3D global and regional patterns of human fetal subplate growth determined in utero. Brain Struct Funct 215(3-4):255–263PubMedCrossRef Corbett-Detig JM, Habas PA, Scott JA, Kim K, Rajagopalan V, McQuillen PS, Barkovich AJ, Glenn OA, Studholme C (2011) 3D global and regional patterns of human fetal subplate growth determined in utero. Brain Struct Funct 215(3-4):255–263PubMedCrossRef
go back to reference Dice LR (1945) Measures of the amount of ecologic association between species. Ecology 26(3):297–302CrossRef Dice LR (1945) Measures of the amount of ecologic association between species. Ecology 26(3):297–302CrossRef
go back to reference Dubois J, Benders M, Cachia A, Lazeiras F, Ha-Vinh Leutcher R, Sizonenko SV, Borradori-Tolsa C, Mangin J-F, Hüppi PS (2008a) Mapping the early cortical folding process in the preterm new born brain. Cereb Cortex 18:1444–1454PubMedCrossRef Dubois J, Benders M, Cachia A, Lazeiras F, Ha-Vinh Leutcher R, Sizonenko SV, Borradori-Tolsa C, Mangin J-F, Hüppi PS (2008a) Mapping the early cortical folding process in the preterm new born brain. Cereb Cortex 18:1444–1454PubMedCrossRef
go back to reference Dubois J, Benders M, Borradori-Tolsa C, Cachia A, Lazeyras F, Ha-Vinh Leuchter R, Sizonenko SV, Warfield SK, Mangin JF, Hüppi PS (2008b) Primary cortical folding in the human newborn: an early marker of later functional development. Brain. 131(Pt 8):2028–2041PubMedCrossRef Dubois J, Benders M, Borradori-Tolsa C, Cachia A, Lazeyras F, Ha-Vinh Leuchter R, Sizonenko SV, Warfield SK, Mangin JF, Hüppi PS (2008b) Primary cortical folding in the human newborn: an early marker of later functional development. Brain. 131(Pt 8):2028–2041PubMedCrossRef
go back to reference Dubois J, Benders M, Lazeyras F, Borradori-Tolsa C, Leuchter RH, Mangin JF, Hüppi PS (2010) Structural asymmetries of perisylvian regions in the preterm newborn. Neuroimage 52(1):32–42PubMedCrossRef Dubois J, Benders M, Lazeyras F, Borradori-Tolsa C, Leuchter RH, Mangin JF, Hüppi PS (2010) Structural asymmetries of perisylvian regions in the preterm newborn. Neuroimage 52(1):32–42PubMedCrossRef
go back to reference Evans AC, the Brain Development Cooperative Group et al (2006) The NIH MRI study of normal brain development. NeuroImage 30(1):184–202PubMedCrossRef Evans AC, the Brain Development Cooperative Group et al (2006) The NIH MRI study of normal brain development. NeuroImage 30(1):184–202PubMedCrossRef
go back to reference Fischl B, Sereno MI, Tootell R, Dale AM (1999) Cortical surface-based analysis, ii: Inflation, flattening and a surface-based coordinate system. Neuroimage 9:195–207PubMedCrossRef Fischl B, Sereno MI, Tootell R, Dale AM (1999) Cortical surface-based analysis, ii: Inflation, flattening and a surface-based coordinate system. Neuroimage 9:195–207PubMedCrossRef
go back to reference Garel C, Chantrel E, Brisse H, Elmaleh M, Luton D, Oury J-F, Sebag G, Hassan M (2001) Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. AJRN Am J Neuradiol 22(1):184–189 Garel C, Chantrel E, Brisse H, Elmaleh M, Luton D, Oury J-F, Sebag G, Hassan M (2001) Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. AJRN Am J Neuradiol 22(1):184–189
go back to reference Gatzke T, Grimm CM (2006) Estimating curvature on triangular meshes. Int J Shape Model 12(1):1–28CrossRef Gatzke T, Grimm CM (2006) Estimating curvature on triangular meshes. Int J Shape Model 12(1):1–28CrossRef
go back to reference Gholipour A, Estroff JA, Warfield SK (2010a) Robust super-resolution volume reconstruction from slice acquisitions: application to fetal brain MRI. IEEE Trans Med Imaging 29(10):1739–1758PubMedCrossRef Gholipour A, Estroff JA, Warfield SK (2010a) Robust super-resolution volume reconstruction from slice acquisitions: application to fetal brain MRI. IEEE Trans Med Imaging 29(10):1739–1758PubMedCrossRef
go back to reference Gholipour A, Estroff JA, Barnewolt CE, Connolly SA, Warfield SK (2010b) Fetal brain volumetry through MRI volumetric reconstruction and segmentation. Int J Comput Assist Radiol Surg 6(3):329–339 Gholipour A, Estroff JA, Barnewolt CE, Connolly SA, Warfield SK (2010b) Fetal brain volumetry through MRI volumetric reconstruction and segmentation. Int J Comput Assist Radiol Surg 6(3):329–339
go back to reference Goldfeather J, Interrante V (2004) A novel cubic-order algorithm for approximating principal direction vectors. ACM Trans Graph 23(1):45–63CrossRef Goldfeather J, Interrante V (2004) A novel cubic-order algorithm for approximating principal direction vectors. ACM Trans Graph 23(1):45–63CrossRef
go back to reference Grossman R, Hoffman C, Mardor Y, Biegon A (2006) Quantitative MRI measurements of human fetal brain development in utero. Neuroimage 33(2):463–470PubMedCrossRef Grossman R, Hoffman C, Mardor Y, Biegon A (2006) Quantitative MRI measurements of human fetal brain development in utero. Neuroimage 33(2):463–470PubMedCrossRef
go back to reference Guihard-Costa AM, Larroche JC (1990) Differential growth between the fetal brain and its infratentorial part. Early Hum Dev 23:27–40PubMedCrossRef Guihard-Costa AM, Larroche JC (1990) Differential growth between the fetal brain and its infratentorial part. Early Hum Dev 23:27–40PubMedCrossRef
go back to reference 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 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
go back to reference Habas PA, Kim K, Corbett-Detig JM, Rousseau F, Glenn OA, Barkovich AJ, Studholme C (2010) A spatiotemporal atlas of MR intensity, tissue probability and shape of the fetal brain with application to segmentation. Neuroimage (in press) Habas PA, Kim K, Corbett-Detig JM, Rousseau F, Glenn OA, Barkovich AJ, Studholme C (2010) A spatiotemporal atlas of MR intensity, tissue probability and shape of the fetal brain with application to segmentation. Neuroimage (in press)
go back to reference Hill J, Dierker D, Neil J, Inder T, Knutsen A, Harwell J, Coalson T, Van Essen D (2010) A surface-based analysis of hemispheric asymmetries and folding of cerebral cortex in term-born human. J Neurosci 30(6):2268–2276PubMedCrossRef Hill J, Dierker D, Neil J, Inder T, Knutsen A, Harwell J, Coalson T, Van Essen D (2010) A surface-based analysis of hemispheric asymmetries and folding of cerebral cortex in term-born human. J Neurosci 30(6):2268–2276PubMedCrossRef
go back to reference Hu H-H, Guo W-Y, Chen H-Y, Wang P-S, Hung C-I, Hsieh J-C, Wu Y-T (2009) Morphological regionalization using fetal magnetic resonance images of normal developing brains. Eur J Neurosci 29:1560–1567PubMedCrossRef Hu H-H, Guo W-Y, Chen H-Y, Wang P-S, Hung C-I, Hsieh J-C, Wu Y-T (2009) Morphological regionalization using fetal magnetic resonance images of normal developing brains. Eur J Neurosci 29:1560–1567PubMedCrossRef
go back to reference Jain AK (1989) Fundamentals of digital image processing. Prentice-Hall, Inc, Upper Saddle River Jain AK (1989) Fundamentals of digital image processing. Prentice-Hall, Inc, Upper Saddle River
go back to reference Jiang H, Xue H, Counsell SJ, Anjari M, Allsop J, Rutherford MA, Rueckert D, Hajnal JV (2007) In utero three dimension high resolution fetal brain diffusion tensor imaging. Med Image Comput Comput Assist Interv 10(Pt 1):18–26PubMed Jiang H, Xue H, Counsell SJ, Anjari M, Allsop J, Rutherford MA, Rueckert D, Hajnal JV (2007) In utero three dimension high resolution fetal brain diffusion tensor imaging. Med Image Comput Comput Assist Interv 10(Pt 1):18–26PubMed
go back to reference Kasprian G, Langs G, Brugger PC, Bittner M, Weber M, Arantes M, Prayer D (2011) The prenatal origin of hemispheric asymmetry: an in utero neuroimaging study. Cereb Cortex 21(5):1076–1083PubMedCrossRef Kasprian G, Langs G, Brugger PC, Bittner M, Weber M, Arantes M, Prayer D (2011) The prenatal origin of hemispheric asymmetry: an in utero neuroimaging study. Cereb Cortex 21(5):1076–1083PubMedCrossRef
go back to reference Kazan-Tannus JF, Dialani V, Kataoka ML, Chiang G, Feldman HA, Brown JS, Levine D (2007) MR volumetry of brain and CSF in fetuses referred for ventriculomegaly. Am J Roentgenol 189(1):145–151CrossRef Kazan-Tannus JF, Dialani V, Kataoka ML, Chiang G, Feldman HA, Brown JS, Levine D (2007) MR volumetry of brain and CSF in fetuses referred for ventriculomegaly. Am J Roentgenol 189(1):145–151CrossRef
go back to reference Kostović I, Judas M (2002) Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anat Rec 267(1):1–6PubMedCrossRef Kostović I, Judas M (2002) Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anat Rec 267(1):1–6PubMedCrossRef
go back to reference Kudelski D, Mari J.-L, Viseur S (2010) 3D Feature Line Detection based on Vertex Labeling and 2D Skeletonization. In: Proceedings of the 2010 Shape Modeling International Conference (SMI ‘10), vol 1. IEEE Computer Society, Washington, pp 246–250 Kudelski D, Mari J.-L, Viseur S (2010) 3D Feature Line Detection based on Vertex Labeling and 2D Skeletonization. In: Proceedings of the 2010 Shape Modeling International Conference (SMI ‘10), vol 1. IEEE Computer Society, Washington, pp 246–250
go back to reference Lee JK, Lee J-M, Kim JS, Kim IY, Evans AC, Kim SI (2006) A novel quantitative cross-validation of different cortical surface reconstruction algorithms using MRI phantom. Neuroimage 31(2):572–584PubMedCrossRef Lee JK, Lee J-M, Kim JS, Kim IY, Evans AC, Kim SI (2006) A novel quantitative cross-validation of different cortical surface reconstruction algorithms using MRI phantom. Neuroimage 31(2):572–584PubMedCrossRef
go back to reference Lefebvre J, Leroy F, Khan S, Dubois J, Hüppi P, Baillet S, Mangin JF (2009) Identification of growth seeds in the neonate brain through surfacic Helmholtz decomposition. Inf Process Med Imaging 21:252–256CrossRef Lefebvre J, Leroy F, Khan S, Dubois J, Hüppi P, Baillet S, Mangin JF (2009) Identification of growth seeds in the neonate brain through surfacic Helmholtz decomposition. Inf Process Med Imaging 21:252–256CrossRef
go back to reference Limperopoulos C, Clouchoux C (2009) Advancing fetal MRI: target for the future. Semin Perinatol 34(4):289–298CrossRef Limperopoulos C, Clouchoux C (2009) Advancing fetal MRI: target for the future. Semin Perinatol 34(4):289–298CrossRef
go back to reference Limperopoulos C, Tworetzky W, McElhinney DB, Newburger JW, Brown DW, Robertson RL Jr, Guizard N, McGrath E, Geva J, Annese D, Dunbar-Masterson C, Trainor B, Laussen PC, du Plessis AJ (2010) Brain volume and metabolism in fetuses with congenital heart disease: evaluation with quantitative magnetic resonance imaging and spectroscopy. Circulation. 121(1):26–33PubMedCrossRef Limperopoulos C, Tworetzky W, McElhinney DB, Newburger JW, Brown DW, Robertson RL Jr, Guizard N, McGrath E, Geva J, Annese D, Dunbar-Masterson C, Trainor B, Laussen PC, du Plessis AJ (2010) Brain volume and metabolism in fetuses with congenital heart disease: evaluation with quantitative magnetic resonance imaging and spectroscopy. Circulation. 121(1):26–33PubMedCrossRef
go back to reference Lohmann G, Von Cramon Y, Colchester A (2007) Deep sulcal landmark provide an organizing framework for human cortical folding. Cereb Cortex 18(6):1415–1420PubMedCrossRef Lohmann G, Von Cramon Y, Colchester A (2007) Deep sulcal landmark provide an organizing framework for human cortical folding. Cereb Cortex 18(6):1415–1420PubMedCrossRef
go back to reference Luders E, Thompson PM, Narr KL, Toga AW, Jancke L, Gaser C (2006) A curvature-based approach to estimate local gyrification on the cortical surface. Neuroimage 29(4):1224–1230PubMedCrossRef Luders E, Thompson PM, Narr KL, Toga AW, Jancke L, Gaser C (2006) A curvature-based approach to estimate local gyrification on the cortical surface. Neuroimage 29(4):1224–1230PubMedCrossRef
go back to reference Lyttelton O, Boucher M, Robbins S, Evans A (2007) An unbiased iterative group registration template for cortical surface analysis. Neuroimage 34(4):1535–1544PubMedCrossRef Lyttelton O, Boucher M, Robbins S, Evans A (2007) An unbiased iterative group registration template for cortical surface analysis. Neuroimage 34(4):1535–1544PubMedCrossRef
go back to reference McDonald D, Kabani N, Avis D, Evans AC et al (2000) Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. Neuroimage 12(3):340–356CrossRef McDonald D, Kabani N, Avis D, Evans AC et al (2000) Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. Neuroimage 12(3):340–356CrossRef
go back to reference O’Rahilly R, Muller F (1999) The embryonic human brain: an atlas of developmental stages. John Wiley & Sons Ltd, Chichester O’Rahilly R, Muller F (1999) The embryonic human brain: an atlas of developmental stages. John Wiley & Sons Ltd, Chichester
go back to reference Prayer D (2006) Investigation of normal organ development with fetal MRI. Eur Radiol 17(10):2458–2471CrossRef Prayer D (2006) Investigation of normal organ development with fetal MRI. Eur Radiol 17(10):2458–2471CrossRef
go back to reference Rajagopalan V, Scott J, Habas PA, Kim K, Corbett-Detig J, Rousseau F, Barkovich AJ, Glenn OA, Studholme C (2011) Local tissue growth patterns underlying normal fetal human brain gyrification quantified in utero. J Neurosci 31(8):2878–2887PubMedCrossRef Rajagopalan V, Scott J, Habas PA, Kim K, Corbett-Detig J, Rousseau F, Barkovich AJ, Glenn OA, Studholme C (2011) Local tissue growth patterns underlying normal fetal human brain gyrification quantified in utero. J Neurosci 31(8):2878–2887PubMedCrossRef
go back to reference Regis J, Mangin J, Ochiai T, Frouin V, Rivière D, Cachia A, Tamura M, Samson Y (2005) Sulcal roots generic model: a hypothesis to overcome the variability of the human cortex folding patterns. Neurol Med Chir 45:1–17CrossRef Regis J, Mangin J, Ochiai T, Frouin V, Rivière D, Cachia A, Tamura M, Samson Y (2005) Sulcal roots generic model: a hypothesis to overcome the variability of the human cortex folding patterns. Neurol Med Chir 45:1–17CrossRef
go back to reference Richman DP, Stewart RM, Hutchinson JW, Caviness VS (1975) Mechanical model of brain convolutional development. Science. 189:18–21CrossRef Richman DP, Stewart RM, Hutchinson JW, Caviness VS (1975) Mechanical model of brain convolutional development. Science. 189:18–21CrossRef
go back to reference Rivière D, Mangin J-F, Papadopoulos-Orfanos D, Martinez J-M, Frouin V, Regis J (2002) Automatic recognition of cortical sulci of the human brain using a congregation of neural network. Med Image Anal 6(2):77–92PubMedCrossRef Rivière D, Mangin J-F, Papadopoulos-Orfanos D, Martinez J-M, Frouin V, Regis J (2002) Automatic recognition of cortical sulci of the human brain using a congregation of neural network. Med Image Anal 6(2):77–92PubMedCrossRef
go back to reference Rössl C, Kobbelt L, Seidel HP (2000) Extraction of feature lines on triangulated surfaces using morphological operators. In: Proceedings of the AAAI Symposium on Smart Graphics, vol 4, pp 71–75 Rössl C, Kobbelt L, Seidel HP (2000) Extraction of feature lines on triangulated surfaces using morphological operators. In: Proceedings of the AAAI Symposium on Smart Graphics, vol 4, pp 71–75
go back to reference Rousseau O, Glenn B, Iordanova et al (2006) Registration-based approach for reconstruction of high-resolution in utero fetal mr brain images. Acad Radiol 13(9):1072–1081PubMedCrossRef Rousseau O, Glenn B, Iordanova et al (2006) Registration-based approach for reconstruction of high-resolution in utero fetal mr brain images. Acad Radiol 13(9):1072–1081PubMedCrossRef
go back to reference Shankle WR, Landing BH, Rafii MS, Schiano A, Chen JM, Hara J (1998) Evidence for a postnatal doubling of neuron number in the developing human cerebral cortex between 15 months and 6 years. J Theor Biol 191(2):115–140PubMedCrossRef Shankle WR, Landing BH, Rafii MS, Schiano A, Chen JM, Hara J (1998) Evidence for a postnatal doubling of neuron number in the developing human cerebral cortex between 15 months and 6 years. J Theor Biol 191(2):115–140PubMedCrossRef
go back to reference Sled JG, Zijdenbos AP, Evans AC (1998) A non-parametric method for automatic correction of intensity non-uniformity in MRI data. IEEE Trans Med Imaging 17(1):87–97PubMedCrossRef Sled JG, Zijdenbos AP, Evans AC (1998) A non-parametric method for automatic correction of intensity non-uniformity in MRI data. IEEE Trans Med Imaging 17(1):87–97PubMedCrossRef
go back to reference Thompson PM, Schwartz C, Lin RT, Khan AA, Toga AW (1996) Three-dimensional statistical analysis of sulcal variability in the human brain. J Neurosci 16(13):4261–4274PubMed Thompson PM, Schwartz C, Lin RT, Khan AA, Toga AW (1996) Three-dimensional statistical analysis of sulcal variability in the human brain. J Neurosci 16(13):4261–4274PubMed
go back to reference Toro R, Burnod Y (2003) Geometric atlas: modeling the cortex as an organized surface. Neuroimage 20(3):1468–1484PubMedCrossRef Toro R, Burnod Y (2003) Geometric atlas: modeling the cortex as an organized surface. Neuroimage 20(3):1468–1484PubMedCrossRef
go back to reference Van Essen D (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature. 385(23):313–318PubMedCrossRef Van Essen D (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature. 385(23):313–318PubMedCrossRef
go back to reference Xu G, Knutsen AK, Dikranian K, Kroenke CD, Bayly PV, Taber LA (2010) Axon pull on the brain, but tension does not drive cortical folding. J Biomech Eng 132(7):071013 Xu G, Knutsen AK, Dikranian K, Kroenke CD, Bayly PV, Taber LA (2010) Axon pull on the brain, but tension does not drive cortical folding. J Biomech Eng 132(7):071013
go back to reference Yoshizawa S, Belyaev A, Seidel H (2005) Fast and robust detection of crest lines on meshes. In: Proceedings of the 2005 ACM symposium on Solid and physical modeling, pp 227–232 Yoshizawa S, Belyaev A, Seidel H (2005) Fast and robust detection of crest lines on meshes. In: Proceedings of the 2005 ACM symposium on Solid and physical modeling, pp 227–232
go back to reference Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation maximization algorithm. IEEE Trans Med Imaging 20(1):45–57PubMedCrossRef Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation maximization algorithm. IEEE Trans Med Imaging 20(1):45–57PubMedCrossRef
go back to reference Zhang Z, Liu S, Lin X, Sun B, Yu T, Geng H (2010) Development of fetal cerebral cortex: assessment of the folding conditions with post-mortem Magnetic Resonance Imaging. Int J Dev Neurosci 28(6):537–543PubMedCrossRef Zhang Z, Liu S, Lin X, Sun B, Yu T, Geng H (2010) Development of fetal cerebral cortex: assessment of the folding conditions with post-mortem Magnetic Resonance Imaging. Int J Dev Neurosci 28(6):537–543PubMedCrossRef
go back to reference Zilles K, Amstrong E, Schleicher A, Kretschmann H (1988) The human pattern of gyrification in the human brain. Anat Embryol 179(2):173–179PubMedCrossRef Zilles K, Amstrong E, Schleicher A, Kretschmann H (1988) The human pattern of gyrification in the human brain. Anat Embryol 179(2):173–179PubMedCrossRef
Metadata
Title
Quantitative in vivo MRI measurement of cortical development in the fetus
Authors
Cédric Clouchoux
Dimitri Kudelski
Ali Gholipour
Simon K. Warfield
Sophie Viseur
Marine Bouyssi-Kobar
Jean-Luc Mari
Alan C. Evans
Adre J. du Plessis
Catherine Limperopoulos
Publication date
01-01-2012
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 1/2012
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-011-0325-x

Other articles of this Issue 1/2012

Brain Structure and Function 1/2012 Go to the issue