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Quantitative in vivo MRI measurement of cortical development in the fetus

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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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References

  • Armstrong E, Schleicher A, Omran H, Curtis M, Zilles K (1995) The ontogeny of human gyrification. Cereb Cortex 5:56–63

    Article  PubMed  CAS  Google Scholar 

  • 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 21:552–563

    Article  PubMed  Google Scholar 

  • Barron DH (1950) An experimental analysis of some factors involved in the development of the fissure pattern of the cerebral cortex. J Exp Zool 113:553–581

    Article  Google Scholar 

  • Bartley AJ, Jones DW, Weinberger DR (1997) Genetic variability of human brain size and cortical gyral patterns. Brain 120:257–269

    Article  PubMed  Google Scholar 

  • 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):953–965

    Article  PubMed  Google Scholar 

  • Boucher M, Whiteside S, Evans AC (2009) Depth potential function for folding pattern representation, registration and analysis. Med Image Anal 13(2):203–214

    Article  PubMed  Google Scholar 

  • Chi JG, Dooling EC, Gilles FH (1977) Gyral development of the human brain. Ann Neurol 1:86–93

    Article  PubMed  CAS  Google Scholar 

  • 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):552–566

    Article  PubMed  CAS  Google Scholar 

  • 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, 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

    Google Scholar 

  • Cohen J (1960) A coefficient for agreement for nominal scales. Educ Psychol Measur 20(1):37–46

    Article  Google Scholar 

  • 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):255–263

    Article  PubMed  CAS  Google Scholar 

  • Dice LR (1945) Measures of the amount of ecologic association between species. Ecology 26(3):297–302

    Article  Google Scholar 

  • 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 18:1444–1454

    Article  PubMed  CAS  Google Scholar 

  • 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):2028–2041

    Article  PubMed  CAS  Google Scholar 

  • 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):32–42

    Article  PubMed  CAS  Google Scholar 

  • Evans AC, the Brain Development Cooperative Group et al (2006) The NIH MRI study of normal brain development. NeuroImage 30(1):184–202

    Article  PubMed  Google Scholar 

  • Fischl B, Sereno MI, Tootell R, Dale AM (1999) Cortical surface-based analysis, ii: Inflation, flattening and a surface-based coordinate system. Neuroimage 9:195–207

    Article  PubMed  CAS  Google Scholar 

  • Garel C (2008) Fetal MRI: what is the future? Ultrasound Obstet Gynecol 31:123–128

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Gatzke T, Grimm CM (2006) Estimating curvature on triangular meshes. Int J Shape Model 12(1):1–28

    Article  Google Scholar 

  • 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):1739–1758

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Goldfeather J, Interrante V (2004) A novel cubic-order algorithm for approximating principal direction vectors. ACM Trans Graph 23(1):45–63

    Article  Google Scholar 

  • Grossman R, Hoffman C, Mardor Y, Biegon A (2006) Quantitative MRI measurements of human fetal brain development in utero. Neuroimage 33(2):463–470

    Article  PubMed  Google Scholar 

  • Guihard-Costa AM, Larroche JC (1990) Differential growth between the fetal brain and its infratentorial part. Early Hum Dev 23:27–40

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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)

  • 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):2268–2276

    Article  PubMed  CAS  Google Scholar 

  • 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 29:1560–1567

    Article  PubMed  Google Scholar 

  • Jain AK (1989) Fundamentals of digital image processing. Prentice-Hall, Inc, Upper Saddle River

  • 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):18–26

    PubMed  Google Scholar 

  • 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):1076–1083

    Article  PubMed  Google Scholar 

  • 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):145–151

    Article  Google Scholar 

  • 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):1–6

    Article  PubMed  Google Scholar 

  • 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

  • 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):572–584

    Article  PubMed  CAS  Google Scholar 

  • 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 21:252–256

    Article  Google Scholar 

  • Limperopoulos C, Clouchoux C (2009) Advancing fetal MRI: target for the future. Semin Perinatol 34(4):289–298

    Article  Google Scholar 

  • 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):26–33

    Article  PubMed  CAS  Google Scholar 

  • Lohmann G, Von Cramon Y, Colchester A (2007) Deep sulcal landmark provide an organizing framework for human cortical folding. Cereb Cortex 18(6):1415–1420

    Article  PubMed  Google Scholar 

  • 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):1224–1230

    Article  PubMed  CAS  Google Scholar 

  • Lyttelton O, Boucher M, Robbins S, Evans A (2007) An unbiased iterative group registration template for cortical surface analysis. Neuroimage 34(4):1535–1544

    Article  PubMed  Google Scholar 

  • 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):340–356

    Article  Google Scholar 

  • O’Rahilly R, Muller F (1999) The embryonic human brain: an atlas of developmental stages. John Wiley & Sons Ltd, Chichester

  • Prayer D (2006) Investigation of normal organ development with fetal MRI. Eur Radiol 17(10):2458–2471

    Article  Google Scholar 

  • 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):2878–2887

    Article  PubMed  CAS  Google Scholar 

  • Rakic P (1988) Specification of cerebral cortical areas. Science 241:170–176

    Article  PubMed  CAS  Google Scholar 

  • 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 45:1–17

    Article  Google Scholar 

  • Richman DP, Stewart RM, Hutchinson JW, Caviness VS (1975) Mechanical model of brain convolutional development. Science. 189:18–21

    Article  Google Scholar 

  • 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):77–92

    Article  PubMed  Google Scholar 

  • 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

  • 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):1072–1081

    Article  PubMed  Google Scholar 

  • 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):115–140

    Article  PubMed  CAS  Google Scholar 

  • 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):87–97

    Article  PubMed  CAS  Google Scholar 

  • 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):4261–4274

    PubMed  CAS  Google Scholar 

  • Toro R, Burnod Y (2003) Geometric atlas: modeling the cortex as an organized surface. Neuroimage 20(3):1468–1484

    Article  PubMed  Google Scholar 

  • Van Essen D (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature. 385(23):313–318

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

  • 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):45–57

    Article  PubMed  CAS  Google Scholar 

  • 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):537–543

    Article  PubMed  Google Scholar 

  • Zilles K, Amstrong E, Schleicher A, Kretschmann H (1988) The human pattern of gyrification in the human brain. Anat Embryol 179(2):173–179

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Yansong Zhao and David Annese for their help with MRI applications. We are indebted to the families for participating in this study. This work was supported by the Canadian Institutes of Health Research (MOP-81116), Sickkids Foundation (XG 06-069), and Canada Research Chairs Program (Dr Limperopoulos).

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Authors and Affiliations

  1. Division of Diagnostic Imaging and Radiology, Children’s National Medical Center, Washington, DC, USA

    Cédric Clouchoux, Marine Bouyssi-Kobar & Catherine Limperopoulos

  2. McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC, Canada

    Cédric Clouchoux, Alan C. Evans & Catherine Limperopoulos

  3. LSIS, UMC CNRS 6168, Université de la Méditerranée, Marseilles, France

    Dimitri Kudelski & Jean-Luc Mari

  4. GSRC, EA 4234, Université de Provence, Marseilles, France

    Dimitri Kudelski & Sophie Viseur

  5. Department of Radiology, Harvard Medical School, Children’s Hospital Boston, Boston, MA, USA

    Ali Gholipour & Simon K. Warfield

  6. Division of Fetal and Transitional Medicine, Children’s National Medical Center, Washington, DC, USA

    Adre J. du Plessis & Catherine Limperopoulos

  7. Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada

    Catherine Limperopoulos

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  1. Cédric Clouchoux
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  2. Dimitri Kudelski
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  8. Alan C. Evans
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  9. Adre J. du Plessis
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  10. Catherine Limperopoulos
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Correspondence to Catherine Limperopoulos.

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

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  • DOI: https://doi.org/10.1007/s00429-011-0325-x

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