Structural Development of Human Fetal and Preterm Brain Cortical Plate Based on Population-Averaged Templates.

We hypothesized that the distinct maturational processes take place across different cortical areas from middle fetal stage to normal time of birth and these maturational processes are altered in late third trimester. Fractional anisotropies (FA) from diffusion tensor imaging (DTI) infer the microstructures of the early developing cortical plate. High-resolution DTI of 11 fetal brain specimens at postmenstrual age of 20 weeks (or simplified as 20 weeks), 19 in vivo brains at 35 weeks, and 17 in vivo brains at normal time of birth at term (40 weeks) were acquired. Population-averaged age-specific DTI templates were established with large deformation diffeomorphic metric mapping for subject groups at 20, 35, and 40 weeks. To alleviate partial volume effects, skeletonized FA values were used for mapping averaged cortical FA to the cortical surface and measuring FA at 12 functionally distinctive cortical regions. Significant and heterogeneous FA decreases take place in distinct cortical areas from 20 to 35 weeks and from 35 to 40 weeks, suggesting differentiated cortical development patterns. Temporally nonuniform FA decrease patterns during 35-40 weeks compared with those during 20-35 weeks were observed in higher-order association cortex. Measured skeletonized FA suggested dissociated changes between cerebral cortex and white matter during 35-40 weeks.

[1]  J. Dobbing,et al.  Vulnerability of developing brain and behaviour. , 1974, British medical bulletin.

[2]  Hsiao-Fang Liang,et al.  Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infarcted brain , 2005, Magnetic resonance in medicine.

[3]  T. Paus,et al.  Why do many psychiatric disorders emerge during adolescence? , 2008, Nature Reviews Neuroscience.

[4]  Susumu Mori,et al.  Coupling diffusion imaging with histological and gene expression analysis to examine the dynamics of cortical areas across the fetal period of human brain development. , 2013, Cerebral cortex.

[5]  F. Turkheimer,et al.  Emergence of resting state networks in the preterm human brain , 2010, Proceedings of the National Academy of Sciences.

[6]  Hao Huang,et al.  White and gray matter development in human fetal, newborn and pediatric brains , 2006, NeuroImage.

[7]  J. Mazziotta,et al.  Positron emission tomography study of human brain functional development , 1987, Annals of neurology.

[8]  P. Rakić,et al.  Neuronal migration, with special reference to developing human brain: a review. , 1973, Brain research.

[9]  Scott T. Grafton,et al.  Automated image registration: I. General methods and intrasubject, intramodality validation. , 1998, Journal of computer assisted tomography.

[10]  J. Volpe Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances , 2009, The Lancet Neurology.

[11]  Susumu Mori,et al.  Quantitative Cortical Mapping of Fractional Anisotropy in Developing Rat Brains , 2008, The Journal of Neuroscience.

[12]  Roland G. Henry,et al.  Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants , 2004, NeuroImage.

[13]  I. Hertz-Picciotto,et al.  Trophoblast Inclusions Are Significantly Increased in the Placentas of Children in Families at Risk for Autism , 2013, Biological Psychiatry.

[14]  Sheng-Kwei Song,et al.  Relative indices of water diffusion anisotropy are equivalent in live and formalin‐fixed mouse brains , 2003, Magnetic resonance in medicine.

[15]  D. Geschwind,et al.  Functional and Evolutionary Insights into Human Brain Development through Global Transcriptome Analysis , 2009, Neuron.

[16]  P. Rakić Mode of cell migration to the superficial layers of fetal monkey neocortex , 1972, The Journal of comparative neurology.

[17]  M. Miller,et al.  Anatomical Characterization of Human Fetal Brain Development with Diffusion Tensor Magnetic Resonance Imaging , 2009, The Journal of Neuroscience.

[18]  J. Dobbing The later growth of the brain and its vulnerability. , 1974, Pediatrics.

[19]  D. V. van Essen,et al.  Microstructural Changes of the Baboon Cerebral Cortex during Gestational Development Reflected in Magnetic Resonance Imaging Diffusion Anisotropy , 2007, The Journal of Neuroscience.

[20]  P. Rakic A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution , 1995, Trends in Neurosciences.

[21]  Hao Huang,et al.  Regional changes of cortical mean diffusivities with aging after correction of partial volume effects , 2012, NeuroImage.

[22]  Kenichi Ohki,et al.  Developing neocortex organization and connectivity in cats revealed by direct correlation of diffusion tractography and histology. , 2011, Cerebral cortex.

[23]  A. Snyder,et al.  Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. , 2002, Cerebral cortex.

[24]  Milos Judas,et al.  Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. , 2002, Cerebral cortex.

[25]  J S Thornton,et al.  Anisotropic water diffusion in white and gray matter of the neonatal piglet brain before and after transient hypoxia-ischaemia. , 1997, Magnetic resonance imaging.

[26]  M. Horsfield,et al.  Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging , 1999, Magnetic resonance in medicine.

[27]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[28]  Joseph V. Hajnal,et al.  Development of cortical microstructure in the preterm human brain , 2013, Proceedings of the National Academy of Sciences.

[29]  L. Younes,et al.  On the metrics and euler-lagrange equations of computational anatomy. , 2002, Annual review of biomedical engineering.

[30]  W. Engle Age Terminology During the Perinatal Period , 2004, Pediatrics.

[31]  D. Shen,et al.  Spatial normalization of diffusion tensor fields , 2003, Magnetic resonance in medicine.

[32]  A. Snyder,et al.  Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. , 2002, AJNR. American journal of neuroradiology.

[33]  J. Dobbing,et al.  Vulnerability of developing brain. I. Some lasting effects of x-irradiation. , 1970, Experimental neurology.

[34]  Colin Blakemore,et al.  Development of the human cerebral cortex: Boulder Committee revisited , 2008, Nature Reviews Neuroscience.

[35]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[36]  T. Kemper,et al.  NEUROANATOMICAL OBSERVATIONS OF THE BRAIN IN AUTISM , 2003 .

[37]  Stephan E Maier,et al.  Developmental changes and injury induced disruption of the radial organization of the cortex in the immature rat brain revealed by in vivo diffusion tensor MRI. , 2007, Cerebral cortex.

[38]  J. Mazziotta,et al.  Automated image registration , 1993 .

[39]  Andrew K Knutsen,et al.  Regional patterns of cerebral cortical differentiation determined by diffusion tensor MRI. , 2009, Cerebral cortex.

[40]  H. Wiśniewski,et al.  Peripheral nerve ischemia: Part 2. Accumulation of organelles , 1978, Annals of neurology.

[41]  Georg Langs,et al.  Fetal functional imaging portrays heterogeneous development of emerging human brain networks , 2014, Front. Hum. Neurosci..

[42]  Hua Jin,et al.  Comparing microstructural and macrostructural development of the cerebral cortex in premature newborns: Diffusion tensor imaging versus cortical gyration , 2005, NeuroImage.

[43]  N. Jovanov-Milošević,et al.  The development of cerebral connections during the first 20-45 weeks' gestation. , 2006, Seminars in fetal & neonatal medicine.

[44]  M. Solaiyappan,et al.  Diffusion tensor imaging of the developing mouse brain , 2001, Magnetic resonance in medicine.

[45]  T. Kemper,et al.  Neuroanatomic observations of the brain in autism: a review and future directions , 2005, International Journal of Developmental Neuroscience.

[46]  Emi Takahashi,et al.  Emerging cerebral connectivity in the human fetal brain: an MR tractography study. , 2012, Cerebral cortex.

[47]  Michael I. Miller,et al.  Multi-contrast human neonatal brain atlas: Application to normal neonate development analysis , 2011, NeuroImage.

[48]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[49]  J. Kleinman,et al.  Spatiotemporal transcriptome of the human brain , 2011, Nature.

[50]  Moriah E. Thomason,et al.  Intrinsic Functional Brain Architecture Derived from Graph Theoretical Analysis in the Human Fetus , 2014, PloS one.

[51]  P. Rakic Specification of cerebral cortical areas. , 1988, Science.

[52]  G. Smith,et al.  Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. , 1927 .

[53]  P. Hüppi,et al.  Diffusion tensor imaging of normal and injured developing human brain ‐ a technical review , 2002, NMR in biomedicine.

[54]  Hangyi Jiang,et al.  DtiStudio: Resource program for diffusion tensor computation and fiber bundle tracking , 2006, Comput. Methods Programs Biomed..

[55]  F Barkhof,et al.  Normal gyration and sulcation in preterm and term neonates: appearance on MR images. , 1996, Radiology.