Assessment of cortical maturation with prenatal MRI:Part I. Normal cortical maturation

Cortical maturation, especially gyral formation, follows a temporospatial schedule and is a good marker of fetal maturation. Although ultrasonography is still the imaging method of choice to evaluate fetal anatomy, MRI has an increasingly important role in the detection of brain abnormalities, especially of cortical development. Knowledge of MRI techniques in utero with the advantages and disadvantages of some sequences is necessary, in order to try to optimize the different magnetic resonance sequences to be able to make an early diagnosis. The different steps of cortical maturation known from histology represent the background necessary for the understanding of maturation in order to be then able to evaluate brain maturation through neuroimaging. Illustrations of the normal cortical maturation are given for each step accessible to MRI for both the cerebral hemispheres and the posterior fossa.

[1]  S. Eik-Nes,et al.  Comparison of prenatal ultrasound and postmortem findings in fetuses and infants with central nervous system anomalies , 1998, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[2]  W. Nitz,et al.  Fast and ultrafast non-echo-planar MR imaging techniques , 2002, European Radiology.

[3]  D. Figarella-Branger,et al.  Fetal brain MR imaging. , 2001, Magnetic resonance imaging clinics of North America.

[4]  D. Levine,et al.  Normal Fetal Anatomy as Visualized with Fast Magnetic Resonance Imaging , 2001, Topics in magnetic resonance imaging : TMRI.

[5]  John G. Parnavelas,et al.  Modes of neuronal migration in the developing cerebral cortex , 2002, Nature Reviews Neuroscience.

[6]  H. Kinney,et al.  Sequence of Central Nervous System Myelination in Human Infancy. II. Patterns of Myelination in Autopsied Infants , 1988, Journal of neuropathology and experimental neurology.

[7]  M. Castillo.  Pediatric Neuroimaging, 3rd ed. , 2000 .

[8]  K. Nicolaides,et al.  Fetal biometry at 14–40 weeks' gestation , 1994, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[9]  Fabio Mosca,et al.  Apparent diffusion coefficient determination in normal fetal brain: a prenatal MR imaging study. , 2003, AJNR. American journal of neuroradiology.

[10]  Diane M Twickler,et al.  Fetal central nervous system ventricle and cisterna magna measurements by magnetic resonance imaging. , 2001, American journal of obstetrics and gynecology.

[11]  S. Back.  Recent advances in human perinatal white matter injury. , 2001, Progress in brain research.

[12]  N. Girard,et al.  In vivo MR study of brain maturation in normal fetuses. , 1995, AJNR. American journal of neuroradiology.

[13]  F. Gilles,et al.  MYELINATED TRACTS: GROWTH PATTERNS , 1983 .

[14]  A. Compston,et al.  Review: Glial lineages and myelination in the central nervous system , 1997 .

[15]  T. Ben-Hur,et al.  From Neural Stem Cells to Myelinating Oligodendrocytes , 1999, Molecular and Cellular Neuroscience.

[16]  C. Garel,et al.  Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. , 2001, AJNR. American journal of neuroradiology.

[17]  R M Henkelman,et al.  Relaxivity and magnetization transfer of white matter lipids at MR imaging: importance of cerebrosides and pH. , 1994, Radiology.

[18]  J. Voogd.  The human cerebellum , 2003, Journal of Chemical Neuroanatomy.

[19]  P. Sonigo,et al.  Features of the developing brain , 2003, Child's Nervous System.

[20]  H. Kinney,et al.  Myelination in the developing human brain: Biochemical correlates , 1994, Neurochemical Research.

[21]  J. Vion-Dury,et al.  Atlas of brain proton magnetic resonance spectra. Part I: General and methodological considerations. , 1998, Journal of neuroradiology. Journal de neuroradiologie.

[22]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[23]  D. Lev,et al.  Fetal brain imaging: a comparison between magnetic resonance imaging and dedicated neurosonography , 2004, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[24]  N. Girard,et al.  Ventriculomegaly and pericerebral CSF collection in the fetus: early stage of benign external hydrocephalus? , 2001, Child's Nervous System.

[25]  N. Baumann,et al.  Biology of oligodendrocyte and myelin in the mammalian central nervous system. , 2001, Physiological reviews.

[26]  Professor Dr. Jacob Valk,et al.  Magnetic Resonance of Myelin, Myelination, and Myelin Disorders , 1989, Springer Berlin Heidelberg.

[27]  R A Zimmerman,et al.  T2-Weighted fast MR imaging with true FISP versus HASTE: comparative efficacy in the evaluation of normal fetal brain maturation. , 2000, AJR. American journal of roentgenology.

[28]  P. Levitt.  Structural and functional maturation of the developing primate brain. , 2003, The Journal of pediatrics.

[29]  G. Fishell,et al.  Parsing the prosencephalon , 2002, Nature Reviews Neuroscience.

[30]  Nadine Girard,et al.  Fetal MR imaging , 2002, European Radiology.

[31]  M Takahashi,et al.  Normal fetal brain development: MR imaging with a half-Fourier rapid acquisition with relaxation enhancement sequence. , 2000, Radiology.

[32]  P. Parizel,et al.  A brief review of parallel magnetic resonance imaging , 2003, European Radiology.

[33]  Roland Kreis,et al.  Development of the human brain: In vivo quantification of metabolite and water content with proton magnetic resonance spectroscopy , 1993, Magnetic resonance in medicine.

[34]  J. Cardoza,et al.  Exclusion of fetal ventriculomegaly with a single measurement: the width of the lateral ventricular atrium. , 1988, Radiology.

[35]  Alan C. Evans,et al.  Maturation of white matter in the human brain: a review of magnetic resonance studies , 2001, Brain Research Bulletin.

[36]  S. Sourbron,et al.  Study of pediatric brain development using magnetic resonance imaging of anisotropic diffusion. , 2002, Magnetic resonance imaging.

[37]  D. Lev,et al.  A normal second‐trimester ultrasound does not exclude intracranial structural pathology , 2002, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[38]  T. Naidich,et al.  The developing cerebral surface. Preliminary report on the patterns of sulcal and gyral maturation--anatomy, ultrasound, and magnetic resonance imaging. , 1994, Neuroimaging clinics of North America.

[39]  N. Girard,et al.  MRI study of brain myelination. , 1991, Journal of neuroradiology. Journal de neuroradiologie.

[40]  J. A. Blake.  The roof and lateral recesses of the fourth ventricle, considered morphologically and embryologically , 1900 .

[41]  B. Brody,et al.  Sequence of Central Nervous System Myelination in Human Infancy. I. An Autopsy Study of Myelination , 1987, Journal of neuropathology and experimental neurology.

[42]  A. Alexander,et al.  Postmortem fetal MR imaging: comparison with findings at autopsy. , 1997, AJR. American journal of roentgenology.

[43]  M Takahashi,et al.  MR imaging of the fetus by a HASTE sequence. , 1997, AJR. American journal of roentgenology.

[44]  Arend Heerschap,et al.  Maturation of the human fetal brain as observed by 1H MR spectroscopy , 2002, Magnetic resonance in medicine.

[45]  M. Rivkin,et al.  Developmental neuroimaging of children using magnetic resonance techniques. , 2000, Mental retardation and developmental disabilities research reviews.

[46]  S. Dymarkowski,et al.  The value of fast MR imaging as an adjunct to ultrasound in prenatal diagnosis , 2003, European Radiology.

[47]  A. Hubbard,et al.  Ultrafast MR imaging of the normal posterior fossa in fetuses. , 2000, AJR. American journal of roentgenology.

[48]  B. Popko,et al.  Galactolipids are molecular determinants of myelin development and axo-glial organization. , 2002, Biochimica et biophysica acta.

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

[50]  D. Figarella-Branger,et al.  Fetal brain injury. , 2004, Journal of neuroradiology. Journal de neuroradiologie.

[51]  A. Kurtz,et al.  The atria of the fetal lateral ventricles: a sonographic study of normal atrial size and choroid plexus volume. , 1995, AJR. American journal of roentgenology.

[52]  A. Bosio,et al.  Galactosphingolipids and axono-glial interaction in myelin of the central nervous system , 1998, Cell and Tissue Research.

[53]  M. Götz,et al.  Radial Glial Cells Defined and MajorIntermediates between EmbryonicStem Cells and CNS Neurons , 2005, Neuron.

[54]  F. Gilles,et al.  TELENCEPHALIC DEVELOPMENT: CHANGING GYRAL PATTERNS , 1983 .

[55]  Orit A Glenn,et al.  Fetal MRI: a developing technique for the developing patient. , 2004, AJR. American journal of roentgenology.

[56]  Guy Sebag,et al.  Fetal MRI: normal gestational landmarks for cerebral biometry, gyration and myelination , 2003, Child's Nervous System.

[57]  J. Parnavelas,et al.  Radial Glial Cells Are They Really Glia? , 2001, Neuron.

[58]  C. Garel.  The role of MRI in the evaluation of the fetal brain with an emphasis on biometry, gyration and parenchyma , 2004, Pediatric Radiology.

[59]  S. Takashima,et al.  Neuronal maturation and N-acetyl-l-aspartic acid development in human fetal and child brains , 1997, Brain and Development.

[60]  Dagmar Timmann,et al.  MRI Atlas of the Human Cerebellar Nuclei , 2002, NeuroImage.

[61]  W. Ellis,et al.  A magnetic resonance template for normal neuronal migration in the fetus. , 1996, Neurosurgery.

[62]  Andrea Righini,et al.  Demonstration of acute ischemic lesions in the fetal brain by diffusion magnetic resonance imaging , 2002, Annals of neurology.

[63]  V. Friedrich,et al.  Progressive remodeling of the oligodendrocyte process arbor during myelinogenesis. , 1996, Developmental neuroscience.

[64]  K. Sawada,et al.  Normal and abnormal neuronal migration in the developing cerebral cortex. , 2002, The journal of medical investigation : JMI.

[65]  I. Timor-Tritsch,et al.  Development of fetal gyri, sulci and fissures: a transvaginal sonographic study , 1997, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[66]  Daniela Prayer,et al.  Diffusion-weighted magnetic resonance imaging of cerebral white matter development. , 2003, European journal of radiology.

[67]  H. Sarnat.  Ependymal Reactions to Injury. A Review , 1995, Journal of neuropathology and experimental neurology.

[68]  C. Adamsbaum,et al.  MRI of the fetal posterior fossa , 2005, Pediatric Radiology.

[69]  S. H. Koenig,et al.  Cholesterol of myelin is the determinant of gray‐white contrast in MRI of brain , 1991, Magnetic resonance in medicine.

[70]  R. Balaban,et al.  Magnetization transfer contrast (MTC) and tissue water proton relaxation in vivo , 1989, Magnetic resonance in medicine.

[71]  D. Levine,et al.  Cortical maturation in normal and abnormal fetuses as assessed with prenatal MR imaging. , 1999, Radiology.

[72]  P Blot,et al.  Supratentorial parenchyma in the developing fetal brain: in vitro MR study with histologic comparison. , 1997, AJNR. American journal of neuroradiology.

[73]  R S Balaban,et al.  Lipid bilayer and water proton magnetization transfer: Effect of cholesterol , 1991, Magnetic resonance in medicine.

[74]  Borut Marincek,et al.  Fetal magnetic resonance imaging of the brain: technical considerations and normal brain development , 2002, European Radiology.

[75]  A. Rossi,et al.  Cystic malformations of the posterior cranial fossa originating from a defect of the posterior membranous area , 1996, Child's Nervous System.

[76]  Deborah Levine,et al.  Fast Fetal Magnetic Resonance Imaging Techniques , 2001, Topics in magnetic resonance imaging : TMRI.