Structural, immunocytochemical, and mr imaging properties of periventricular crossroads of growing cortical pathways in preterm infants.

BACKGROUND AND PURPOSE Periventricular white matter (WM) areas are widely recognized as predilection sites for complex cellular damage after ischemia/reperfusion or inflammatory injury of the perinatal cerebrum. We analyzed histochemical and MR imaging properties of fiber architectonics and extracellular matrix (ECM) of periventricular areas to disclose the potential significance of topographically specific WM lesions for the neurodevelopmental outcome. METHODS We combined histochemical methods for demonstration of fibers, axonal guidance molecules, and ECM with T1-weighted MR images on postmortem specimens aged 15 to 36 postovulatory weeks (POW) and T2-weighted MR images on in vivo fetuses aged 14 to 26 POW. RESULTS The fiber architectonics of the fetal cerebrum display tangential axon strata in frontopolar and occipitopolar regions, whereas the central periventricular region contains crossroads of intersecting callosal (transverse), associative (sagittal), and thalamocortical/corticofugal (radial) fiber bundles. In early preterms, crossroads contain hydrophylic ECM with axonal guidance molecules, and they are easily recognized as hypointensities on T1-weighted MR images or hyperintensities on T2-weighted MR images. After the 28 POW, tangential fetal fiber-architectonic stratification transforms into the corona radiata system; however, the growth of cortical pathways continues in crossroad areas, as indicated by the presence of ECM and their distinct MR imaging signal intensities. CONCLUSIONS The correlation of MR imaging with histochemical findings demonstrated the presence of periventricular fiber crossroads rich in ECM and axonal guidance molecules. We propose that, in perinatal WM lesions, periventricular WM crossroads represent a hitherto unrecognized and vulnerable cellular and topographic target in which combined damage of association-commissural and projection fibers may explain the complexity of cognitive, sensory, and motor deficit in survivors of periventricular WM lesions.

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

[2]  A. Beltramello,et al.  Cerebral cortex three‐dimensional profiling in human fetuses by magnetic resonance imaging , 2004, Journal of anatomy.

[3]  C. Verney,et al.  Gestational Hypoxia Induces White Matter Damage in Neonatal Rats: A New Model of Periventricular Leukomalacia , 2004, Brain pathology.

[4]  P. Rakic,et al.  3 Setting the Stage for Cognition: Genesis of the Primate Cerebral Cortex , 2004 .

[5]  I. Kostović Guidance Cues in the Developing Brain , 2012, Progress in Molecular and Subcellular Biology.

[6]  J. Volpe Cerebral white matter injury of the premature infant-more common than you think. , 2003, Pediatrics.

[7]  David J Larkman,et al.  Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. , 2003, Pediatrics.

[8]  H. Kinney,et al.  Nitrosative and Oxidative Injury to Premyelinating Oligodendrocytes in Periventricular Leukomalacia , 2003, Journal of neuropathology and experimental neurology.

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

[10]  I. Kostović,et al.  Complex patterns and simple architects: molecular guidance cues for developing axonal pathways in the telencephalon. , 2003, Progress in molecular and subcellular biology.

[11]  Steven P. Miller,et al.  Serial quantitative diffusion tensor MRI of the premature brain: Development in newborns with and without injury , 2002, Journal of magnetic resonance imaging : JMRI.

[12]  M. Solaiyappan,et al.  Diffusion tensor imaging of periventricular leukomalacia shows affected sensory cortex white matter pathways , 2002, Neurology.

[13]  P. Rakic,et al.  Origin of GABAergic neurons in the human neocortex , 2002, Nature.

[14]  Milos Judas,et al.  Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants , 2002, The Anatomical record.

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

[16]  Henry Kennedy,et al.  Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. , 2002, Cerebral cortex.

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

[18]  J. Rothstein,et al.  Altered expressions of glutamate transporter subtypes in rat model of neonatal cerebral hypoxia-ischemia. , 2001, Brain research. Developmental brain research.

[19]  W. Chan,et al.  Axonal Patterns in the Prosencephalon of the Human Developing Brain , 2001, Neuroembryology and Aging.

[20]  O. Marín,et al.  A long, remarkable journey: Tangential migration in the telencephalon , 2001, Nature Reviews Neuroscience.

[21]  S. Takashima,et al.  Characteristic neuropathology and plasticity in periventricular leukomalacia. , 2001, Pediatric neurology.

[22]  P. Evrard Pathophysiology of Perinatal Brain Damage , 2001, Developmental Neuroscience.

[23]  Akira Ishida,et al.  The Developing Nervous System: A Series of Review Articles: Neurobiology of Hypoxic-Ischemic Injury in the Developing Brain , 2001, Pediatric Research.

[24]  Alan Leviton,et al.  Is Periventricular Leukomalacia an Axonopathy as Well as an Oligopathy? , 2001, Pediatric Research.

[25]  R. Kikinis,et al.  Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. , 2001, Pediatrics.

[26]  M. Segal,et al.  Quantitative analysis of MR images in asphyxiated neonates: correlation with neurodevelopmental outcome. , 2001, AJNR. American journal of neuroradiology.

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

[28]  E. Courchesne,et al.  Regional size reduction in the human corpus callosum following pre- and perinatal brain injury. , 2000, Cerebral cortex.

[29]  C Blakemore,et al.  Morphology and Growth Patterns of Developing Thalamocortical Axons , 2000, The Journal of Neuroscience.

[30]  L. D. de Vries,et al.  Asymmetrical myelination of the posterior limb of the internal capsule in infants with periventricular haemorrhagic infarction: an early predictor of hemiplegia. , 1999, Neuropediatrics.

[31]  Marc Tessier-Lavigne,et al.  Conservation and divergence of axon guidance mechanisms , 1999, Current Opinion in Neurobiology.

[32]  G M Bydder,et al.  Relationship between MR imaging and histopathologic findings of the brain in extremely sick preterm infants. , 1999, AJNR. American journal of neuroradiology.

[33]  B. Poll-The,et al.  Continuing education in neurometabolic disorders--serine deficiency disorders. , 1999, Neuropediatrics.

[34]  David N. Kennedy,et al.  MRI-Based Topographic Parcellation of Human Cerebral White Matter I. Technical Foundations , 1999, NeuroImage.

[35]  J. Perlman,et al.  White matter injury in the preterm infant: an important determination of abnormal neurodevelopment outcome. , 1998, Early human development.

[36]  E. Mercuri,et al.  Abnormal Magnetic Resonance Signal in the Internal Capsule Predicts Poor Neurodevelopmental Outcome in Infants With Hypoxic-Ischemic Encephalopathy , 1998, Pediatrics.

[37]  M. Levene,et al.  An atlas of neonatal brain sonography. , 1998 .

[38]  M. Saysell,et al.  MR features of developing periventricular white matter in preterm infants: evidence of glial cell migration. , 1998, AJNR. American journal of neuroradiology.

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

[40]  C. Shatz,et al.  Developmental changes revealed by immunohistochemical markers in human cerebral cortex. , 1996, Cerebral cortex.

[41]  A Leviton,et al.  Ventriculomegaly, delayed myelination, white matter hypoplasia, and "periventricular" leukomalacia: how are they related? , 1996, Pediatric neurology.

[42]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[43]  A. Pearlman,et al.  Extracellular matrix in early cortical development. , 1996, Progress in brain research.

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

[45]  P. Rakić,et al.  Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain , 1990, The Journal of comparative neurology.

[46]  I. Kostović,et al.  Structural and histochemical reorganization of the human prefrontal cortex during perinatal and postnatal life. , 1990, Progress in brain research.

[47]  P S Goldman-Rakic,et al.  Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain , 1983, The Journal of comparative neurology.

[48]  S. Hsu,et al.  The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase technics. , 1981, American journal of clinical pathology.

[49]  J. Volpe Neurology of the Newborn , 1959, Major problems in clinical pediatrics.

[50]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[51]  A. Minkowski,et al.  Regional Development of the Brain in Early Life , 1968 .

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

[53]  B. Banker,et al.  Periventricular leukomalacia of infancy. A form of neonatal anoxic encephalopathy. , 1962, Archives of neurology.

[54]  W. His Die Entwickelung des menschlichen Gehirns : während der ersten Monate , 1904 .

[55]  G. C. Die Entwicklung des menschlichen Gehirns wahrend der ersten Monate , 1904, Nature.