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The premature brain: developmental and lesional anatomy

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Abstract

Introduction

Neurodevelopmental outcome in prematures who suffer from a neonatal brain injury depends on the lesion itself, and on how the lesion interferes with the still developing functional anatomy.

Methods

Most of the neuronal migration is completed by midgestation. The second part of the gestation corresponds to the development of the connectivity and sulcation, of the maturation of the oligodendrocytic lineage and of the microglia, and of the vascular bed in the parenchyma beyond the germinal matrix.

Results

In this paper, the main processes of the developmental anatomy of the premature brain are reviewed, and are correlated with the findings in a prospective series of 105 premature infants born between 24 and 32 weeks of gestation, and serially examined with MR imaging at birth, at term-equivalent age, at 2 years, and at 4 years. Special emphasis was placed (1) on the intraventricular hemorrhage because of the resulting destruction of the germinal matrix and its impact on the late cellular production, (2) on the periventricular venous hemorrhagic infarction because of the selective destruction of the intermediate zone which is associated, and (3) on the apparently perivenous punctate lesions of the white matter because they involve the intermediate zone also, because they have no convincing explanation yet, and because the microglia seems to be associated with their pathogenesis.

Conclusion

These deep venous injuries appear to preserve the subplate zone, which is likely to be a significant element to consider in the perspective of the neurodevelopmental outcome.

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Abbreviations

CP:

Cortical plate

CST:

Cortico-spinal tract

DTI:

Diffusion tensor imaging

DWI/ADC:

Diffusion-weighted imaging–average diffusion coefficient

GA:

Gestational age

GE:

Ganglionic eminence

GM:

Germinal matrix

HIE:

Hypoxic-ischemic encephalopathy

IVH:

Intra-ventricular hemorrhage

IZ:

Intermediate zone

MRS:

Magnetic resonance spectroscopy

MTR:

Magnetization transfer ration

MZ:

Marginal zone

NICU:

Neonatal intensive care unit

PLIC:

Posterior limb of the internal capsule

PP:

Pre-plate

PVHI:

Periventricular venous hemorrhagic infarction

PVL:

Peri-ventricular leukomalacia

PVZ:

Peri-ventricular zone

SP:

Sub-plate

SVZ:

Subventricular zone

TEA:

Term-equivalent age

VZ:

Ventricular zone

References

  1. Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8(1):110–124

    Article  PubMed  Google Scholar 

  2. Nossin-Manor R, Chung AD, Morris D et al (2011) Optimized T1- and T2-weighted volumetric brain imaging as a diagnostic tool in very preterm neonates. Pediatr Radiol 41:702–710

    Article  PubMed  Google Scholar 

  3. Counsell SJ, Allsopp JM, Harrison MC et al (2003) Diffusion weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics 112:1–7

    Article  PubMed  Google Scholar 

  4. Inder TE, Warfield SK, Wang H et al (2005) Abnormal cerebral structure is present at term in premature infants. Pediatrics 115:286–294

    Article  PubMed  Google Scholar 

  5. Leijser LM, de Bruïne FT, Steggerda SJ et al (2009) Brain imaging findings in very preterm infants throughout the neonatal period: Part I. Incidence and evolution of lesions, comparison between ultrasound and MRI. Early Human Devel 85:101–109

    Article  Google Scholar 

  6. Hagman CF, De Vita E, Brainbridge A et al (2009) T2 at MR imaging is an objective quantitative measure of cerebral white matter signal intensity abnormality in preterm infants at term-equivalent age. Radiology 252:209–217

    Article  Google Scholar 

  7. Brown NG, Inder TE, Bear MJ et al (2009) Neurobehavior at term and white and gray matter abnormalities in very preterm infants. J Pediatr 155:32–38

    Article  PubMed  Google Scholar 

  8. Jinnou H, Kouwaki M, Kiyosawa S, Yokochi K (2009) Neonatal MRI in preterm infants with periventricular leukomalacia and mild disability. Pediatr Internat 51:780–785

    Article  Google Scholar 

  9. Hart AR, Smith MF, Rigby AS et al (2010) Appearances of diffuse excessive high signal intensity (DEHSI) on MR imaging following preterm birth. Pediatr Radiol 40:1390–1396

    Article  PubMed  Google Scholar 

  10. Boardman JP, Craven C, Valappil S et al (2010) A common neonatal image phenotype predicts adverse neurodevelopmental outcome in children born preterm. Neur Image 52:409–414

    CAS  Google Scholar 

  11. de Bruïne FT, van den Berg-Huysmans AA, Leijser LM et al (2011) Clinical implications of MR imaging findings in the white matter in very preterm infants. Radiology 261:899–906

    Article  PubMed  Google Scholar 

  12. Jeon TY, Kim JH, Joo SY et al (2012) Neurodevelopmental outcomes in preterm infants: comparison of infants with and without diffuse excessive high signal intensity on MR images at near-term-equivalent age. Radiology 263:518–526

    Article  PubMed  Google Scholar 

  13. Smyser CD, Kidokoro H, Inder TE (2012) Magnetic resonance imaging of the brain at term equivalent age in extremely premature neonates: to scan or not to scan? Child Health 48:794–800

    Google Scholar 

  14. Counsell SJ, Rutherford MA, Cowan FM, Edwards AD (2003) Magnetic resonance imaging of preterm brain injury. Arch Dis Child Fetal Neonatal Ed 88:F269–F274

    Article  CAS  PubMed  Google Scholar 

  15. Miller SP, Ferreiro DM, Leonard C et al (2005) Early brain injury in premature newborns detected with magnetic resonance imaging is associated with adverse early neurodevelopmental outcome. J Pediatr 147:609–616

    Article  PubMed  Google Scholar 

  16. Dyet LE, Kennea N, Counsell SJ et al (2006) Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 118:536–548

    Article  PubMed  Google Scholar 

  17. Glass HC, Bonifacio SL, Sullivan J et al (2009) Magnetic resonance imaging and ultrasound injury in preterm infants with seizures. J Child Neurol 24:1105–1111

    Article  PubMed  Google Scholar 

  18. Rutherford MA, Supramaniam V, Ederies A et al (2010) Magnetic resonance imaging of white matter disease of prematurity. Neuroradiology 52:505–521

    Article  PubMed  Google Scholar 

  19. Niwa T, de Vries LS, Benders MJNL et al (2011) Punctate white matter lesions in infants: new insights using susceptibility-weighted imaging. Neuroradiology 53:669–679

    Article  PubMed  Google Scholar 

  20. Bystron I, Blakemore C, Rakic P (2008) Development of the human cerebral cortex: Boulder Committee revisited. Nature Rev Neurosci 9:110–122

    Article  CAS  Google Scholar 

  21. Kanold PO, Luhmann HJ (2010) The subplate and early cortical circuits. Ann Rev Neurosci 33:23–48

    Article  CAS  PubMed  Google Scholar 

  22. Kostovic I, Judas M, Rados M, Hrabac P (2002) Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cerebral Cortex Mon 12:536–544

    Article  Google Scholar 

  23. Montiel JF, Wang WZ, Oeschger FM et al (2011) Hypothesis on the dual origin of the mammalian subplate. Front Neuroanatomy 1:5–25

    Google Scholar 

  24. Judas M, Sedmak G, Pletikos M, Jovanov-Milosevic N (2010) Populations of subplate and interstitial neurons in fetal and adult human telencephalon. J Anat 217:381–399

    Article  PubMed  Google Scholar 

  25. Kriegstein AR, Noctor SC (2004) Pattern of neuronal migration in the embryonic cortex. Trends Neurosci 27:392–399

    Article  CAS  PubMed  Google Scholar 

  26. Faux C, Rakic S, Andrews W, Britto JM (2012) Neurons on the move: migrations and lamination of cortical interneurons. Neurosignals 20:164–185

    Article  CAS  Google Scholar 

  27. Del Bigio MR (2011) Cell proliferation in human ganglionic eminence and suppression after prematurity-associated haemorrhage. Brain 134:1344–1361

    Article  PubMed  Google Scholar 

  28. Haynes RL, Borenstein NS, Desilva TM, Folkerth RD et al (2005) Axonal development in the cerebral white matter of the human fetus and infant. J Comp Neurol 484:156–167

    Article  PubMed  Google Scholar 

  29. ten-Donkelaar HJ, Lammens M, Hori A (2006) Clinical neuroembryology. Springer, Berlin

    Google Scholar 

  30. Marin-Padilla M (1970) Prenatal and early postnatal ontogenesis of the human motor cortex: a Golgi study. I. The sequential development of the cortical layers. Brain Res 23:167–183

    Article  CAS  PubMed  Google Scholar 

  31. Smart IHM, McSherry GM (1986) Gyrus formation in the cerebral cortex of the ferret. II. Description of the internal histological changes. J Anat 147:27–43

    CAS  PubMed  Google Scholar 

  32. Ferrer I, Hernandez-Marti M, Bernet E, Galofre E (1988) Formation and growth of the cerebral convolutions. I. Postnatal development of the median-suprasylvian gyrus and adjoining sulci in the cat. J Anat 160:89–100

    CAS  PubMed  Google Scholar 

  33. Ferrer I, Hernandez-Marti M, Bernet E, Calopa M (1989) Formation and growth of the cerebral convolutions. II. Cell death in the gyrus suprasylvius and adjoining sulci in the cat. Develop Brain Res 45:303–308

    Article  CAS  Google Scholar 

  34. Sarnat HB, Flores-Sarnat L (2013) Radial microcolumnar cortical architecture: maturational arrest or cortical dysplasia. Pediatr Neurol 48:259–270

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  36. du Plessis A (2009) Cerebral blood flow and metabolism in the developing fetus. Clin Perinatol 36:531–548

    Article  PubMed  Google Scholar 

  37. Streeter GL (1918) The developmental alterations in the vascular system of the brain of the human embryo. Contrib Embryol 271(24):5–38

    Google Scholar 

  38. Klosovskii BN (1963) Chapter 1. Fundamental facts concerning the stages and principles of development of the brain and its response to noxious agents. In: The development of the brain and its disturbance by harmful factors. Pergamon Press, London, pp 3–43

    Google Scholar 

  39. Sabin FR (1917) Preliminary note on the differentiation of angioblasts and the method by which they produce blood-vessels, blood-plasma and red blood-cells as seen in the living chick. Anat Rec 13:199–204

    Article  Google Scholar 

  40. Sabin FR (1917) Origin and development of the primitive vessels of the chick and the pig. Contrib Embryol 226(6):61–124

    Google Scholar 

  41. Allsopp G, Gamble HJ (1979) Light and electron microscopic observations on the development of the blood vascular system of the human brain. J Anat 128:461–477

    CAS  PubMed  Google Scholar 

  42. Kuban KC, Gilles FH (1985) Human telencephalic angiogenesis. Ann Neurol 17:539–548

    Article  CAS  PubMed  Google Scholar 

  43. Norman MG, O’Kusky JR (1986) The growth and development of the microvasculature in the human cortex. J Neuropathol Exp Neurol 45:222–232

    CAS  PubMed  Google Scholar 

  44. Padget DH (1957) The development of the cranial venous system in man from the view point of comparative anatomy. Contrib Embryol 247:81–140

    Google Scholar 

  45. Raybaud C (2010) Normal and abnormal embryology and development of the intracranial vascular system. Neurosurg Clin N Am 21:399–426

    Article  PubMed  Google Scholar 

  46. Marin-Padilla M (2012) The human brain microvascular system: development and structure. Front Neuroanat 6:38

    Article  PubMed  Google Scholar 

  47. Mito T, Konomi H, Houdou S, Takashima S (1991) Immunohistological study of the vasculature of the developing brain. Pediatr Neurol 7:18–22

    Article  CAS  PubMed  Google Scholar 

  48. Ballabh P, Braun A, Nedergaard M (2004) Anatomic analysis of blood vessels in germinal matrix, cerebral cortex, and white matter in developing infants. Pediatr Res 56:117–124

    Article  PubMed  Google Scholar 

  49. Anstrom JA, Thore CR, Moody DM, Brown WR (2007) Immunolocalization of tight junction proteins in blood vessels in human germinal matrix and cortex. Histochem Cell Biol 127:205–213

    Article  CAS  PubMed  Google Scholar 

  50. Anstrom JA, Brown WR, Moody DM et al (2004) Subependymal veins in premature neonates: implications for hemorrhage. Pediatr Neurol 30:46–53

    Article  PubMed  Google Scholar 

  51. Nakamura Y, Okudera T, Hashimoto T (1994) Vascular archtecture in white matter of neonates: its relationship to periventricular leukomalacia. J Neuropathol Exp Neurol 53:582–589

    Article  CAS  PubMed  Google Scholar 

  52. Okudera T, Huang PY, Fukusumi A et al (1999) Micro-angiographical studies of the medullary venous system of the cerebral hemisphere. Neuropathol 19:93–111

    Article  CAS  Google Scholar 

  53. Degani S (2009) Evaluation of fetal cerebrovascular circulation and brain development: the role of ultrasound and Doppler. Semin Perinatol 33:259–269

    Article  PubMed  Google Scholar 

  54. Cruz-Martinez R, Figueras F, Hernandez-Andrade E et al (2011) Normal reference ranges of fetal regional blood perfusion as measured by fractional moving blood volume. Ultrasound Obstet Gynecol 37:196–201

    Article  CAS  PubMed  Google Scholar 

  55. Altman DI, Powers WJ, Perlman JM et al (1988) Cerebral blood flow requirement for brain viability in newborn infants is lower than in adults. Ann Neurol 24:218–226

    Article  CAS  PubMed  Google Scholar 

  56. Børch K, Greisen G (1998) Blood flow distribution in the human preterm brain. Pediatr Res 43:28–33

    Article  PubMed  Google Scholar 

  57. Børch K, Lou HC, Greisen G (2010) Cerebral white matter blood flow and arterial blood pressure in preterm infants. Acta Paediatr 99:1489–1492

    Article  PubMed  Google Scholar 

  58. Meek JH, Tyszczuk L, Elwell CE, Wyatt JS (1998) Cerebral blood flow increases over the first three days of life in extremely preterm neonates. Arch Dis Child Fetal Neonatal Ed 78:F33–F37

    Article  CAS  PubMed  Google Scholar 

  59. Pellicer A, Valverde E, Gayá F et al (2001) Postnatal adaptation of brain circulation in preterm infants. Pediatr Neurol 24:103–109

    Article  CAS  PubMed  Google Scholar 

  60. Kehrer M, Blumenstock G, Ehehalt S et al (2005) Development of cerebral blood flow volume in preterm neonates during the first two weeks of life. Pediatr Res 58:927–930

    Article  PubMed  Google Scholar 

  61. Freeman MR (2010) Specification and morphogenesis of astrocytes. Sxcience 330:774–778

    Article  CAS  Google Scholar 

  62. Zecevic N (2004) Specific characteristic of radial glia in the human fetal telencephalon. Glia 48:27–35

    Article  PubMed  Google Scholar 

  63. Bushong EA, Martone ME, Ellisman MH (2004) Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Devl Neuroscience 22:73–86

    Article  Google Scholar 

  64. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119:7–35

    Article  PubMed  Google Scholar 

  65. Chaboub LS, Deneen B (2012) Developmental origins od astrocyte heterogeneity: the final frontier of CNS development. Dev Neurosci 34:379–388

    Article  CAS  PubMed  Google Scholar 

  66. Jakovcevski I, Filipovic R, Mo ZC et al (2009) Oligodendrocyte development and the onset of myelination in the human fetal brain. Front Neuroanat 3:5

    Article  PubMed  CAS  Google Scholar 

  67. Bradl M, Lassmann H (2010) Oligodendrocytes: biology and pathology. Acta Neuropathol 119:37–53

    Article  PubMed  Google Scholar 

  68. Back SA, Luo NL, Borenstein NS et al (2001) Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 21:1302–1312

    CAS  PubMed  Google Scholar 

  69. Back SA, Luo NL, Borenstein NS et al (2002) Arrested oligodendrocytic lineage progression during human cerebral white matter development: dissociation between the timing of progenitor differentiation and myelinogenesis. J Neuropathol Exp Neurol 61:197–211

    PubMed  Google Scholar 

  70. Flechsig P (1920) Anatomie des menschlichen Gehirns und Rückenmarks. Georg Thieme Verlag, Leipzig

    Google Scholar 

  71. Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA (2011) The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int J Dev Neurosci 29:423–440

    Article  CAS  PubMed  Google Scholar 

  72. Buser JR, Maire J, Riddle A et al (2012) Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 71:93–109

    Article  PubMed  Google Scholar 

  73. Verney C, Pogledic I, Biran V et al (2012) Microglial reaction in axonal crossroads is a hallmark of non-cystic periventricular white matter injury in very preterm infants. J Neuropathol Exp Neurol 71:251–264

    Article  CAS  PubMed  Google Scholar 

  74. Rezaie P, Dean A, Male D, Ulfig N (2005) Microglia in the cerebral wall of the human telencephalon at second trimester. Cereb Cortex 15:938–949

    Article  PubMed  Google Scholar 

  75. Monier A, Evrard P, Gressens P, Verney C (2006) Distribution and differentiation of microglia in the human encephalon during the first two trimesters of gestation. J Comp Neurol 499:565–582

    Article  CAS  PubMed  Google Scholar 

  76. Verney C, Monier A, Fallet-Bianco C, Gressens P (2010) Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants. J Anat 217:436–448

    Article  PubMed  Google Scholar 

  77. Judas M, Rados M, Jovanov-Milosevic N et al (2005) Structural, immunocytochemical, and MR imaging properties of periventricular crossroads of growing cortical pathways in preterm infants. Am J Neuroradiol AJNR 26:2671–2684

    Google Scholar 

  78. Volpe JJ (1989) Intraventricular hemorrhage in the premature infant: current concepts. Ann Neurol 25:3–11

    Article  CAS  PubMed  Google Scholar 

  79. Ghazi-Birry HS, Brown WR, Moody DM et al (1997) Human germinal matrix: venous origin of hemorrhage and vascular characteristics. AJNR Am J Neuroradiol 18:219–229

    CAS  PubMed  Google Scholar 

  80. Ballabh P (2010) Intraventricular hemorrhage in premature infants: mechanism of disease. Pediatr Res 67:1–8

    Article  PubMed  Google Scholar 

  81. Tsitouras V, Sgouros S (2011) Infantile post hemorrhagic hydrocephalus. Childs Nerv Syst 27:1595–1608

    Article  PubMed  Google Scholar 

  82. Jary S, De Carli A, Ramenghi LA, Whitelaw A (2012) Impaired brain growth and neurodevelopment in preterm infants with posthaemorrhagic ventricular dilatation. Acta Paediatr 101:743–8

    Google Scholar 

  83. Vasileiadis GT, Gelman N, Han VKM et al (2004) Uncomplicated intraventricular hemorrhage is followed by reduced cortical volume at near-term age. Pediatrics 114:e367–e372

    Article  PubMed  Google Scholar 

  84. Bulat M, Klarica M (2011) Recent insight into a new hydrodynamics of the cerebrospinal fluid. Brain Res Rev 65:99–112

    Article  PubMed  Google Scholar 

  85. Filippidis AS, Kalani MY, Rekate HL (2011) Hydrocephalus and aquaporins: lessons learned from the bench. Childs Nerv Syst 27:27–33

    Article  PubMed  Google Scholar 

  86. Del Bigio MR (1993) Neuropathological changes caused by hydrocephalus. Acta Neuropathol 85:573–585

    Article  PubMed  Google Scholar 

  87. Takashima S, Mito T, Ando Y (1986) Pathogenesis of periventricular white matter hemorrhages in preterm infants. Brain Dev 8:25–30

    Article  CAS  PubMed  Google Scholar 

  88. Gould SJ, Howard S, Hope PL, Reynolds EOR (1987) Periventricular intraparenchymal cerebral haemorrhage in preterm infants: the role of venous infarction. J Pathol 151:197–202

    Article  CAS  PubMed  Google Scholar 

  89. Counsell SJ, Maalouf EF, Rutherford MA, Edwards AD (1999) Periventricular haemorrhagic infarct in a preterm neonate. Eur J Paediatr Neurol 3:25–28

    Article  CAS  PubMed  Google Scholar 

  90. De Vries LS, Roelants-van Rijn AM, Rademaker KJ et al (2001) Unilateral parenchymal haemorrhagic infarction in the preterm infant. Eur J Paediatr Neurol 5:139–149

    Article  PubMed  Google Scholar 

  91. Levene MI, de Vries LS (1984) Extension of neonatal intraventricular hemorrhage. Arch Dis Child 59:631–636

    Article  CAS  PubMed  Google Scholar 

  92. Rushton DI, Preston PR, Durbin GM (1985) Structure and evolution of echo dense lesions in the neonatal brain. A combined ultrasound and necropsy study. Arch Dis Child 60:798–808

    Article  CAS  PubMed  Google Scholar 

  93. Harteman JC, Nikkels PGJ, Kwee A et al (2012) Pattern of placental pathology in preterm infants with a periventricular haemorrhagic infarction: association with time of onset and clinical presentation. Placenta 33:839–844

    Article  CAS  PubMed  Google Scholar 

  94. Wolf BS, Huang YP (1964) The subependymal veins of the lateral ventricle. AJR Am J Roentgenol 90:474–489

    Google Scholar 

  95. Dudink J, Lequin M, Weisglas-Kuperus N et al (2008) Venous subtypes of preterm periventricular haemorrhagic infarction. Arch Dis Child Fetal Neonatal Ed 93:F201–F206

    Article  CAS  PubMed  Google Scholar 

  96. Arrigoni F, Parazzini C, Righini A et al (2011) Deep medullary vein involvement in neonates with brain damage: an MR imaging study. AJNR Am J Neuroradiol 32:2030–2036

    Article  CAS  PubMed  Google Scholar 

  97. Maitre NL, Marshall DD, Price WA et al (2009) Neurodevelopmental outcome in infants with unilateral or bilateral periventricular hemorrhagic infarction. Pediatrics 124:e1153–e1160

    Article  PubMed  Google Scholar 

  98. Staudt M (2010) Reorganization after pre- and perinatal brain lesions. J Anat 217:469–474

    Article  PubMed  Google Scholar 

  99. Marin-Padilla M (1996) Developmental neuropathology and impact of perinatal brain damage. I: Hemorrhagic lesions of neocortex. J Neuropathol Exp Neurol 55:758–773

    Article  CAS  PubMed  Google Scholar 

  100. Marin-Padilla M (1997) Developmental neuropathology and impact of perinatal brain damage. II: White matter lesions of the cortex. J Neuropathol Exp Neurol 56:219–235

    Article  CAS  PubMed  Google Scholar 

  101. Blümcke I, Thom M, Aronica E et al (2011) The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 52:158–174

    Article  PubMed  Google Scholar 

  102. Keeney SE, Adcock EW, McArdle CB (1991) Prospective observations of 100 high-risk neonates by high-field (1.5 Tesla) manetic resonance imaging of the central nervous system. II. Lesions associated with hypoxic-ischemic encephalopathy. Pediatrics 87:431–438

    CAS  PubMed  Google Scholar 

  103. Baenziger O, Martin E, Steinlin M et al (1993) Early pattern recognition in severe perinatal asphyxia: a prospective MRI study. Neuroradiology 35:437–442

    Article  CAS  PubMed  Google Scholar 

  104. Childs AM, Cornette L, Ramenghi L et al (2001) Magnetic resonance and cranial ultrasound characteristics of periventricular white matter abnormalities in newborn infants. Clin Radiol 56:647–655

    Article  CAS  PubMed  Google Scholar 

  105. Cornette LG, Tanner SF, Ramenghi LA et al (2002) Magnetic resonance of the infant brain: anatomical characteristics and clinical significance of the punctate lesions. Arch Dis Child Fetal Neonatal Ed 86:F171–F177

    Article  CAS  PubMed  Google Scholar 

  106. Ramenghi LA, Fumagalli M, Righini A et al (2007) Magnetic resonance imaging assessment of brain maturation in preterm neonates with punctate white matter lesions. Neuroradiology 49:161–167

    Article  PubMed  Google Scholar 

  107. Li AM, Chau V, Poskitt KJ et al (2009) White matter injury in term newborn with neonatal encephalopathy. Pediatr Res 65:85–89

    Article  PubMed  Google Scholar 

  108. Bassi L, Chew A, Merchant N et al (2011) Diffusion tensor imaging in preterm infants with punctate white matter lesions. Pediatr Res 69:561–566

    Article  PubMed  Google Scholar 

  109. Kato T, Okumura A, Tsuji T et al (2012) Punctate white matter lesions in a late preterm-born infant with hypoxic-ischaemic encephalopathy: chronological changes in magnetic resonance imaging. Dev Med Child Neurol 54:862

    Article  PubMed  Google Scholar 

  110. Kaur C, Ling EA (2009) Periventricular white matter damage in the hypoxic neonatal brain: role of microglial cells. Prog Neurobiol 87:264–280

    Article  CAS  PubMed  Google Scholar 

  111. Graeber MB (2010) Changing face of microglia. Science 330:783–788

    Article  CAS  PubMed  Google Scholar 

  112. Billiards SS, Haynes RL, Folkerth RD et al (2006) Development of microglia in the cerebral white matter of the human fetus and infant. J Comp Neurol 497:199–208

    Article  PubMed  Google Scholar 

  113. Hristova M, Cuthill D, Zbarsky V et al (2010) Activation and deactivation of periventricular white matter phagocytes during postnatal mouse development. Glia 58:11–28

    Article  PubMed  Google Scholar 

  114. Banker BQ, Larroche JC (1962) Periventricular leukomalacia of infancy. Arch Neurol 7:386–410

    Article  CAS  PubMed  Google Scholar 

  115. Friede RL (1975) Developmental neuropathology. Springer, Wien

    Book  Google Scholar 

  116. Golden JA, Gilles FH, Rudelli R, Leviton A (1997) Frequency of neuropathological abnormalities in very low birth weight infants. J Neuropathol Exp Neurol 56:472–478

    Article  CAS  PubMed  Google Scholar 

  117. Volpe JJ (2001) Neurology of the newborn. Saunders, Philadelphia

    Google Scholar 

  118. Riddle A, Maire J, Gong X et al (2012) Differential susceptibility to axonopathy in necrotic and non-necrotic perinatal white matter injury. Stroke 43:178–184

    Article  PubMed  Google Scholar 

  119. McQuillen PS, Sheldon RA, Shatz CJ, Ferreiro DM (2003) Selective vulnerability of subplate neurons after early neonatal hypoxia-ischemia. J Neurosci 23:3308–3315

    CAS  PubMed  Google Scholar 

  120. Kinney HC, Haynes RL, Xu G et al (2012) Neuron deficit in the white matter and subplate in periventricular leukomalacia. Ann Neurol 71:397–406

    Article  PubMed  Google Scholar 

  121. Leviton A, Gressens P (2007) Neuronal damage accompanies perinatal white-matter damage. TINS Trends Neurosci 30:473–478

    Article  CAS  Google Scholar 

  122. Pierson CR, Folkerth RD, Billiards SS et al (2007) Gray matter injury associated with periventricular leukomalacia in the premature infant. Acta Neuropathol 114:619–631

    Article  PubMed  Google Scholar 

  123. Benders MJNL, Groenendaal F, Uiterwaal CSPM, de Vries LS (2008) Perinatal arterial stroke in the preterm infant. Semin Perinatol 32:344–349

    Article  PubMed  Google Scholar 

  124. Golomb MR, Garg BP, Edwards-Brown M, Williams LS (2008) Very early arterial ischemic stroke in premature infants. Pediatr Neurol 38:329–334

    Article  PubMed  Google Scholar 

  125. Ahdab-Barmada M, Moossy J, Painter M (1980) Pontosubicular necrosis and hyperoxemia. Pediatrics 66:840–847

    CAS  PubMed  Google Scholar 

  126. Takashima S, Itoh M, Oka A (2009) A history of our understanding of cerebral vascular development and pathogenesis of perinatal brain damage over the past 30 years. Semin Pediatr Neurol 16:226–236

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors thank John Wiley and Sons for permission to reproduce Fig. 5A from Okudera et al. Microangiographical studies of the medullary venous system of the cerebral hemisphere. Neuropathology 1999, 19:93–111 (reference 52 here).

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We declare that we have no conflict of interest.

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Correspondence to Charles Raybaud.

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This article is part of the special supplement “The Premature Brain"—Guest Editor: Charles Raybaud

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Raybaud, C., Ahmad, T., Rastegar, N. et al. The premature brain: developmental and lesional anatomy. Neuroradiology 55 (Suppl 2), 23–40 (2013). https://doi.org/10.1007/s00234-013-1231-0

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  • DOI: https://doi.org/10.1007/s00234-013-1231-0

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