Neuroradiology

, Volume 52, Issue 6, pp 447–477 | Cite as

The corpus callosum, the other great forebrain commissures, and the septum pellucidum: anatomy, development, and malformation

Topic Article

Abstract

There are three telencephalic commissures which are paleocortical (the anterior commissure), archicortical (the hippocampal commissure), and neocortical. In non-placental mammals, the neocortical commissural fibers cross the midline together with the anterior and possibly the hippocampal commissure, across the lamina reuniens (joining plate) in the upper part of the lamina terminalis. In placental mammals, a phylogenetically new feature emerged, which is the corpus callosum: it results from an interhemispheric fusion line with specialized groups of mildline glial cells channeling the commissural axons through the interhemispheric meninges toward the contralateral hemispheres. This concerns the frontal lobe mainly however: commissural fibers from the temporo-occipital neocortex still use the anterior commissure to cross, and the posterior occipito-parietal fibers use the hippocampal commissure, forming the splenium in the process. The anterior callosum and the splenium fuse secondarily to form the complete commissural plate. Given the complexity of the processes involved, commissural ageneses are many and usually associated with other diverse defects. They may be due to a failure of the white matter to develop or to the commissural neurons to form or to migrate, to a global failure of the midline crossing processes or to a selective failure of commissuration affecting specific commissural sites (anterior or hippocampal commissures, anterior callosum), or specific sets of commissural axons (paleocortical, hippocampal, neocortical commissural axons). Severe hemispheric dysplasia may prevent the axons from reaching the midline on one or both sides. Besides the intrinsically neural defects, midline meningeal factors may prevent the commissuration as well (interhemispheric cysts or lipoma). As a consequence, commissural agenesis is a malformative feature, not a malformation by itself. Good knowledge of the modern embryological data may allow for a good understanding of a specific pattern in a given individual patient, paving the way for better clinical correlation and genetic counseling.

Keywords

Corpus callosum Anterior commissure Hippocampal commissure Septum pellucidum Commissural anatomy Commissural development Commissural malformation Commissural agenesis 

Notes

Conflict of interest statement

I declare that I have no conflict of interest.

References

  1. 1.
    Rakic P, Yakovlev PI (1968) Development of the corpus callosum and cavum septi in man. J Comp Neurol 132:45–72PubMedCrossRefGoogle Scholar
  2. 2.
    Déjerine J. Anatomie des Centres Nerveux, vol 1. Rueff, Paris, 1895. Masson, Paris, 1980, pp 119-120, 738-741 (reprint)Google Scholar
  3. 3.
    Silver J, Lorenz SE, Wahlsten D, Coughlin J (1982) Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J Comp Neurol 210:10–29PubMedCrossRefGoogle Scholar
  4. 4.
    Katz MJ, Lasek RJ, Silver J (1983) Ontophyletics of the nervous system: development of the corpus callosum and evolution of axon tracts. Proc Natl Acad Sci USA 80:5936–5940PubMedCrossRefGoogle Scholar
  5. 5.
    Wahlsten D (1987) Defects of the fetal forebrain in mice with hereditary agenesis of the corpus callosum. J Comp Neurol 262:227–241PubMedCrossRefGoogle Scholar
  6. 6.
    Hankin MH, Schneider BF, Silver J (1988) Death of the subcallosal glial sling is correlated with formation of the cavum septi pellucidi. J Comp Neurol 272:191–202PubMedCrossRefGoogle Scholar
  7. 7.
    Koester SE, O’Leary DM (1994) Axons of early generated neurons in cingulate cortex pioneer the corpus callosum. J Neurosci 14:6608–6620PubMedGoogle Scholar
  8. 8.
    Livy DJ, Wahlsten D (1997) Retarded formation of the hippocampal commissure in embryos from mouse strains lacking a corpus callosum. Hippocampus 7:2–14PubMedCrossRefGoogle Scholar
  9. 9.
    Shu T, Richards LJ (2001) Cortical axon guidance by the glial wedge during the development of the corpus callosum. J Neurosci 21:2749–2758PubMedGoogle Scholar
  10. 10.
    Richards LJ (2002) Axonal pathfinding mechanisms at the cortical midline and in the development of the corpus callosum. Braz J Med Biol Res 35:1431–1439PubMedCrossRefGoogle Scholar
  11. 11.
    Shu T, Puche AC, Richards LJ (2003) Development of midline glial populations at the corticoseptal boundary. J Neurobiol 57:81–94PubMedCrossRefGoogle Scholar
  12. 12.
    Shu T, Li Y, Keller A, Richards LJ (2003) The glial sling is a migratory population of developing neurons. Development 130:2929–2937PubMedCrossRefGoogle Scholar
  13. 13.
    Richards LJ, Plachez C, Ren T (2004) Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human. Clin Genet 66:276–289PubMedCrossRefGoogle Scholar
  14. 14.
    Lent R, Uziel D, Baudrimont M, Fallet C (2005) Cellular and molecular tunnels surrounding the forebrain commissures of human fetuses. J Comp Neurol 483:375–382PubMedCrossRefGoogle Scholar
  15. 15.
    Ren T, Anderson A, Shen WB et al (2006) Imaging, anatomical and molecular analysis of callosal formation in the developing human fetal brain. Anat Record Part A 288A:191–204CrossRefGoogle Scholar
  16. 16.
    Vulliemoz S, Raineteau O, Jahaudon D (2005) Reaching beyond the midline: why are human brains cross wired? Lancet Neurology 4:87–99PubMedCrossRefGoogle Scholar
  17. 17.
    Abbie AA (1939) The origin of the corpus callosum and the fate of the structures related to it. J Comp Neurol 70:9–44CrossRefGoogle Scholar
  18. 18.
    Ariëns Kappers CU, Huber GC, Crosby EC. The comparative anatomy of the nervous system of vertebrates including man, vol III. Hafner, New York, 1967Google Scholar
  19. 19.
    Sarnat HB, Netsky MG (1974) Evolution of the nervous system. Oxford University Press, New YorkGoogle Scholar
  20. 20.
    Romer AS, Parsons TS (1977) The vertebrate body. Saunders, PhiladelphiaGoogle Scholar
  21. 21.
    Aboitiz F (2003) Montiel J. One hundred million years of interhemispheric communication: the history of the corpus callosum Braz J Med Biol Res 36:409–420Google Scholar
  22. 22.
    Yakovlev PI (1968) Telencephalon “impar”, “semipar”, “totopar” (morphogenetic, tectogenetic, and architectonic definitions). Int J Neurol 6:245–265PubMedGoogle Scholar
  23. 23.
    Gloor P, Salanova V, Olivier A, Quesney LF (1993) The human dorsal hippocampal commissure. Brain 116:1249–1273PubMedCrossRefGoogle Scholar
  24. 24.
    Amaral DG, Insausti R, Cowan WM (1984) The commissural connections of the monkey hippocampal formation. J Comp Neurol 224:307–336PubMedCrossRefGoogle Scholar
  25. 25.
    Demeter S, Rosene DL, Van Hoesen GW (1985) Interhemispheric pathways of the hippocampal formation, presubiculum and entorhinal and posterior parahippocampal cortices in the rhesus monkey: the structure and organization of the hippocampal commissures. J Comp Neurol 233:30–47PubMedCrossRefGoogle Scholar
  26. 26.
    Guénot M. Transfert interhémisphérique et agénésie du corps calleux. Capacités et limites de la commissure blanche antérieure. Neurochirurgie (Paris) 1998, 44(Suppl 1):113-115Google Scholar
  27. 27.
    Lamantia AS, Rakic P (1990) Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey. J Comp Neurol 291:520–537PubMedCrossRefGoogle Scholar
  28. 28.
    Di Virgilio G, Clarke S, Pizzolato G, Schaffner T (1999) Cortical regions contributing to the anterior commissure in man. Exp Brain Res 124:1–7PubMedCrossRefGoogle Scholar
  29. 29.
    Wilson CL, Isokawa M, Babb TL, Crandall PH. Functional connections in the human temporal lobe. I. Analysis of limbic system pathways using neuronal response evoked by electrical stimulation. Exp Brain Re 1990, 82:279-292Google Scholar
  30. 30.
    Wilson CL, Isokawa M, Babb TL et al (1991) Functional connections in the human temporal lobe. II. Evidence for a loss of functional linkage between contralateral limbic structures. Exp Brain Res 85:174–187PubMedCrossRefGoogle Scholar
  31. 31.
    Spencer SS, Williamson PD, Spencer DD, Mattson RH (1987) Human hippocampal seizure spread studied by depth and subdural recording: the hippocampal commissure. Epilepsia 28:479–489PubMedCrossRefGoogle Scholar
  32. 32.
    Phelps EA, Hirst W, Gazzaniga MS (1991) Deficits in recall following partial and complete commissurotomy. Cerebral cortex 1:492–498PubMedCrossRefGoogle Scholar
  33. 33.
    Kier EL, Truwit CL (1997) The lamina rostralis: modification of concepts concerning the anatomy, embryology, and MR appearance of the rostrum of the corpus callosum. AJNR Am J Neuroradiol 18:715–722PubMedGoogle Scholar
  34. 34.
    Velut S, Destrieux C, Kakou M (1998) Anatomie morphologique du corps calleux. Neurochirurgie (Paris) 44(Suppl 1):17–30Google Scholar
  35. 35.
    Hofer S, Frahm J (2006) Topography of the human corpus callosum revisited—comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. NeuroImage 32:989–994PubMedCrossRefGoogle Scholar
  36. 36.
    Kier L, Truwit CL (1996) The normal and abnormal genu of the corpus callosum: an evolutionary, embryologic, anatomic and MR analysis. AJNR Am J Neuroradiol 17:1631–1641PubMedGoogle Scholar
  37. 37.
    Aboitiz F, Scheibel AB, Fisher RS, Zaidel E (1992) Fiber composition of the corpus callosum. Brain Res 598:143–153PubMedCrossRefGoogle Scholar
  38. 38.
    Widjaja E, Nilsson D, Blaser S, Raybaud C (2008) White matter abnormalities in children with idiopathic developmental delay. Acta Radiol 49:589–595PubMedCrossRefGoogle Scholar
  39. 39.
    Jea A, Vachhrajani S, Widjaja E et al (2008) Corpus callosotomy in children and the disconnection syndromes: a review. Childs Nerv Syst 24:685–692PubMedCrossRefGoogle Scholar
  40. 40.
    De Lacoste C, Kirkpatrick JB, Ross ED (1985) Topography of the human corpus callosum. J Neuropathol Exp Neurol 44:578–591PubMedCrossRefGoogle Scholar
  41. 41.
    Oh JS, Park KS, Song IC et al (2005) Fractional anisotropy-based divisions of midsagittal corpus callosum. NeuroReport 16:317–320PubMedCrossRefGoogle Scholar
  42. 42.
    Déjerine J. Anatomie des Centres Nerveux, vol 2, Rueff, Paris 1901. Masson, Paris 1980, pp 263-267 (reprint)Google Scholar
  43. 43.
    Liss L, Mervis L (1964) The ependymal lining of the cavum septi pellucidi: a histological and histochemical study. J Neuropathol Exp Neurol 23:355–367PubMedCrossRefGoogle Scholar
  44. 44.
    Lancon JA, Haines DE, Lewis AI, Parent AD (1999) Endoscopic treatment of symptomatic septum pellucidum cysts: with some preliminary observations on the ultrastructure of the cyst wall: two technical reports. Neurosurgery 45:1251–1257PubMedCrossRefGoogle Scholar
  45. 45.
    Ronsin E, Grosskopf D, Perre J (1997) Morphology and immunohistochemistry of a symptomatic septum pellucidum cavum Vergae cyst in man. Acta Neurochir 139:366–372CrossRefGoogle Scholar
  46. 46.
    Shu T, Shen WB, Richards LJ (2001) Development of the perforating pathway: an ipsilaterally projecting pathway between the medial septum/diagonal band of Broca and the cingulate cortex that intersects the corpus callosum. J Comp Neurol 436:411–422PubMedCrossRefGoogle Scholar
  47. 47.
    Yakovlev PI, Locke S (1961) nuclei of thalamus and connections of limbic cortex. III. Cortico-cortical connections of the anterior cingulate gyrus, the cingulum, and the subcallosal bundle in the monkey. Arch Neurol 5:364–400PubMedGoogle Scholar
  48. 48.
    Johnston TB (1934) A note on the peduncle of the flocculus and the posterior medullary velum. J Anat 68:471–479PubMedGoogle Scholar
  49. 49.
    Raybaud C, Girard N. Etude anatomique par IRM des agénésies and dysplasies commissurales télencéphaliques. Corrélations cliniques et interprétation morphogénétique. Neurochirurgie (Paris) 1998, 44(Suppl 1):38-60Google Scholar
  50. 50.
    Larroche JC, Baudey J (1961) septi pellucidi, cavum Vergae, cavum veli interpositi: cavités de la ligne médiane. Etude anatomique et pneumoencéphalographique dans la période néonatale. Biol Neonate 3:193–236CrossRefGoogle Scholar
  51. 51.
    Shaw CM, Alvord EC (1969) Cava septi pellucidi et Vergae: their normal and pathological states. Brain 92:213–224PubMedCrossRefGoogle Scholar
  52. 52.
    Scoffings DJ, Kurian KM (2008) Congenital and acquired lesions of the septum pellucidum. Clin Radiol 63:210–219PubMedCrossRefGoogle Scholar
  53. 53.
    Auer RN, Gilbert JJ (1982) Cavum Vergae without cavum septi pellucidi. Arch Pathol Lab Med 106:462–463PubMedGoogle Scholar
  54. 54.
    Blakemore WF, Jolly RD (1972) The subependymal plate and associated ependyma in the dog. An ultrastructural study J Neurocytol 1:69–84Google Scholar
  55. 55.
    Hopewell JW (1975) The subependymal plate and the genesis of gliomas. J Pathol 117:101–103PubMedCrossRefGoogle Scholar
  56. 56.
    Nishio S, Fujiwara S, Tashima T et al (1990) Tumors of the lateral ventricular wall, especially the septum pellucidum: clinical presentation and variations in pathological features. Neurosurgery 27:224–230PubMedCrossRefGoogle Scholar
  57. 57.
    Aldur MM, Çelik HH, Sargon MF et al (1997) Unreported anatomical variation of septum pellucidum. Clin Anat 10:245–249PubMedCrossRefGoogle Scholar
  58. 58.
    Bayer SA (2006) Altman J. Atlas of central nervous system development. The human brain during the late first trimester. CRC, Boca RatonGoogle Scholar
  59. 59.
    Bayer SA (2005) Altman J. Atlas of Central Nervous System Development. The human brain during the second trimester. CRC, Boca RatonGoogle Scholar
  60. 60.
    Shen WB, Plachez C, Mongi AS, Richards LJ (2006) Identification of candidate genes at the corticoseptal boundary during development. Gene Expres Patterns 6:471–481CrossRefGoogle Scholar
  61. 61.
    Silver J, Ogawa MY (1983) Postnatally induced formation of the corpus callosum in acallosal mice on glia-coated cellulose bridges. Science 220:1067–1069PubMedCrossRefGoogle Scholar
  62. 62.
    Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123–1133PubMedCrossRefGoogle Scholar
  63. 63.
    Lanier LM, Gates MA, Witke W et al (1999) Mena is required for neurulation and commissure formation. Neuron 22:313–325PubMedCrossRefGoogle Scholar
  64. 64.
    Shu T (2003) Butz KG. Plachez et al Abnormal development of forebrain midline glia and commissural projections in Nfia knock-out mice J Neurosci 23:203–212Google Scholar
  65. 65.
    Jovanov-Milošević N, Čuljat M, Kostović I (2009) Growth of the human corpus callosum: modular and laminar morphogenetic zones. Frontiers Neuroanat 3:1–10Google Scholar
  66. 66.
    Pascual M, Pozas E, Barallobre J et al (2004) Coordinated functions of netrin-1 and class 3 secreted semaphorins in the guidance of reciprocal septohippocampal connections. Mol Cell Neurosci 26:24–33PubMedCrossRefGoogle Scholar
  67. 67.
    Flanagan JG, van Vactor D (1998) Through the looking glass: axon guidance at the midline choice point. Cell 92:429–432PubMedCrossRefGoogle Scholar
  68. 68.
    Kaprielian Z, Imondi R, Runko E (2000) Axon guidance at the midline of the developing CNS. Anat Rec (New Anat) 261:176–197CrossRefGoogle Scholar
  69. 69.
    Probst M. Über den Bau des vollständigen balkenlosen Groβhirns sowie über Microgyrie und Heterotopie den Grauen Substanz. Arch Psychiat Nervenkr 1901, 34:709-786 (quoted by [70])Google Scholar
  70. 70.
    Probst FP (1973) Congenital defects of the corpus callosum. Acta Radiol Suppl 331:1–152PubMedGoogle Scholar
  71. 71.
    Onufrowicz W. Das balkenlose Microcephalengehirn. Arch J Psychiat 1887, 18:305-328 (quoted by [47])Google Scholar
  72. 72.
    Sachs H. Das Hemisphärenmark des Menschlichen Grosshirns. I. der Hinterhauptlappen. Leipzig, 1892 (quoted by [2])Google Scholar
  73. 73.
    Nakata Y, Barkovich AJ, Wahl M et al (2009) Diffusion abnormalities and reduced volume of the ventral cingulum bundle in agenesis of the corpus callosum: a 3T imaging study. AJNR Am J Neuroradiol 30:1142–1148PubMedCrossRefGoogle Scholar
  74. 74.
    Mufson EJ, Pandya DN (1984) Some observations on the course and composition of the cingulum bundle in the rhesus monkey. J Comp Neurol 225:31–43PubMedCrossRefGoogle Scholar
  75. 75.
    Dávila-Gutiérrez G (2002) Agenesis and dysgenesis of the corpus callosum. Sem Ped Neurol 9:292–301CrossRefGoogle Scholar
  76. 76.
    Barkovich AJ, Simon EM, Walsh CA (2001) Callosal agenesis with cyst. A better understanding and new classification. Neurology 56:220–227PubMedGoogle Scholar
  77. 77.
    Pavone P, Barone R, Baieli S et al (2005) Callosal anomalies with interhemispheric cysts: expanding the phenotype. Acta Paediat 94:1066–1072PubMedCrossRefGoogle Scholar
  78. 78.
    Sener RN (1993) Septo-optic dysplasia associated with total absence of the corpus callosum: MR and CT features. Eur Radiol 3:551–553Google Scholar
  79. 79.
    De León GA, Radkowski MA, Gutierrez FA (1995) Single forebrain ventricle without prosencephaly: agenesis of the corpus callosum with dehiscent fornices. Acta Neuropathol 89:454–458PubMedCrossRefGoogle Scholar
  80. 80.
    Aicardi J (1996) Aicardi syndrome. In: Guerrini R et al (eds) Dysplasias of cerebral cortex and epilepsy. Lippincott-Raven, Philadelphia, pp 211–216Google Scholar
  81. 81.
    Truwit CL, Barkovich AJ (1990) Pathogenesis of intracranial lipomas: an MR study in 42 patients. AJNR Am J Neuroradiol 11:665–674Google Scholar
  82. 82.
    Osaka K, Handa H, Matsumoto S, Yasuda M (1980) Development of the cerebrospinal fluid pathway in the normal and abnormal human embryo. Child’s Brain 6:26–38PubMedGoogle Scholar
  83. 83.
    McLone DG (1980) The subarachnoid space: a review. Child’s Brain 6:113–130PubMedGoogle Scholar
  84. 84.
    Tart RP, Quisling RG (1991) Curvilinear and tubulonodular varieties of lipoma of the corpus callosum: an MR and CT study. J Comput Assist Tomogr 15:805–810PubMedCrossRefGoogle Scholar
  85. 85.
    Demaerel P, Van de Gaer P, Wilms G, Baert AL (1996) Interhemispheric lipoma with variable callosal dysgenesis: relationship between embryology, morphology and symptomatology. Eur Radiol 6:904–909PubMedGoogle Scholar
  86. 86.
    De Morsier G (1956) Etudes sur les dysraphies crânio-encéphaliques. III Agénésie du septum lucidum avec malformation du tractus optique La dysplasie septo-optique Schweiz Arch Neurol Psychiat 77:267–292Google Scholar
  87. 87.
    Fernandes M, Hébert JM (2008) The ups and downs of holoprosencephaly: dorsal versus ventral patterning forces. Clin Genet 73:413–23PubMedCrossRefGoogle Scholar
  88. 88.
    Kelberman D, Dattani MT (2008) Septo-optic dysplasia—novel insights into the aetiology. Horm Res 69:257–265PubMedCrossRefGoogle Scholar
  89. 89.
    Schachter KA, Krauss RS (2008) Murine models of holoprosencephaly. Curr Top Develop Biol 84:139–170CrossRefGoogle Scholar
  90. 90.
    Hoyt WF, Kaplan SL, Grumbach MM, Glaser JS. Septo-optic dysplasia and pituitary dwarfism. Lancet 1970, 1:893-894 (letter)Google Scholar
  91. 91.
    Acers TE (1981) Optic nerve hypoplasia: septo-optic-pituitary dysplasia syndrome. Tr Am Ophth Soc 79:425–457PubMedGoogle Scholar
  92. 92.
    Barkovich AJ, Fram EK, Norman D (1989) Septo-optic dysplasia: MR imaging. Radiology 171:189–192PubMedGoogle Scholar
  93. 93.
    Williams J, Brodsky MC, Griebel M et al (1993) Septo-optic dysplasia: the clinical insignificance of an absent septum pellucidum. Dev Med Child Neurol 35:490–501PubMedCrossRefGoogle Scholar
  94. 94.
    Belhocine O, André C, Khalifa G, Adamsbaum C (2005) Does asymptomatic septal agenesis exist? A review of 34 cases. Pediatr Radiol 35:410–418PubMedCrossRefGoogle Scholar
  95. 95.
    Supprian T, Sian J, Heils A et al (1999) Isolated absence of the septum pellucidum. Neuroradiology 41:563–566PubMedCrossRefGoogle Scholar
  96. 96.
    Raybaud C, Girard N, Levrier O et al (2001) Schizencephaly: correlation between the lobar topography of the cleft(s) and absence of the septum pellucidum. Childs Nerv Syst 17:217–222PubMedCrossRefGoogle Scholar
  97. 97.
    Bodensteiner JB (1995) The saga of the septum pellucidum: a tale of unfunded clinical investigations. J Child Neurol 10:227–231PubMedCrossRefGoogle Scholar
  98. 98.
    Bodensteiner JB, Schaefer GB, Craft JM (1998) Cavum septi pellucidi and cavum Vergae in normal and developmentally delayed populations. J Child Neurol 13:120–121PubMedCrossRefGoogle Scholar
  99. 99.
    Miller E, Widjaja E, Blaser S et al (2008) The old and the new: supratentorial MR findings in Chiari II malformation. Childs Nerv Syst 24:563–575PubMedCrossRefGoogle Scholar
  100. 100.
    Vachha B, Adams RC, Rollins NK (2006) Limbic tract anomalies in pediatric myelomeningocele and Chiari II malformation: anatomic correlation with memory and learning—initial investigation. Radiology 240:194–202PubMedCrossRefGoogle Scholar
  101. 101.
    Raybaud C (1982) Cystic malformations of the posterior fossa—abnormalities associated with development of the roof of the fourth ventricle and adjacent meningeal structures. J Neuroradiol 9:103–133PubMedGoogle Scholar
  102. 102.
    Michaud J, Mizrahi EM, Urich H (1982) Agenesis of the vermis with fusion of the cerebellar hemispheres, septo-optic dysplasia and associated anomalies. Report of a case Acta Neuropathol (Berl) 56:161–166CrossRefGoogle Scholar
  103. 103.
    Jellinger KA (2002) Rhombencephalosynapsis. Acta Neuropathol 103:305–6PubMedCrossRefGoogle Scholar
  104. 104.
    Guion-Almeida ML, Richieri-Costa A, Saavedra D, Cohen MM Jr (1996) Frontonasal dysplasia: analysis of 21 cases and literature review. Int J Oral Maxillofac Surg 25:91–97PubMedCrossRefGoogle Scholar
  105. 105.
    Wu E, Vargevik K, Slavotinek AM (2007) Subtypes of frontonasal dysplasia are useful in determining clinical prognosis. Am J Clin Genet Part A 143A:3069–3078CrossRefGoogle Scholar
  106. 106.
    Koenig SB, Naidich TP, Lissner G (1982) The morning glory syndrome associated with sphenoidal cephalocele. Ophtalmology 89:1368–1373Google Scholar
  107. 107.
    Vermeulen RJ, Wilke M, Horber V, Krägeloh-Mann I (2010) Microcephaly with simplified gyral pattern. MRI classification Neurology 74:386–391Google Scholar
  108. 108.
    Kappeler C, Dhenain M (2007) Phan Dinh Tuy F et al. Magnetic resonance imaging and histological studies of corpus callosum and hippocampal abnormalities linked to doublecortin deficiency J Comp Neurol 500:239–254Google Scholar
  109. 109.
    Kitamura K, Yanazawa M, Sugiyama N et al (2002) Mutation in ARX causes abnormal development of brain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans. Nat Genet 32:359–369PubMedCrossRefGoogle Scholar
  110. 110.
    Miyata H, Chute DJ, Fink J et al (2004) Lissencephaly with agenesis of corpus callosum and rudimentary dysplastic cerebellum: a subtype of lissencephaly with cerebellar hypoplasia. Acta Neuropathol 107:69–81PubMedCrossRefGoogle Scholar
  111. 111.
    Sato N, Ota M, Yagishita A et al (2008) Aberrant midsagittal fiber tracts in patients with hemimegalencephaly. AJNR Am J Neuroradiol 29:823–827PubMedCrossRefGoogle Scholar
  112. 112.
    Robin NH, Taylor CJ, McDonald-McGinn et al. Polymicrogyria and deletion 22q11.2 syndrome: window to the etiology of a common cortical malformation. Am J Med Genet Part A 2006, 140A:2416-2425Google Scholar
  113. 113.
    Barkovich AJ, Kuzniecky RI, Jackson GD et al (2005) A developmental and genetic classification for malformations of cortical development. Neurology 65:1873–1887PubMedCrossRefGoogle Scholar
  114. 114.
    Pierson TM, Zimmerman RA, Tennekoon GI, Bönnemann CG (2008) Mega-corpus callosum, polymicrogyria, and psychomotor retardation: confirmation of a syndromic entity. Neuropediatrics 39:123–127PubMedCrossRefGoogle Scholar
  115. 115.
    Online Mendelian Inheritance in Man, OMIM (TM). McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University (Baltimore, MD) and National Center for Biotechnology Information, National Library of Medicine (Bethesda, MD), World Wide Web URL: http://www.ncbi.nlm.nih.gov/omim/
  116. 116.
    Schmid RS, Maness PF (2008) L1 and NCAM adhesion molecules as signaling co-receptors in neuronal migration and process outgrowth. Curr Opin Neurobiol 18:245–250PubMedCrossRefGoogle Scholar
  117. 117.
    Fransen E, Van Camp G, Vits L, Willems PJ (1997) L1-associated diseases: clinical geneticists divide, molecular geneticists unite. Hum Mol Genet 6:1625–1632PubMedCrossRefGoogle Scholar
  118. 118.
    Yamasaki M, Thompson P, Lemmon V (1997) CRASH syndrome: mutations in L1CAM correlate with severity of the disease. Neuropediatrics 28:175–178PubMedCrossRefGoogle Scholar
  119. 119.
    Weller S, Gärtner J (2001) Genetic and clinical aspects of X-linked hydrocephalus (L1 disease): mutations in the L1CAM gene. Hum Mutat 18:1–12PubMedCrossRefGoogle Scholar
  120. 120.
    Reed UC (2009) Congenital muscular dystrophy. Part II: a review of pathogenesis and therapeutic perspectives. Arq Neuropsiquiatr 67:343–362PubMedGoogle Scholar
  121. 121.
    Raybaud C, Di Rocco C (2007) Brain malformation in syndromic craniosynostoses, a primary disorder of white matter: a review. Childs Nerv Syst 23:1379–1388PubMedCrossRefGoogle Scholar
  122. 122.
    Doherty P, Wlash F (1996) CAM-FGF receptor interaction: a model for axonal growth. Mol Cell Neurosci 8:99–111CrossRefGoogle Scholar
  123. 123.
    Kamiguchi H, Lemmon V (1997) Neural cell adhesion molecule L1: signaling pathways and growth cone motility. J Neurosc Res 49:1–8CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Division of Neuroradiology, Hospital for Sick ChildrenTorontoCanada
  2. 2.Division of RadiologyUniversity of TorontoTorontoCanada

Personalised recommendations