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Disturbances of Late Neuronal Migrations in the Perinatal Period

Disturbances of Late Neuronal Migrations in the Perinatal Period Abstract Abnormal neuronal migrations in the developing human brain are generally thought of in the context of early gestational events induced by genetic factors, teratogens, or infections. Although the major neuronal migrations that form the cortical plate occur by the 16th week of gestation, late migrations from the germinal matrix into the cerebral cortex continue until five months postnatally. The external granular layer of the cerebellar cortex continues to migrate until 1 year of age. Ample opportunity thus exists for disturbances of these migratory processes in the postnatal period. Focal zones of imperfect cortical lamination, small hamartomas, and microscopic subcortical heterotopia are often encountered during postmortem examination of infant brains. These focal structural anomalies are usually dismissed as "incidental findings." In survivors, however, such "minor" lesions perhaps contribute to the later seizure disorders, developmental delays, learning disabilities, perceptual disorders, and motor incoordination that are so common following premature birth or neonatal References 1. Herrick CJ: The Brain of the Tiger Salamander . Toronto, University of Toronto Press, 1948. 2. Sarnat HB, Netsky MG: Evolution of the Nervous System , ed 2. New York, Oxford University Press Inc, 1981. 3. Chi JG, Dooling EC, Gilles FH: Gyral development of the human brain . Ann Neurol 1977;1: 86-93.Crossref 4. Barth PG: Disorders of neuronal migration . Can J Neurol Sci 1987;14:1-16. 5. Rakić P: Mode of cell migration to the superficial layers of fetal monkey neocortex . J Comp Neurol 1972;145:61-84.Crossref 6. Poliakov GI: Some results of research into the development of the neuronal structure of the cortical ends of analyzers in man . J Comp Neurol 1961;117:197-212.Crossref 7. Sidman SL, Rakić P: Neuronal migration, with special reference to developing human brain: A review . Brain Res 1973;62:1-35.Crossref 8. Marin-Padilla M: Prenatal and early postnatal ontogenesis of the human motor cortex: A Golgi study: I. The sequential development of the cortical layers . Brain Res 1970;23:167-183.Crossref 9. Golgi C: Sulla fina anatomia delgi organi centrali del sistema nervoso, 1885 , republished in: Opera Omni . Milan, U Hoepli, 1903, pp 397-536. 10. Von Lenhossék M: Zur Kenntnis der Neuroglia des menschlichen Rueckenmarkes . Verh Anat Ges 1891;5:193-221. 11. Retzius G: Die Neuroglia des Gehirns beim Meuschen und bei Saugethieren . Biol Untersuchungen 1894;6:1-24. 12. Ramón y Cajal S de: Histologie du systéme nerveux central de l'homme et des vertébrés . Paris, Maloine Editeurs, 1909-1911. 13. Sarnat HB, Campa JF, Lloyd JM: Inverse prominence of ependyma and capillaries in the spinal cord of vertebrates: A comparative histochemical study . Am J Anat 1975;143:439-450.Crossref 14. Hajós F, Bascó E: The surface-contact glia . Adv Anat Embryol Cell Biol 1984;84:1-81. 15. Rakić P: Guidance of neurons migrating to the fetal monkey neocortex . Brain Res 1971;33:471-476.Crossref 16. Choi BH, Kim RC, Lapham LW: Do radial glia give rise to both astroglial and oligodendroglial cells? Dev Brain Res 1983;8:119-130.Crossref 17. Antanitus DS, Choi BH, Lapham LW: The demonstration of glial fibrillary acidic protein in the cerebrum of the human fetus by indirect immunofluorescence . Brain Res 1976;103: 613-616.Crossref 18. Choi BH, Lapham LW: Radial glia in the human fetal cerebrum: A combined Golgi, immunofluorescent and electron microscopic study . Brain Res 1978;148:295-311.Crossref 19. Roessmann U, Velasco ME, Sindely SD, et al: Glial fibrillary acidic protein (GFAP) in ependymal cells during development: An immunocytochemical study . Brain Res 1980;200:13-21.Crossref 20. Choi BH: Glial fibrillary acidic protein in radial glia of early human fetal cerebrum: A light and electron microscopic immunoperoxidase study . J Neuropathol Exp Neurol 1986;45:408-418.Crossref 21. Cochard P, Paulin D: Initial expression of neurofilaments and vimentin in the central and periphyeral nervous system of the mouse embryo in vivo . J Neurosci 1984;4:2080-2094. 22. Roessmann U, Gambetti P: Astrocytes in the developing human brain: An immunohistochemical study . Acta Neuropathol 1986;70: 308-313.Crossref 23. Borit A, McIntosh GC: Myelin basic protein and glial fibrillary acid protein in human fetal brain . Neuropathol Appl Neurobiol 1981;7: 279-287.Crossref 24. Takashima S, Becker LE: Developmental changes of glial fibrillary acidic protein in cerebral white matter . Arch Neurol 1983;40:14-18.Crossref 25. Card JP, Rafols JA: Tanycytes of the third ventricle of the neonatal rat: A Golgi study . Am J Anat 1978;151:173-190.Crossref 26. Bleier R: The relations of ependyma to neurons and capillaries in the hypothalamus: A Golgi-Cox study . J Comp Neurol 1971;142: 439-464.Crossref 27. Angevine JB, Sidman RL: Autoradiographic study of cell migration during histogenesis of the cerebral cortex in the mouse . Nature 1961;192:766-768.Crossref 28. Berry M, Rogers AW: The migration of neuroblasts in the developing cerebral cortex . J Anat 1965;99:691-709. 29. Larroche J-C: Quelques aspects anatomiques du développement cérébral . Biol Neonate 1962;4:126-153.Crossref 30. Friede RL: Developmental Neuropathology . New York, Springer-Verlag NY Inc, 1975. 31. Kater S, Letourneau P (eds): Biology of the Growth Cone . New York, Alan R Liss Inc, 1985. 32. Morest D: A study of neurogenesis in the forebrain of opossum pouch young . Z Anat Entwicklungsgesch 1970;130:265-305.Crossref 33. Molliver ME, Kostović I, Van der Loos H: The development of synapses in cerebral cortex of the human fetus . Brain Res 1973;50:403-407.Crossref 34. Hinds JW, Hinds PL: Synapse formation in the mouse olfactory bulb: I. Quantitative studies . J Comp Neurol 1976;169:15-40.Crossref 35. Rorke LB, Riggs HE: Myelination of the Brain in the Newborn . New York, JB Lippincott, 1969. 36. Woodard JS: Origin of the external granule layer of the cerebellar cortex . J Comp Neurol 1960;115:65-73.Crossref 37. Rakić P, Sidman RL: Histogenesis of cortical layers in human cerebellum, particularly the lamina dissecans . J Comp Neurol 1970;139: 473-500.Crossref 38. Mugnaini E, Forströnen PF: Ultrastructural studies on the cerebellar histogenesis: I. Differentiation of granule cells and development of glomeruli in the chick embryo . Z Mikrosk Anat Forsch 1967;77:115-143.Crossref 39. Rakić P: Neuron-glia relationship during granule cell migration in developing cerebellar cortex: A Golgi and electron microscopic study in Macacus rhesus . J Comp Neurol 1971;141:283-312.Crossref 40. Hausmann B, Sievers J: Cerebellar external granule cells are attached to the basal lamina from the onset of migration up to the end of their proliferative activity . J Comp Neurol 1985;241: 50-62.Crossref 41. Trenkner E, Smith D, Segil N: Is cerebellar granule cell migration regulated by an internal clock? J Neurosci 1984;11:2850-2855. 42. Zećević N, Rakić P: Differentiation of Purkinje cells and their relationship to other components of developing cerebellar cortex in man . J Comp Neurol 1976;167:27-47.Crossref 43. Altman J: Postnatal development of the cerebellar cortex in the rat: I. The external germinal layer and transitional molecular layer . J Comp Neurol 1972;145:353-397.Crossref 44. Altman J: Postnatal development of the cerebellar cortex in the rat: III. Maturation of the components of the granular layer . J Comp Neurol 1972;145:465-513.Crossref 45. West MJ, Del Cerro M: Early formation of synapses in the molecular layer of the fetal rat cerebellum . J Comp Neurol 1975;165:137-160.Crossref 46. Shimada M, Langman J: Repair of the external granular layer of the hamster cerebellum after prenatal and postnatal administration of methylazoxymethanol . Teratology 1970; 3:119-134.Crossref 47. Margolis G, Kilham L, Johnson RH: The parvoviruses and replicating cells: Insights into the pathogenesis of cerebellar hypoplasia . Prog Neuropathol 1971;1:168-201. 48. Altman J, Anderson WJ: Experimental reorganization of the cerebellar cortex: I. Morphological effects of elimination of all microneurons with prolonged x-irradiation started at birth . J Comp Neurol 1972;146:355-406.Crossref 49. Jones MZ, Gardner E: Pathogenesis of methylazoxymethanol-induced lesions in the postnatal mouse cerebellum . J Neuropathol Exp Neurol 1976;35:413-444.Crossref 50. Yakovlev PI, Lecours A-R: The myelination cycles of regional maturation of the brain , in Minkowski A (ed): Regional Development of the Brain in Early Life . Philadelphia, FA Davis Co Publishers, 1967, pp 3-70. 51. Roessmann U, Gambetti P: Pathological reaction of astrocytes in perinatal brain injury: Immunohistochemical study . Acta Neuropathol 1986;70:302-307.Crossref 52. Choi BH, Lapham LW, Amin Zaki L, et al: Abnormal neuronal migration, deranged cerebral cortical organization, and diffuse white matter astrocytosis of human fetal brain: A major effect of methylmercury poisoning in utero . J Neuropathol Exp Neurol 1978;37:719-733.Crossref 53. Marsh DO, Myers GY, Clarkson Th W, et al: Fetal methylmercury poisoning: Clinical and toxicological data on 29 cases . Ann Neurol 1980;7:348-353.Crossref 54. Choi BH, Cho KH, Lapham LW: Effects of methylmercury on DNA synthesis of human fetal astrocytes: A radioautographic study . Brain Res 1980;202:238-242. 55. Choi BH, Cho KH, Lapham LW: Effects of methylmercury on human fetal neurons and astrocytes in vitro: A time-lapse cinematographic, phase, and electron microscopic study . Environ Res 1981;24:61-74.Crossref 56. Choi BH: Mercury and abnormal development of the fetal brain , in Dreosti I, Smith R (eds): Neurobiology of Trace Elements . Clifton, NJ, Humana Press, 1983, vol 1, pp 197-235. 57. Norman MG, O'Kusky JR: The growth and development of microvasculature in human cerebral cortex . J Neuropathol Exp Neurol 1986; 45:222-232. 58. Norman MG: On the morphogenesis of ulegyria . Acta Neuropathol 1981;53:331-332.Crossref 59. Larroche J-C: Fetal encephalopathies of circulatory origin . Biol Neonate 1986;50:61-74.Crossref 60. Norman MG: Bilateral encephaloclastic lesions in a 26-week gestation fetus: Effect on neuronal migration . Can J Neurol Sci 1980;7: 191-194. 61. Levine DN, Fisher MA, Caviness VS Jr: Porencephaly with micropolygyria: A pathologic study . Acta Neuropathol 1974;29:99-113.Crossref 62. Richman DP, Steward RM, Caviness VS Jr: Cerebral microgyria in a 27-week fetus: An architectonic and topographic analysis . J Neuropathol Exp Neurol 1974;33:374-384.Crossref 63. Williams RS, Ferrante RJ, Caviness VS Jr: The cellular pathology of microgyria: A Golgi analysis . Acta Neuropathol 1976;36:269-283.Crossref 64. Dekaban A: Large defects in cerebral hemispheres associated with cortical dysgenesis . J Neuropathol Exp Neurol 1965;24:512-530.Crossref 65. Friede RL, Mikolasek J: Postencephalitic porencephaly, hydranencephaly, or polymicrogyria: A review . Acta Neuropathol 1978;43:161-168.Crossref 66. Ferrer I, Navarro C: Multicystic encephalomalacia of infancy: Clinico-pathological report of seven cases . J Neurol Sci 1978;38:179-189.Crossref 67. Ferrer I: A Golgi analysis of unlayered polymicrogyria . Acta Neuropathol 1984;65: 69-76.Crossref 68. McBride MC, Kemper TL: Pathogenesis of four-layered microgyric cortex in man . Acta Neuropathol 1982;57:93-98.Crossref 69. Dvorak K, Feit J, Jurankova Z: Experimentally induced focal microgyria and status verrucosus deformis in rats—pathogenesis and interrelation: Histological and autoradiographical study . Acta Neuropathol 1978; 44:121-129.Crossref 70. Brun A: Marginal glioneuronal heterotopias of the central nervous system . Acta Pathol Microbiol Immunol Scand A 1975;65:221-233. 71. Caviness VS, Evrard PH Jr, Lyon G: Radial neuronal assemblies, ectopies, and necrosis of developing cortex: A case analysis . Acta Neuropathol 1978;41:67-72.Crossref 72. Robain O, Deonna T: Pachygyria and congenital nephrosis: Disorder of migration and neuronal orientation . Acta Neuropathol 1983;60: 137-141.Crossref 73. Dambska M, Wisniewski KE, Sher JH: Marginal glioneuronal heterotopias in nine cases with and without cortical abnormalities . J Child Neurol 1986;1:149-157.Crossref 74. Duckett S, Pearse AGE: The cells of CajalRetzius in the developing human brain . J Anat 1968;102:183-187. 75. Noback CR, Purpura DP: Postnatal ontogenesis of neurons in cat neocortex . J Comp Neurol 1961;117:291-308.Crossref 76. Brun A: The subpial granular layer of the foetal cerebral cortex in man: Its ontogeny and significance in cortical malformations . Acta Pathol Microbiol Immunol Scand Suppl 1965; 179:1-98. 77. Sarnat HB: Granular cell glioblastoma . J Neuropathol Exp Neurol 1976;46:112-113.Crossref 78. Ronnevi L-O, Conradi S: Ultrastructural evidence for spontaneous elimination of synaptic terminals on spinal motoneurons in the kitten . Brain Res 1974;80:335-359.Crossref 79. Inagaki S, Sakanaka S, Shiosaka S, et al: Experimental and immunohistochemical studies on the cerebellar substance P of the rat: Localization, postnatal ontogeny, and ways of entry into the cerebellum . Neuroscience 1982;7:639-646.Crossref 80. Inagaki S, Shiosaka S, Takatsuki K, et al: Ontogeny of somatostatin-containing neuron system of the rat cerebellum including its fiber connections: An experimental and immunohistochemical analysis . Dev Brain Res 1982;3:509-529.Crossref 81. Schulman JA: Chemical neuroanatomy of the cerebellar cortex , in Emson PC (ed): Chemical Neuroanatomy . New York, Raven Press, 1983, pp 209-228. 82. Johnston MV, Silverstein FS, Reindel FO, et al: Muscarinic cholinergic receptors in human infant forebrain: [3H] Quinuclidinyl benzilate binding in homogenates and quantitative autoradiography in sections . Dev Brain Res 1985; 19:195-203.Crossref 83. Sarnat HB: L'acridine-orange: un fluorochrome des acides nucléiques pour l'étude des cellules musculaires et nerveuses . Rev Neurol 1985;141:120-127. 84. Sarnat HB, Curry B, Rewcastle NB, et al: Gliosis and glioma distinguished by acridine orange . Can J Neurol Sci 1987;14:31-35. 85. Sarnat HB, Seagram CGF, Trevenen CL, et al: A fluorochromic stain for nucleic acids to demonstrate submucosal and myenteric neurons in Hirschsprung's disease . Am J Clin Pathol 1985;83:722-725. 86. Sarnat HB: Répartition d'A.R.N. neuronal au cours de la migration dans les cerveaux normaux et dysplastiques chez le foetus humain. Rev Neurol, in press. 87. Fabian JE, Sarnat HB: Acridine orange fluorochrome study of RNA distribution in the brain of two newt species. Trans Am Microscopical Soc, in press. 88. Sarnat NB, Sarnat HB; Répartition tissulaire de l'acide ribonucléique chez la planaire Dugesia tigrina: Une étude fluorochromique à l'acridine-orange. Can J Zool, in press. 89. Sarnat HB: Hypoxic alterations in neonatal neurons: An acridine orange fluorochromic study of nucleic acids . Brain Dev 1986;9:43-47.Crossref 90. Galloway PG, Roessmann U: Neuronal Karyorrhexis in Sommer's sector in a 22-week stillborn . Acta Neuropathol 1986;70:343-344.Crossref http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png American Journal of Diseases of Children American Medical Association

Disturbances of Late Neuronal Migrations in the Perinatal Period

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American Medical Association
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Copyright © 1987 American Medical Association. All Rights Reserved.
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0002-922X
DOI
10.1001/archpedi.1987.04460090046022
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Abstract

Abstract Abnormal neuronal migrations in the developing human brain are generally thought of in the context of early gestational events induced by genetic factors, teratogens, or infections. Although the major neuronal migrations that form the cortical plate occur by the 16th week of gestation, late migrations from the germinal matrix into the cerebral cortex continue until five months postnatally. The external granular layer of the cerebellar cortex continues to migrate until 1 year of age. Ample opportunity thus exists for disturbances of these migratory processes in the postnatal period. Focal zones of imperfect cortical lamination, small hamartomas, and microscopic subcortical heterotopia are often encountered during postmortem examination of infant brains. These focal structural anomalies are usually dismissed as "incidental findings." In survivors, however, such "minor" lesions perhaps contribute to the later seizure disorders, developmental delays, learning disabilities, perceptual disorders, and motor incoordination that are so common following premature birth or neonatal References 1. Herrick CJ: The Brain of the Tiger Salamander . Toronto, University of Toronto Press, 1948. 2. Sarnat HB, Netsky MG: Evolution of the Nervous System , ed 2. New York, Oxford University Press Inc, 1981. 3. Chi JG, Dooling EC, Gilles FH: Gyral development of the human brain . Ann Neurol 1977;1: 86-93.Crossref 4. Barth PG: Disorders of neuronal migration . Can J Neurol Sci 1987;14:1-16. 5. Rakić P: Mode of cell migration to the superficial layers of fetal monkey neocortex . J Comp Neurol 1972;145:61-84.Crossref 6. Poliakov GI: Some results of research into the development of the neuronal structure of the cortical ends of analyzers in man . J Comp Neurol 1961;117:197-212.Crossref 7. Sidman SL, Rakić P: Neuronal migration, with special reference to developing human brain: A review . Brain Res 1973;62:1-35.Crossref 8. Marin-Padilla M: Prenatal and early postnatal ontogenesis of the human motor cortex: A Golgi study: I. The sequential development of the cortical layers . Brain Res 1970;23:167-183.Crossref 9. Golgi C: Sulla fina anatomia delgi organi centrali del sistema nervoso, 1885 , republished in: Opera Omni . Milan, U Hoepli, 1903, pp 397-536. 10. Von Lenhossék M: Zur Kenntnis der Neuroglia des menschlichen Rueckenmarkes . Verh Anat Ges 1891;5:193-221. 11. Retzius G: Die Neuroglia des Gehirns beim Meuschen und bei Saugethieren . Biol Untersuchungen 1894;6:1-24. 12. Ramón y Cajal S de: Histologie du systéme nerveux central de l'homme et des vertébrés . Paris, Maloine Editeurs, 1909-1911. 13. Sarnat HB, Campa JF, Lloyd JM: Inverse prominence of ependyma and capillaries in the spinal cord of vertebrates: A comparative histochemical study . Am J Anat 1975;143:439-450.Crossref 14. Hajós F, Bascó E: The surface-contact glia . Adv Anat Embryol Cell Biol 1984;84:1-81. 15. Rakić P: Guidance of neurons migrating to the fetal monkey neocortex . Brain Res 1971;33:471-476.Crossref 16. Choi BH, Kim RC, Lapham LW: Do radial glia give rise to both astroglial and oligodendroglial cells? Dev Brain Res 1983;8:119-130.Crossref 17. Antanitus DS, Choi BH, Lapham LW: The demonstration of glial fibrillary acidic protein in the cerebrum of the human fetus by indirect immunofluorescence . Brain Res 1976;103: 613-616.Crossref 18. Choi BH, Lapham LW: Radial glia in the human fetal cerebrum: A combined Golgi, immunofluorescent and electron microscopic study . Brain Res 1978;148:295-311.Crossref 19. Roessmann U, Velasco ME, Sindely SD, et al: Glial fibrillary acidic protein (GFAP) in ependymal cells during development: An immunocytochemical study . Brain Res 1980;200:13-21.Crossref 20. Choi BH: Glial fibrillary acidic protein in radial glia of early human fetal cerebrum: A light and electron microscopic immunoperoxidase study . J Neuropathol Exp Neurol 1986;45:408-418.Crossref 21. Cochard P, Paulin D: Initial expression of neurofilaments and vimentin in the central and periphyeral nervous system of the mouse embryo in vivo . J Neurosci 1984;4:2080-2094. 22. Roessmann U, Gambetti P: Astrocytes in the developing human brain: An immunohistochemical study . Acta Neuropathol 1986;70: 308-313.Crossref 23. Borit A, McIntosh GC: Myelin basic protein and glial fibrillary acid protein in human fetal brain . Neuropathol Appl Neurobiol 1981;7: 279-287.Crossref 24. Takashima S, Becker LE: Developmental changes of glial fibrillary acidic protein in cerebral white matter . Arch Neurol 1983;40:14-18.Crossref 25. Card JP, Rafols JA: Tanycytes of the third ventricle of the neonatal rat: A Golgi study . Am J Anat 1978;151:173-190.Crossref 26. Bleier R: The relations of ependyma to neurons and capillaries in the hypothalamus: A Golgi-Cox study . J Comp Neurol 1971;142: 439-464.Crossref 27. Angevine JB, Sidman RL: Autoradiographic study of cell migration during histogenesis of the cerebral cortex in the mouse . Nature 1961;192:766-768.Crossref 28. Berry M, Rogers AW: The migration of neuroblasts in the developing cerebral cortex . J Anat 1965;99:691-709. 29. Larroche J-C: Quelques aspects anatomiques du développement cérébral . Biol Neonate 1962;4:126-153.Crossref 30. Friede RL: Developmental Neuropathology . New York, Springer-Verlag NY Inc, 1975. 31. Kater S, Letourneau P (eds): Biology of the Growth Cone . New York, Alan R Liss Inc, 1985. 32. Morest D: A study of neurogenesis in the forebrain of opossum pouch young . Z Anat Entwicklungsgesch 1970;130:265-305.Crossref 33. Molliver ME, Kostović I, Van der Loos H: The development of synapses in cerebral cortex of the human fetus . Brain Res 1973;50:403-407.Crossref 34. Hinds JW, Hinds PL: Synapse formation in the mouse olfactory bulb: I. Quantitative studies . J Comp Neurol 1976;169:15-40.Crossref 35. Rorke LB, Riggs HE: Myelination of the Brain in the Newborn . New York, JB Lippincott, 1969. 36. Woodard JS: Origin of the external granule layer of the cerebellar cortex . J Comp Neurol 1960;115:65-73.Crossref 37. Rakić P, Sidman RL: Histogenesis of cortical layers in human cerebellum, particularly the lamina dissecans . J Comp Neurol 1970;139: 473-500.Crossref 38. Mugnaini E, Forströnen PF: Ultrastructural studies on the cerebellar histogenesis: I. Differentiation of granule cells and development of glomeruli in the chick embryo . Z Mikrosk Anat Forsch 1967;77:115-143.Crossref 39. Rakić P: Neuron-glia relationship during granule cell migration in developing cerebellar cortex: A Golgi and electron microscopic study in Macacus rhesus . J Comp Neurol 1971;141:283-312.Crossref 40. Hausmann B, Sievers J: Cerebellar external granule cells are attached to the basal lamina from the onset of migration up to the end of their proliferative activity . J Comp Neurol 1985;241: 50-62.Crossref 41. Trenkner E, Smith D, Segil N: Is cerebellar granule cell migration regulated by an internal clock? J Neurosci 1984;11:2850-2855. 42. Zećević N, Rakić P: Differentiation of Purkinje cells and their relationship to other components of developing cerebellar cortex in man . J Comp Neurol 1976;167:27-47.Crossref 43. Altman J: Postnatal development of the cerebellar cortex in the rat: I. The external germinal layer and transitional molecular layer . J Comp Neurol 1972;145:353-397.Crossref 44. Altman J: Postnatal development of the cerebellar cortex in the rat: III. Maturation of the components of the granular layer . J Comp Neurol 1972;145:465-513.Crossref 45. West MJ, Del Cerro M: Early formation of synapses in the molecular layer of the fetal rat cerebellum . J Comp Neurol 1975;165:137-160.Crossref 46. Shimada M, Langman J: Repair of the external granular layer of the hamster cerebellum after prenatal and postnatal administration of methylazoxymethanol . Teratology 1970; 3:119-134.Crossref 47. Margolis G, Kilham L, Johnson RH: The parvoviruses and replicating cells: Insights into the pathogenesis of cerebellar hypoplasia . Prog Neuropathol 1971;1:168-201. 48. Altman J, Anderson WJ: Experimental reorganization of the cerebellar cortex: I. Morphological effects of elimination of all microneurons with prolonged x-irradiation started at birth . J Comp Neurol 1972;146:355-406.Crossref 49. Jones MZ, Gardner E: Pathogenesis of methylazoxymethanol-induced lesions in the postnatal mouse cerebellum . J Neuropathol Exp Neurol 1976;35:413-444.Crossref 50. Yakovlev PI, Lecours A-R: The myelination cycles of regional maturation of the brain , in Minkowski A (ed): Regional Development of the Brain in Early Life . Philadelphia, FA Davis Co Publishers, 1967, pp 3-70. 51. Roessmann U, Gambetti P: Pathological reaction of astrocytes in perinatal brain injury: Immunohistochemical study . Acta Neuropathol 1986;70:302-307.Crossref 52. Choi BH, Lapham LW, Amin Zaki L, et al: Abnormal neuronal migration, deranged cerebral cortical organization, and diffuse white matter astrocytosis of human fetal brain: A major effect of methylmercury poisoning in utero . J Neuropathol Exp Neurol 1978;37:719-733.Crossref 53. Marsh DO, Myers GY, Clarkson Th W, et al: Fetal methylmercury poisoning: Clinical and toxicological data on 29 cases . Ann Neurol 1980;7:348-353.Crossref 54. Choi BH, Cho KH, Lapham LW: Effects of methylmercury on DNA synthesis of human fetal astrocytes: A radioautographic study . Brain Res 1980;202:238-242. 55. Choi BH, Cho KH, Lapham LW: Effects of methylmercury on human fetal neurons and astrocytes in vitro: A time-lapse cinematographic, phase, and electron microscopic study . Environ Res 1981;24:61-74.Crossref 56. Choi BH: Mercury and abnormal development of the fetal brain , in Dreosti I, Smith R (eds): Neurobiology of Trace Elements . Clifton, NJ, Humana Press, 1983, vol 1, pp 197-235. 57. Norman MG, O'Kusky JR: The growth and development of microvasculature in human cerebral cortex . J Neuropathol Exp Neurol 1986; 45:222-232. 58. Norman MG: On the morphogenesis of ulegyria . Acta Neuropathol 1981;53:331-332.Crossref 59. Larroche J-C: Fetal encephalopathies of circulatory origin . Biol Neonate 1986;50:61-74.Crossref 60. Norman MG: Bilateral encephaloclastic lesions in a 26-week gestation fetus: Effect on neuronal migration . Can J Neurol Sci 1980;7: 191-194. 61. Levine DN, Fisher MA, Caviness VS Jr: Porencephaly with micropolygyria: A pathologic study . Acta Neuropathol 1974;29:99-113.Crossref 62. Richman DP, Steward RM, Caviness VS Jr: Cerebral microgyria in a 27-week fetus: An architectonic and topographic analysis . J Neuropathol Exp Neurol 1974;33:374-384.Crossref 63. Williams RS, Ferrante RJ, Caviness VS Jr: The cellular pathology of microgyria: A Golgi analysis . Acta Neuropathol 1976;36:269-283.Crossref 64. Dekaban A: Large defects in cerebral hemispheres associated with cortical dysgenesis . J Neuropathol Exp Neurol 1965;24:512-530.Crossref 65. Friede RL, Mikolasek J: Postencephalitic porencephaly, hydranencephaly, or polymicrogyria: A review . Acta Neuropathol 1978;43:161-168.Crossref 66. Ferrer I, Navarro C: Multicystic encephalomalacia of infancy: Clinico-pathological report of seven cases . J Neurol Sci 1978;38:179-189.Crossref 67. Ferrer I: A Golgi analysis of unlayered polymicrogyria . Acta Neuropathol 1984;65: 69-76.Crossref 68. McBride MC, Kemper TL: Pathogenesis of four-layered microgyric cortex in man . Acta Neuropathol 1982;57:93-98.Crossref 69. Dvorak K, Feit J, Jurankova Z: Experimentally induced focal microgyria and status verrucosus deformis in rats—pathogenesis and interrelation: Histological and autoradiographical study . Acta Neuropathol 1978; 44:121-129.Crossref 70. Brun A: Marginal glioneuronal heterotopias of the central nervous system . Acta Pathol Microbiol Immunol Scand A 1975;65:221-233. 71. Caviness VS, Evrard PH Jr, Lyon G: Radial neuronal assemblies, ectopies, and necrosis of developing cortex: A case analysis . Acta Neuropathol 1978;41:67-72.Crossref 72. Robain O, Deonna T: Pachygyria and congenital nephrosis: Disorder of migration and neuronal orientation . Acta Neuropathol 1983;60: 137-141.Crossref 73. Dambska M, Wisniewski KE, Sher JH: Marginal glioneuronal heterotopias in nine cases with and without cortical abnormalities . J Child Neurol 1986;1:149-157.Crossref 74. Duckett S, Pearse AGE: The cells of CajalRetzius in the developing human brain . J Anat 1968;102:183-187. 75. Noback CR, Purpura DP: Postnatal ontogenesis of neurons in cat neocortex . J Comp Neurol 1961;117:291-308.Crossref 76. Brun A: The subpial granular layer of the foetal cerebral cortex in man: Its ontogeny and significance in cortical malformations . Acta Pathol Microbiol Immunol Scand Suppl 1965; 179:1-98. 77. Sarnat HB: Granular cell glioblastoma . J Neuropathol Exp Neurol 1976;46:112-113.Crossref 78. Ronnevi L-O, Conradi S: Ultrastructural evidence for spontaneous elimination of synaptic terminals on spinal motoneurons in the kitten . Brain Res 1974;80:335-359.Crossref 79. Inagaki S, Sakanaka S, Shiosaka S, et al: Experimental and immunohistochemical studies on the cerebellar substance P of the rat: Localization, postnatal ontogeny, and ways of entry into the cerebellum . Neuroscience 1982;7:639-646.Crossref 80. 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Journal

American Journal of Diseases of ChildrenAmerican Medical Association

Published: Sep 1, 1987

References