Normal and abnormal development of the human cerebral cortex

Neuroembryology

Volumn 1, Issue 2, 2002, Pages 78-90

  Chan, Wood Yee ^a   Kostovic, Ivica ^b   Takashima, Sachio ^c   Feldhaus, Christian ^d   Stoltenburg Didinger, Gisela ^e   Verney, Catherine ^f   Yew, David ^a   Ulfig, Norbert ^d  

^a and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

^b UNIVERSITY OF ZAGREB   (Croatia)

^c NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^d UNIVERSITY OF ROSTOCK   (Germany)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

^f HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

Brain injury; Cortical development; Cortical plate; Ganglionic eminence; Marginal zone; Premature brain; Subplate; Subventricular zone

Indexed keywords

CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; CELL NUCLEUS ANTIGEN; CHOLECYSTOKININ; DOUBLECORTIN; GLYCOPROTEIN; NEUROPEPTIDE Y; PARVALBUMIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; REELIN; SUBSTANCE P;

AGYRIA; AMYGDALOID NUCLEUS; BRAIN CELL; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN DISEASE; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN MATURATION; BRAIN PERFUSION; CAUDATE NUCLEUS; CELL MIGRATION; CELL PROLIFERATION; CELL TYPE; CENTRAL NERVOUS SYSTEM; CEREBRAL PALSY; CHROMOSOME 9Q; CORTICAL DYSPLASIA; DENDRITIC SPINE; DEVELOPMENTAL DISORDER; ENVIRONMENTAL FACTOR; FETUS DEVELOPMENT; GENE EXPRESSION; GESTATIONAL AGE; HUMAN; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOREACTIVITY; INTELLECTUAL IMPAIRMENT; LATERAL BRAIN VENTRICLE; LEUKOMALACIA; MEDIAN EMINENCE; MICROGYRIA; MORPHOLOGY; MUSCULAR DYSTROPHY; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; OLIVARY NUCLEUS; PACHYGYRIA; PATHOLOGY; PERIKARYON; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; STEM CELL; TELENCEPHALON; THALAMUS;

EID: 0009836315     PISSN: 14248522     EISSN: None     Source Type: Journal    
DOI: 10.1159/000054267     Document Type: Review

References (98)

1. His W: Die Entwicklung des menschlichen Gehirns während der ersten Monate. Leipzig, Hirzel, 1904.
2. Ulfig N, Neudörfer F, Bohl J: Transient structures of the human fetal brain: Subplate, thalamic reticular complex, ganglionic eminence. Histol Histopathol 2000;15:771-790.
3. Molnar Z: Development of Thalamocortical Connections. Berlin, Springer, 1998.
4. Ulfig N, Feldhaus C, Bohl J: Transient expression of synaptogyrin in the ganglionic eminence of the human fetal brain. Ann Anat 2000;182:505-508.
5. Embryonic vertebrate central nervous system: Revised terminology. The Boulder Committee. Anat Rec 1970;166:257-262.
6. Rakic P: Developmental events leading laminar and areal organization of the neocortex; in Schmitt FO (ed): The Organization of the Cerebral Cortex. Boston, MIT, 1981.
7. Pearlman AL, Faust PL, Hatten ME, Brunstrom JE: New directions for neuronal migration. Curr Opin Neurobiol 1998;8:45-54.
8. Förster E, Saum B, Tielsch A, Frotscher M: Reelin und die neuronale Migration entlang radialer Gliafortsätze. Ann Anat 2001; 183(suppl):24.
9. Kostovic I: Zentralnervensystem; in Hinrichsen KV (ed): Humanembryologie. Berlin, Springer, 1990.
10. Allendoerfer KL, Shatz CJ: The subplate, a transient neocortical structure: Its role in the development of connections between thalamus and cortex. Annu Rev Neurosci 1994;17:185-218.
11. Parnavelas JG: The origin and migration of cortical neurons: New vistas. Trends Neurosci 2000;23:126-131.
12. Kostovic I, Petanjek Z, Delalle I, Judas M: Developmental reorganization of the human association cortex during perinatal and postnatal life; in Kostovic I, Knezevic S, Wisniewski HM, Spilich GJ (eds): Neurodevelopment, Aging and Cognition. Boston, Birkhäuser, 1992, pp 3-17.
13. McConnell SK: Development and decision-making in the mammalian cerebral cortex. Brain Res 1988;472:1-23.
14. Yan YH, Van Brederode JFM, Hendrickson AE: Developmental changes in calretinin expression in GABAergic and nonGABAergic neurons in monkey striate cortex. J Comp Neurol 1995;363:78-92.
15. Smart I: The subependymal layer of the mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J Comp Neurol 1961;116:325-347.
16. Fischer K: Subependymale Zellproliferation und Tumordisposition brachycephaler Hunderassen. Acta Neuropathol (Berl) 1967;8:242-252.
17. Blakemore WF, Jolly RD: The subependymal plate and associated ependyma in the dog: An ultrastructural study. J Neurocytol 1972;1:69-84.
18. Blakemore WF: The ultrastructure of the subependymal plate in the rat. J Anat 1969;104:423-433.
19. Jacobson M: Developmental Neurobiology, ed 3. New York, Plenum, 1991.
20. Pierce ET: Histogenesis of the nuclei griseum pontis, corporis pontobulbaris and reticularis tegmenti pontis (Bechterew) in the mouse. An autoradiographic study. J Comp Neurol 1966;126:219-254.
21. Rakic P, Sidman RL: Telencephalic origin of pulvinar neurons in the fetal human brain. Z Anat Entwicklungsgesch 1969;129:53-82.
22. Sturrock RR, Smart IHM: A morphological study of the mouse subependymal layer from embryonic life to old age. J Anat 1980;130:391-415.
23. Levison SW, Goldman JE: Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 1993;10:201-212.
24. Luskin MB: Neuronal cell lineage in the vertebrate central nervous system. FASEB J 1994;8:722-730.
25. Jankovski A, Garcia C, Soriao E, Sotelo C: Proliferation, migration and differentiation of neuronal progenitor cells in the adult mouse subventricular zone surgically separated from its olfactory bulb. Eur J Neurosci 1998;10:3853-3868.
26. Alvarez-Buylla A, Herrera DG, Wichterle H: The subventricular zone: Source of neuronal precursors for brain repair. Prog Brain Res 2000;127:1-11.
27. Menezes JRL, Luskin MB: Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J Neurosci 1994;14:5399-5416.
28. Kakita A, Goldman JE: Patterns and dynamics of SVZ cell migration in the postnatal forebrain: Monitoring living progenitors in slice preparations. Neuron 1999;23:461-472.
29. Lim DA, Alvarez-Buylla A: Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci USA 1999;96:7526-7531.
30. Reynolds BA, Weiss S: Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707-1710.
31. Shen Q, Qian X, Capela A, Temple S: Stem cells in the embryonic cerebral cortex: Their role in histogenesis and patterning. J Neurobiol 1998;36:162-174.
32. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A: Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97:703-716.
33. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J: Identification of a neural stem cell in the adult mammalian central nervous system. Cell 1999;96:25-34.
34. Smart IHM, Sturrock RR: Ontogeny of the neostriatum; in Divac I, Öberg RGE (eds): The Neostriatium. New York, Pergamon, 1979, pp 127-146.
35. Fentress JC, Stanfield BB, Cowan WM: Observations on the development of the striatum in mice and rats. Anat Embryol (Berl) 1981;163:275-298.
36. Olsson M, Campbell K, Turnbull DH: Specification of mouse telencephalic and mid-hindbrain progenitors following heterotopic ultrasound-guided embryonic transplantation. Neuron 1997;19:761-772.
37. Kostovic I, Judas M: Transient patterns of organization of the human fetal brain. Croat Med J 1998;39:107-114.
38. Kostovic I: Prenatal development of nucleus basalis complex and related fiber systems in man: A histochemical study. Neuroscience 1986;17:1047-1077.
39. Letinic K, Kostovic I: Transient fetal structure, the gangliothalamic body, connects telencephalic germinal zone with all thalamic regions in the developing human brain. J Comp Neurol 1997;384:373-395.
40. Ulfig N, Feldhaus C, Setzer M, Bohl J: Expression of MAP1a and MAP1b in the ganglionic eminence and the internal capsule of the human fetal brain. Neurosci Res 2000;38:397-405.
41. Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG: The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci 1999; 19:7881-7888.
42. Anderson SA, Marin O, Horn C, Jennings K, Rubenstein JLR: Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 2001;128:353-363.
43. Métin C, Godement P: The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons. J Neurosci 1996;16:3219-3235.
44. Ulfig N, Setzer M, Neudörfer F, Bohl J: Distribution of SNAP-25 in transient neuronal circuitries of the developing human forebrain. Neuroreport 2000;11:1259-1263.
45. Marin-Padilla M: Neurons of layer I. A developmental analysis; in Peters A, Jones A (eds): Cerebral Cortex. New York, Plenum, 1986, vol 1, pp 447-478.
46. Zecevic N, Milosevic A, Rakic S, Marin-Padilla M: Early development and composition of the human primordial plexiform layer: An immunohistochemical study. J Comp Neurol 1999;412:241-254.
47. Meyer G, Schaaps JP, Moreau L, Goffinet AM: Embryonic and early fetal development of the human neocortex. J Neurosci 2000;20:1858-1868.
48. Marin-Padilla M, Marin-Padilla TM: Origin, prenatal development and structural organization of layer I of the human cerebral (motor) cortex. A Golgi study. Anat Embryol (Berl) 1982;164:161-206.
49. Molliver ME, Kostovic I, van der Loos H: The development of synapses in cerebral cortex of the human fetus. Brain Res 1973;50:403-407.
50. Larroche JC: The marginal layer in the neocortex of a 7 week-old human embryo. A light and electron microscopic study. Anat Embryol (Berl) 1981;162:301-312.
51. Zecevic N, Verney C: Development of the catecholamine neurons in human embryos and fetuses, with special emphasis on the innervation of the cerebral cortex. J Comp Neurol 1995; 351:509-535.
52. Brun A: The subpial granular layer of the foetal cerebral cortex in man. Its ontogeny and significance in congenital cortical malformations. Acta Pathol Microbiol Scand Suppl 1965;179:1-98.
53. Gadisseux J-F, Goffinet AM, Lyon G, Evrard P: The human transient subpial granular layer: An optical, immunohistochemical, and ultrastructural analysis. J Comp Neurol 1992;324:94-114.
54. Meyer G, González-Hernández T: Developmental changes in layer I of the human neocortex during prenatal life: A DiI-tracing and AChE and NADPH-d histochemistry study. J Comp Neurol 1993;338:317-336.
55. Verney C, Derer P: Cajal-Retzius neurons in human cerebral cortex at midgestation show immunoreactivity for neurofilament and calcium-binding proteins. J Comp Neurol 1995;359:144-153.
56. Meyer G, Goffinet AM: Prenatal development of reelin-immunoreactive neurons in the human neocortex. J Comp Neurol 1998;397:29-40.
57. Marin-Padilla M: Three-dimensional structural organization of layer I of the human cerebral cortex: A Golgi study. J Comp Neurol 1990;299:89-105.
58. Ulfig N, Tietz B, Bohl J: Alterations in the organization of the isocortical layer I in trisomy 22. Neurosci Res 1999;33:119-125.
59. Zecevic N, Milosevic A: Initial development of gamma-aminobutyric acid immunoreactivity in the human cerebral cortex. J Comp Neurol 1997;380:495-506.
60. Soriano E, Alvarado-Mallart RM, Dumesnil N, Del Rio JA, Sotelo C: Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron 1997;18:563-577.
61. Rice DS, Curran T: Mutant mice with scrambled brains: Understanding the signaling pathways that control cell positioning in the CNS. Genes Dev 1999;13:2758-2773.
62. Caviness VS Jr: Neocortical histogenesis in normal and reeler mice: A developmental study based upon [3H]thymidine autoradiography. Brain Res 1982;256:293-302.
63. Mrzljak L, Uylings HBM, Kostovic I, Van Eden CG: Prenatal development of neurons in the human prefrontal cortex. I. A qualitative Golgi study. J Comp Neurol 1988;271:355-386.
64. Kostovic I, Rakic P: Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 1990;297:441-470.
65. Shatz CJ, Chun JJM, Luskin MB: The role of the subplate in the development of the mammalian telencephalon; in Jones EG, Peters A (eds): Cerebral Cortex. New York, Plenum, 1988, vol 7, pp 35-58.
66. Allendoerfer KL, Shelton DL, Shooter EM, Shatz CJ: Nerve growth factor receptor immunoreactivity is transiently associated with the subplate neurons of the mammalian cerebral cortex. Proc Natl Acad Sci USA 1990;87:187-190.
67. O'Leary DD, Koester SE: Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron 1993;10:991-1006.
68. Ghosh A, Shatz CJ: Involvement of subplate neurons in the formation of ocular dominance columns. Science 1992;255:1441-1443.
69. Blakemore C: Introduction: Mysteries in the making of the cerebral cortex; in Bock G, Cardew G (eds): Development of the Cerebral Cortex: Ciba Foundation Symposium. New York, Wiley, 1995, pp 1-20.
70. McConnell SK, Ghosh A, Shatz CJ: Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 1989;245:978-982.
71. Kostovic I, Lukinovic N, Judas M, Bogdanovic N, Mrzljak L, Zecevic N, Kubat M: Structural basis of the developmental plasticity in the human cerebral cortex: The role of the transient subplate zone. Metab Brain Dis 1989;4:17-23.
72. Volpe JJ: Neurology of the Newborn, ed 3. Philadelphia, Saunders, 1995.
73. Ulfig N, Szabo A, Bohl J: Effect of fetal hydrocephalus on the distribution patterns of calcium-binding proteins in the human occipital cortex. Pediatr Neurosurg 2001;34:20-32.
74. Volpe JJ: Subplate neurons - missing link in brain injury of the premature infant? Pediatrics 1996;97:112-113.
75. Kostovic I, Molliver ME: A new interpretation of the laminar development of cerebral cortex: Synaptogenesis in different layers of neopallium in the human fetus. Anat Rec 1974;178:395.
76. Rakic P: Specification of cerebral cortical areas. Science 1988;241:170-176.
77. Luskin MB, Shatz CJ: Studies of the earliest generated cells of the cat's visual cortex: Cogeneration of subplate and marginal zones. J Neurosci 1985;5:1062-1075.
78. Bayer SA, Altman J: Development of layer I and the subplate in the rat neocortex. Exp Neurol 1990;107:48-62.
79. Brown M, Keynes R, Lumsden A: The Developing Brain. Oxford, Oxford University Press, 2001.
80. Kostovic I: Structural and histochemical reorganization of the human prefrontal cortex during perinatal and postnatal life. Prog Brain Res 1990;85:223-240.
81. Mizuguchi M, Takashima S, Kakita A, Yamada M, Ikeda K: Lissencephaly gene product: Localization in the central nervous system and loss of immunoreactivity in Miller-Dieker syndrome. Am J Pathol 1995;147:1142-1151.
82. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T: A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995;374:719-723.
83. Hirotsune S, Takahara T, Sasaki N, Imoto H, Okazaki Y, Eki T, Murakami Y, Abe M, Furuya K, Muramatsu M, Eto Y, Chapman VM, Hayashizaki Y: The reeler gene encodes a protein with an EGF-like motif expressed by pioneer neurons. Nat Genet 1995;10:77-83.
84. Reiner O, Carrozzo R, Shen Y, Wehnert M, Faustinella F, Dobyns WB, Caskey CT, Ledbetter DH: Isolation of a Miller-Dieker lissencephaly gene containing G protein β-subunitlike repeats. Nature 1993;364:717-721.
85. des Portes V, Pinard JM, Billuart P, Vinet MC, Koulakoff A, Carrie A, Gelot A, Dupuis E, Motte J, Berwald-Netter Y, Catala M, Kahn A, Beldjord C, Chelly J: A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 1998;92:51-61.
86. Identification and characterization of the tuberous sclerosis gene on chromosome 16. The European Chromosome 16 Tuberous Sclerosis Consortium. Cell 1993;75:1305-1315.
87. Brunelli S, Faiella A, Capra V, Nigro V, Simeone A, Cama A, Boncinelli E: Germline mutations in the homeobox gene EMX2 in patients with severe schizencephaly. Nat Genet 1996;12:94-96.
88. Mizuguchi M, Yamada M, Ikeda K, Takashima S: Expression of doublecortin and KIAA0369 protein in the fetal brain. Neuropathology 1999;19(suppl):A12.
89. Mallamaci A, Iannone R, Briata P, Pintonello L, Mercurio S, Boncinelli E, Corte G: EMX2 protein in the developing mouse brain and olfactory area. Mech Dev 1998;77:165-172.
90. Park S-H, Pepkowitz SH, Kerfoot C, De Rosa MJ, Poukens V, Wienecke R, DeClue JE, Vinters HV: Tuberous sclerosis in a 20-week gestation fetus: Immunohistochemical study. Acta Neuropathol (Berl) 1997;94:180-186.
91. Marin-Padilla M: Cajal-Retzius cells and the development of the neocortex. Trends Neurosci 1998;21:64-71.
92. Frotscher M: Dual role of Cajal-Retzius cells and reelin in cortical development. Cell Tissue Res 1997;290:315-322.
93. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K: The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 1995;14:899-912.
94. Isumi H, Takashima S, Kakita A, Yamada M, Ikeda K, Mizuguchi M: Expression of the LIS-1 gene product in brain anomalies with a migration disorder. Pediatr Neurol 1997;16:42-44.
95. Qin J, Mizuguchi M, Itoh M, Takashima S: Immunohistochemical expression of doublecortin in the human cerebrum: Comparison of normal development and neuronal migration disorders. Brain Res 2000;863:225-232.
96. Saito Y, Mizuguchi M, Oka A, Takashima S: Fukutin protein is expressed in neurons of the normal developing human brain but is reduced in Fukuyama-type congenital muscular dystrophy brain. Ann Neurol 2000;47:756-765.
97. Takashima S, Hirayama A, Okoshi Y, Itoh M: Vascular, axonal and glial pathogenesis of periventricular leukomalacia in fetuses and neonates. Neuroembryology 2002;1:72-77.
98. Ulfig N, Nickel J, Bohl J: Monoclonal antibodies SMI 311 and SMI 312 as tools to investigate the maturation of nerve cells and axonal patterns in human fetal brain. Cell Tissue Res 1998;291:433-443.