Populations of subplate and interstitial neurons in fetal and adult human telencephalon

Journal of Anatomy

Volumn 217, Issue 4, 2010, Pages 381-399

  Judaš, Miloš ^a   Sedmak, Goran ^a   Pletikos, Mihovil ^a   Jovanov Milošević, Nataša ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

Author keywords

Deep (periventricular) interstitial neurons; Deep fetal interstitial neurons; Intermediate subventricular zone; Subplate neurons; Subplate zone; Superficial (gyral) interstitial neurons

Indexed keywords

CALBINDIN; CALRETININ; MICROTUBULE ASSOCIATED PROTEIN 2; NEURON SPECIFIC NUCLEAR PROTEIN; NEUROPEPTIDE Y; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANTERIOR COMMISSURE; ARTICLE; CAPSULA INTERNA; CORPUS CALLOSUM; HISTOCHEMISTRY; HUMAN; IMMUNOCYTOCHEMISTRY; INTERSTITIAL NEURON; NERVE CELL; PRIORITY JOURNAL; SUBPLATE NEURON; TELENCEPHALON; WHITE MATTER;

HUMANS; IMMUNOHISTOCHEMISTRY; INFANT, NEWBORN; NEURONS; PHENOTYPE; TELENCEPHALON;

PRIMATES; RADIATA; RODENTIA;

EID: 77956461438     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2010.01284.x     Document Type: Article

References (132)

1. Allen SJ, Dawbarn D, Spillantini MG. Distribution of beta-nerve growth factor receptors in the human basal forebrain. J Comp Neurol 1989, 289:626-640.
2. Allendoerfer KL, Shatz CJ. The subplate, a transient neocortical structure: its role in the development of connec-tions between thalamus and cortex. Annu Rev Neurosci 1994, 17:185-218.
3. Andersen DL, Tannenberg AEG, Burke CJ. Develop-mental rearrangements of cortical glutamate-NMDA receptor binding sites in late human gestation. Dev Brain Res 1995, 88:178-185.
4. Aoki C, Fenstemaker S, Lubin M. Nitric oxide synthase in the visual cortex of monocular monkeys as revealed by light and electron microscopic immunocytochemistry. Brain Res 1993, 620:97-113.
5. Barone P, Kennedy H. Non-uniformity of neocortex, areal heterogeneity of NADPH-diaphorase reactive neurons in adult macaque monkeys. Cereb Cortex 2000, 10:160-174.
6. Bayatti N, Moss JA, Sun L. A molecular neuro-anatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone. Cereb Cortex 2008, 18:1536-1548.
7. Benson DL, Isakson PJ, Jones EG. In situ hybridization reveals VIP precursor mRNA-containing neurons in monkey and rat neocortex. Mol Brain Res 1991, 9:169-174.
8. Chronwall B, Wolff JR. Prenatal and postnatal development of GABA-accumulating cells in the occipital neocortex of rat. J Comp Neurol 1980, 190:187-208.
9. Cipolloni PB, Pandya DN. Golgi, histochemical, and immunocytochemical analyses of the neurons of auditory-related cortices of the rhesus monkey. Exp Neurol 1991, 114:104-122.
10. Clancy B, Teague-Ross TJ, Nagarajan R. Cross-species analyses of the cortical GABAergic and subplate neural populations. Front Neuroanat 2009, 3:20. (Vol. 3, article 20, pp. 1-14)
11. Cobas A, Fairén A, Alvarez-Bolado G. Prenatal development of the intrinsic neurons of the rat neocortex: a comparative study of the distribution of GABA-immunoreactive cells and the GABA-A receptor. Neuroscience 1991, 40:375-397.
12. Colombo JA, Bentham C. Immunohistochemical analysis of subcortical white matter astroglia of infant and adult primate brains, with a note on resident neurons. Brain Res 2006, 1100:93-103.
13. Das GD, Kreutzberg GW. Evaluation of interstitial nerve cells in the central nervous system. A correlative study using acetylcholinesterase and Golgi techniques. Ergeb Anat Entwicklungsgesch 1968, 41:1-59.
14. DeAzevedo LC, Hedin-Pereira C, Lent R. Callosal neurons in the cingulate cortical plate and subplate of human fetuses. J Comp Neurol 1997, 386:60-70.
15. DeDiego I, Smith-Fernández A, Fairén A. Cortical cells that migrate beyond area boundaries: characterization of an early neuronal population in the lower intermediate zone of prenatal rats. Eur J Neurosci 1994, 6:983-997.
16. DeFelipe J. A study of NADPH diaphorase-positive axonal plexuses in the human temporal cortex. Brain Res 1993, 615:342-346.
17. Del Rio JA, Soriano E, Ferrer I. The development of GABA immunoreactivity in the neocortex of the mouse. J Comp Neurol 1992, 326:501-526.
18. Del Rio JA, Martínez A, Auladell C. Developmental history of the subplate and developing white matter in the murine neocortex. Neuronal organization and relationship with the main afferent systems at embryonic and perinatal stages. Cereb Cortex 2000, 10:784-801.
19. Delalle I, Evers P, Kostovic I. Laminar distribution of neuropeptide Y-immunoreactive neurons in human prefrontal cortex during development. J Comp Neurol 1997, 379:515-522.
20. Dombrowski SM, Barbas H. Differential expression of NADPH diaphorase in functionally distinct prefrontal cortices in the rhesus monkey. Neuroscience 1996, 72:49-62.
21. Egberongbe YI, Gentleman SM, Falkai P. The distribution of nitric oxide synthase immunoreactivity in the human brain. Neuroscience 1994, 59:561-578.
22. Ellison DW, Kowall NW, Martin JB. Subset of neurons characterized by the presence of NADPH-diaphorase in human substantia innominata. J Comp Neurol 1987, 260:233-245.
23. Estrada C, DeFelipe J. Nitric oxide-producing neurons in the neocortex, morphological and functional relationship with intraparenchymal microvasculature. Cereb Cortex 1998, 8:193-203.
24. Fischer HC, Kuljis RO. Multiple types of nitrogen monoxide synthase-/NADPH diaphorase-containing neurons in the human cerebral neocortex. Brain Res 1994, 654:105-117.
25. Foix C, Nicolesco J. Les Noyaux Gris Centraux et la Région Mésencéphalo-sousoptique 1925, Paris, Mason & Cie
26. Friedlander MJ, Torres-Reveron J. The changing roles of neurons in the cortical subplate. Front Neuroanat 2009, 3:15. (Vol. 3, article 15, pp. 1-8)
27. Gabbott PLA, Bacon SJ. Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: I. Cell morphology and morphometrics. J Comp Neurol 1996a, 364:567-608.
28. Gabbott PLA, Bacon SJ. Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions. J Comp Neurol 1996b, 364:609-636.
29. Gabbott PLA, Jays PR, Bacon SJ. Calretinin in human medial prefrontal cortex (areas 24a,b,c, 32 and 25). J Comp Neurol 1997, 38:389-410.
30. Garbossa D, Fontanella M, Tomasi S. Differential distribution of NADPH-diaphorase histochemistry in human cerebral cortex. Brain Res 2005, 1034:1-10.
31. Hashikawa T, Leggio MG, Hattori R. Nitric oxide synthase immunoreactivity colocalized with NADPH-diaphorase histochemistry in monkey cerebral cortex. Brain Res 1994, 641:341-349.
32. Hayashi M, Yamashita A, Shimizu K. Ontogeny of cholecystokinin-8 and glutamic acid decarboxylase in cerebral neocortex of macaque monkey. Exp Brain Res 1989, 74:249-255.
33. Haynes RL, Borenstein NS, Desilva TM. Axonal development in the cerebral white matter of the human fetus and infant. J Comp Neurol 2005, 484:156-167.
34. Hedlich A, Lüth HJ, Werner L. GABAerge NADPH-diaphorase-positive Martinottizellen im visuellen Cortex der Ratte. J Hirnforsch 1990, 31:681-687.
35. Hendrickson AE, Hunt SP, Wu JY. Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 1981, 292:605-607.
36. Hendry SH, Jones EG, Killackey HP. Choline acetyltransferase-immunoreactive neurons in fetal monkey cerebral cortex. Brain Res 1987, 465:311-317.
37. Honig LS, Herrmann K, Shatz CJ. Developmental changes revealed by immunohistochemical markers in human cerebral cortex. Cereb Cortex 1996, 6:794-806.
38. Huntley GW, Hendry SHC, Killackey HP. Temporal sequence of neurotransmitter expression by developing neurons of fetal monkey visual cortex. Dev Brain Res 1988, 43:69-96.
39. Huntley GW, deBlas AL, Jones EG. GABA-A receptor immunoreactivity in adult and developing monkey sensory-motor cortex. Exp Brain Res 1990, 82:519-535.
40. Iritani I, Satoh K. Distribution of somatostatin-immunoreactive cell bodies and fibers in the neocortex of Macaca fuscata. Synapse 1991, 9:50-59.
41. Jovanov-Milošević N, Petrović D, Petanjek Z. Mor-phology, molecular phenotypes and distribution of neurons in developing human corpus callosum. Eur J Neurosci 2010
42. Judaš M, Šestan N, Kostović I. Nitrinergic neurons in the developing and adult human telencephalon: transient and permanent patterns of expression in comparison to other mammals. Microsc Res Tech 1999, 45:401-419.
43. Judaš M, Radoš M, Jovanov-Milošević N. Structural, immunocytochemical and MR imaging properties of periventricular crossroads of growing cortical pathways in preterm infants. Am J Neuroradiol 2005, 26:2671-2684.
44. Judaš M, Sedmak G, Pletikos M. Early history of subplate and interstitial neurons: from Theodor Meynert (1867) to the discovery of the subplate zone (1974). J Anat 2010, 217:344-367.
45. Kanold PO, Luhmann HJ. The subplate and early cortical circuits. Annu Rev Neurosci 2010, 33:23-48.
46. Kordower JH, Mufson EJ. Nerve growth factor receptor-immunoreactive neurons within the developing human cortex. J Comp Neurol 1992, 323:25-41.
47. Kordower JH, Bartus RT, Bothwell M. Nerve growth factor receptor immunoreactivity in the nonhuman primate (Cebus apella): distribution, morphology, and colocalization with cholinergic enzymes. J Comp Neurol 1988, 277:465-486.
48. Kordower JH, Bartus RT, Marciano FF. Telencephalic cholinergic system of the New World monkey (Cebus apella): morphological assessment and analysis of the projection to amygdala. J Comp Neurol 1989, 279:528-545.
49. Kordower JH, Chen EY, Sladek JR. TRK-immunoreactivity in the monkey central nervous system: forebrain. J Comp Neurol 1994, 349:20-35.
50. Kostović I. Prenatal development of interstitial neurons in the " white" matter of the human telencephalon. Soc Neurosci Abstr 1984, 10:47.
51. Kostović I. Prenatal development of nucleus basalis complex and related fiber systems in man: a histochemical study. Neuroscience 1986, 17:1047-1077.
52. Kostović I. Structural and histochemical reorganization of the human prefrontal cortex during perinatal and postnatal life. Prog Brain Res 1990, 85:131-147.
53. Kostović I, Goldman-Rakic PS. Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain. J Comp Neurol 1983, 219:431-447.
54. Kostović I, Jovanov-Milošević N. The development of cerebral connections during the first 20-45 weeks' gestation. Semin Fetal Neonatal Med 2006, 11:415-422.
55. Kostović I, Judaš M. Correlation between sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anat Rec 2002, 267:1-6.
56. Kostović I, Judaš M. Prolonged coexistence of transient and permanent circuitry elements in the developing cerebral cortex of fetuses and preterm infants. Dev Med Child Neurol 2006, 48:388-393.
57. Kostović I, Judaš M. Transient patterns of cortical lamination during prenatal life: do they have implications for treatment? Neurosci Biobehav Rev 2007, 31:1157-1168.
58. Kostović I, Judaš M. The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatr 2010, 99:1119-1127.
59. Kostovic I, Rakic P. Cytology and the time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. J Neurocytol 1980, 9:219-242.
60. Kostovic I, Rakic P. Development of prestriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesterase staining. J Neurosci 1984, 4:25-42.
61. 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.
62. Kostović I, Kelović Z, Mrzljak L. Distribution and morphology of interstitial acetylcholinesterase (AChE) reactive neurons in the fiber bundles of the human fetal telencephalon. Neurosci Lett 1981, 7(Suppl):S288.
63. Kostović I, Judaš M, Kostović-Knežević Lj. Zagreb Research Collection of human brains for developmental neurobiologists and clinical neuroscientists. Int J Dev Biol 1991a, 35:215-230.
64. Kostović I, Štefulj-Fučić A, Mrzljak L. Prenatal and perinatal development of the somatostatin-immunoreactive neurons in the human prefrontal cortex. Neurosci Lett 1991b, 124:153-156.
65. Kostović I, Judaš M, Radoš M. Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 2002, 12:536-544.
66. Kostović I, Judaš M, Sedmak G. Developmental history of the subplate zone, subplate neurons and interstitial white matter neurons: relevance for schizophrenia. Int J Dev Neurosci 2010
67. Kowall NW, Beal MF. Cortical somatostatin, neuropeptide Y, and NADPH diaphorase neurons: normal anatomy and alterations in Alzheimer's disease. Ann Neurol 1988, 23:105-114.
68. Kuljis RO, Rakic P. Distribution of neuropeptide Y-containing perikarya and axons in various neocortical areas in the macaque monkey. J Comp Neurol 1989, 280:383-392.
69. Lauder JM, Han VKM, Henderson P. Prenatal ontogeny of the GABAergic system in the rat brain: an immunocytochemical study. Neuroscience 1986, 19:465-493.
70. Lee H, Choi BH. Density and distribution of excitatory amino acid receptors in the developing human fetal brain: a quantitative autoradiographic study. Exp Neurol 1992, 118:284-290.
71. Lehéricy S, Hirsch EC, Cervera-Piérot P. Heterogeneity and selectivity of the degeneration of cholinergic neurons in the basal forebrain of patients with Alzheimer's disease. J Comp Neurol 1993, 330:15-31.
72. Luhmann HJ, Kilb W, Hanganu-Opatz IL. Subplate cells: amplifiers of neuronal activity in the developing cerebral cortex. Front Neuroanat 2009, 3:19. (Vol. 3, article 19, pp. 1-11)
73. 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.
74. Lüth HJ, Hedlich A, Hilbig H. Morphological analyses of NADPH-diaphorase/nitric oxide synthase positive structures in human visual cortex. J Neurocytol 1994, 23:770-782.
75. Masood F, Wadhwa S, Bijlani V. An immunohistochemical study of neurotransmitter profiles in developing human visual cortex. Int J Dev Neurosci 1993, 11:387-397.
76. Mehra RD, Hendrickson AE. A comparison of the development of neuropeptide and MAP2 immunocyto-chemical labeling in the macaque visual cortex during prenatal and postnatal development. J Neurobiol 1993, 24:101-124.
77. Meinecke DL, Rakic P. Expression of GABA and GABA-A receptors by neurons of the subplate zone in developing primate occipital cortex: evidence for transient local circuits. J Comp Neurol 1992, 317:91-101.
78. Mesulam MM, Geula C. Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: observations based on the distribution of acetylcholinesterase and choline acetyltransferase. J Comp Neurol 1988, 275:216-240.
79. Mesulam MM, Mufson EJ. Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain 1984, 107:253-274.
80. Mesulam MM, Mufson EJ, Levey AI. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata) and hypothalamus in the rhesus monkey. J Comp Neurol 1983, 214:170-197.
81. Meyer G, Wahle P, Castaneyra-Perdomo A. Morphology of neurons in the white matter of the adult human neocortex. Exp Brain Res 1992, 88:204-212.
82. Mizukawa K, Vincent SR, McGeer PL. Reduced nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase-positive neurons in cat cerebral white matter. Brain Res 1988, 461:274-281.
83. Molnár Z, Metin C, Stoykova A. Comparative aspects of cerebral cortical development. Eur J Neurosci 2006, 23:921-934.
84. Mori S. Neuropeptide Y-like immunoreactivity in area 17 of chimpanzee. Okajimas Folia Anat Jpn 1996, 73:219-229.
85. Mrzljak L, Uylings HBM, Kostovic I. Prenatal development of neurons in the human prefrontal cortex: I. A qualitative Golgi study. J Comp Neurol 1988, 271:355-386.
86. Mrzljak L, Uylings HBM, Van Eden CG. Neuronal development in human prefrontal cortex in prenatal and postnatal stages. Prog Brain Res 1990, 85:185-222.
87. Mrzljak L, Uylings HBM, Kostović I. Prenatal development of neurons in the human prefrontal cortex. II. A quantitative Golgi study. J Comp Neurol 1992, 316:485-496.
88. Mufson EJ, Bothwell MA, Hersh LB. Nerve growth factor receptor immunoreactive profiles in the normal aged human basal forebrain: colocalization with cholinergic neurons. J Comp Neurol 1989, 285:196-217.
89. Norris PJ, Faull RLM, Emson PC. Neuronal nitric oxide synthase (nNOS) mRNA expression and NADPH-diaphorase staining in the frontal cortex, visual cortex and hippocampus of control and Alzheimer's disease brains. Mol Brain Res 1996, 41:36-49.
90. Northington FJ, Koehler RC, Traystman RJ. Nitric oxide synthase 1 and nitric oxide synthase 3 protein expression is regionally and temporally regulated in fetal brain. Dev Brain Res 1996, 95:1-14.
91. Ohyu J, Takashima S. Developmental characteristics of neuronal nitric oxide synthase (nNOS) immunoreactive neurons in fetal to adolescent human brains. Dev Brain Res 1998, 110:193-202.
92. Okhotin VE, Kalinichenko SG. Subcortical white matter interstitial cells: their connections, neurochemical specialization, and role in the histogenesis of the cortex. Neurosci Behav Physiol 2003, 33:177-194.
93. Okhotin VE, Kupriyanov VV. Neurovascular relationships in the human neocortex. Neurosci Behav Physiol 1997, 27:482-488.
94. Ramón y Cajal S. Histologie du Systeme Nerveux de l'Homme & des Vertébrés 1911, Tome II. Paris, A. Maloine, p
95. Reep RL. Cortical layer VII and persistent subplate cells in mammalian brains. Brain Behav Evol 2000, 56:212-234.
96. Regidor J, Edvinsson L, Divac I. NOS neurones lie near branchings of cortical arteriolae. Neuroreport 1993, 4:112-114.
97. Riche D, Foutz AS, Denavit-Saubie M. Developmental changes of NADPH-diaphorase neurons in the forebrain of neonatal and adult cat. Dev Brain Res 1995, 89:139-145.
98. Ritter LM, Unis AS, Meador-Woodruff JH. Ontogeny of ionotropic glutamate receptor expression in human fetal brain. Dev Brain Res 2001, 127:123-133.
99. Sandell JH. NADPH diaphorase histochemistry in the macaque striate cortex. J Comp Neurol 1986, 251:388-397.
100. Satoh J, Fibiger HC. Distribution of central cholinergic neurons in the baboon (Papio papio). I. General morphology. J Comp Neurol 1985, 236:197-214.
101. Satoh K, Arai R, Ikemoto K. Distribution of nitric oxide synthase in the central nervous system of Macaca fuscata: subcortical regions. Neuroscience 1995, 66:685-696.
102. Schiffmann S, Campistron G, Tugendhaft P. Immunocytochemical detection of GABAergic nerve cells in the human temporal cortex using a direct gamma-aminobutyric acid antiserum. Brain Res 1988, 442:270-278.
103. Schottler F, Collins JL, Fergus A. Structural interactions between NOS-positive neurons and blood vessels in the hippocampus. NeuroReport 1996, 7:966-968.
104. Schröder H, Schütz U, Burghaus L. Expression of the alpha4 isoform of the nicotinic acetylcholine receptor in the fetal human cerebral cortex. Dev Brain Res 2001, 132:33-45.
105. Schwartz ML, Meinecke ML. Early expression of GABA-containing neurons in the prefrontal and visual cortices of rhesus monkeys. Cereb Cortex 1992, 2:16-37.
106. Schwartz ML, Zheng DS, Goldman-Rakic PS. Periodicity of GABA-containing cells in primate prefrontal cortex. J Neurosci 1988, 8:1962-1970.
107. Sims KB, Crandall JE, Kosik KS. Microtubule-associated protein 2 (MAP2) immunoreactivity in human fetal neocortex. Brain Res 1988, 449:192-200.
108. Smiley JF, Levey AI, Mesulam MM. Infracortical interstitial cells concurrently expressing M2-muscarinic receptors, acetylcholinesterase and nicotinamide adenine dinucleotide phosphate-diaphorase in the human and monkey cerebral cortex. Neuroscience 1998, 84:755-769.
109. Smiley JF, McGinnis JP, Javitt DC. Nitric oxide synthase interneurons in the monkey cerebral cortex are subsets of the somatostatin, neuropeptide Y, and calbindin cells. Brain Res 2000, 863:205-212.
110. Sorensen KV. Somatostatin localization and distribution in the cortex and the subcortical white matter of human brain. Neuroscience 1982, 7:1227-1232.
111. Stensaas LJ. The development of hippocampal and dorsolateral pallial region of the cerebral hemisphere in fetal rabbits. II. Twenty millimeter stage, neuroblast morphology. J Comp Neurol 1967a, 129:71-84.
112. Stensaas LJ. The development of hippocampal and dorsolateral pallial regions of the cerebral hemisphere in fetal rabbits. IV. Forty-one millimeter stage, intermediate lamina. J Comp Neurol 1967b, 131:409-422.
113. Suárez-Solá ML, González-Delgado FJ, Pueyo-Morlans M. Neurons in the white matter of the adult human neocortex. Front Neuroanat 2009, 3:7. (Vol. 3, article 7, pp. 1-6)
114. Talos DM, Follett PL, Folkerth RD. Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. II. Human cerebral white matter and cortex. J Comp Neurol 2006, 497:61-77.
115. Tomioka R, Rockland KS. Long-distance corticocortical GABAergic neurons in the adult monkey white and gray matter. J Comp Neurol 2007, 505:526-538.
116. Ulfig N. Calcium-binding proteins in the human developing brain. Adv Anat Embryol Cell Biol 2002, 165:1-92.
117. Unger JW, Lange W. NADPH-diaphorase-positive cell populations in the human amygdala and temporal cortex: neuroanatomy, peptidergic characteristics and aspects of aging and Alzheimer's disease. Acta Neuropathol 1992, 83:636-646.
118. Uylings HBM, Delalle I. Morphology of neuropeptide Y-immunoreactive neurons and fibres in human prefrontal cortex during prenatal and postnatal development. J Comp Neurol 1997, 379:523-540.
119. Valtschanoff JG, Weinberg RJ, Kharazia VN. Neurons in rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, NOS immunocytochemistry, and colocalization with GABA. Neurosci Lett 1993, 157:157-161.
120. Valverde F, Facal-Valverde MV. Postnatal development of interstitial (subplate) cells in the white matter of the temporal cortex of kittens: a correlated Golgi and electron microscopic study. J Comp Neurol 1988, 269:168-192.
121. Van Eden CG, Mrzljak L, Voorn P. Prenatal development of GABA-ergic neurons in the neocortex of the rat. J Comp Neurol 1989, 289:213-227.
122. Vasung L, Huang H, Jovanov-Milošević N. Development of axonal pathways in the human fetal fronto-limbic brain: histochemical characterization and diffusion tensor imaging. J Anat 2010, 217:400-417.
123. Von Monakow C. Gehirnpathologie 1905, Vienna, Alfred Hölder
124. Wolff JR, Böttcher H, Zetzsche T. Development of GABAergic neurons in rat visual cortex as identified by glutamate decarboxylase-like immunoreactivity. Neurosci Lett 1984, 47:207-212.
125. Yamashita A, Hayashi M, Shimizu K. Ontogeny of somatostatin in cerebral cortex of macaque monkey: an immunohistochemical study. Dev Brain Res 1989, 45:103-111.
126. Yamashita A, Shimizu K, Hayashi M. Ontogeny of substance P-immunoreactive structures in the primate cerebral neocortex. Dev Brain Res 1990, 57:197-207.
127. Yan XX, Ribak CE. Prenatal development of nicotinamide adenine dinucleotide phosphate-diaphorase activity in the human hippocampal formation. Hippocampus 1997, 7:215-231.
128. Yan XX, Zheng DS, Garey LJ. Prenatal development of GABA-immunoreactive neurons in the human striate cortex. Dev Brain Res 1992, 65:191-204.
129. Yan XX, Garey LJ, Jen LS. Development of NADPH-diaphorase activity in the rat neocortex. Dev Brain Res 1994, 79:29-38.
130. Yan XX, Garey LJ, Jen LS. Prenatal development of NADPH-diaphorase-reactive neurons in human frontal cortex. Cereb Cortex 1996a, 6:737-745.
131. Yan XX, Jen LS, Garey LJ. NADPH-diaphorase-positive neurons in primate cerebral cortex colocalize with GABA and calcium-binding proteins. Cereb Cortex 1996b, 6:524-529.
132. Zecevic N, Milosevic A. Initial development of gamma-aminobutyric acid immunoreactivity in the human cerebral cortex. J Comp Neurol 1997, 380:495-506.