Differential distribution of neurons in the gyral white matter of the human cerebral cortex

Journal of Comparative Neurology

Volumn 518, Issue 23, 2010, Pages 4740-4759

  Garcia Marin V ^a,b   Blazquez Llorca, L ^a,b   Rodriguez, J R ^a,b   Gonzalez Soriano, J ^c   DeFelipe, J ^a,b  

^a TECHNICAL UNIVERSITY OF MADRID   (Spain)

^b INSTITUTO CAJAL   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Cortical differences; Electron microscopy; Interneurons; Number of neurons; Synapses

Indexed keywords

CALRETININ;

ADULT; AGED; ARTICLE; BRAIN CORTEX; CELL DENSITY; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; GABAERGIC SYSTEM; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; INNERVATION; INTERNEURON; MALE; MICROSCOPY; NERVE CELL; NERVE ENDING; NEUROCHEMISTRY; NEUROPIL; PRIORITY JOURNAL; SYNAPSE; WHITE MATTER;

EID: 77958559543     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22485     Document Type: Article

References (119)

1. Akbarian S, Bunney WE Jr, Potkin SG, Wigal SB, Hagman JO, Sandman CA, Jones EG. 1993. Altered distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase cells in frontal lobe of schizophrenics implies disturbances of cortical development. Arch Gen Psychiatry 50: 169-177.
2. Akbarian S, Kim JJ, Potkin SG, Hetrick WP, Bunney WE Jr, Jones EG. 1996. Maldistribution of interstitial neurons in prefrontal white matter of the brains of schizophrenic patients. Arch Gen Psychiatry 53: 425-436.
3. Allendoerfer KL, Shatz CJ. 1994. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci 17: 185-218.
4. Alonso-Nanclares L, DeFelipe J. 2005. Vesicular glutamate transporter 1 immunostaining in the normal and epileptic human cerebral cortex. Neuroscience 134: 59-68.
5. Alonso-Nanclares L, Minelli A, Melone M, Edwards RH, Defelipe J, Conti F. 2004. Perisomatic glutamatergic axon terminals: a novel feature of cortical synaptology revealed by vesicular glutamate transporter 1 immunostaining. Neuroscience 123: 547-556.
6. Alonso-Nanclares L, Gonzalez-Soriano J, Rodriguez JR, DeFelipe J. 2008. Gender differences in human cortical synaptic density. Proc Natl Acad Sci USA 105: 14615- 14619.
7. Anderson SA, Volk DW, Lewis DA. 1996. Increased density of microtubule associated protein 2-immunoreactive neurons in the prefrontal white matter of schizophrenic subjects. Schizophr Res 19: 111-119.
8. Andrioli A, Alonso-Nanclares L, Arellano JI, DeFelipe J. 2007. Quantitative analysis of parvalbumin-immunoreactive cells in the human epileptic hippocampus. Neuroscience 149: 131-143.
9. Ang LC, Shul DD. 1995. Peptidergic neurons of subcortical white matter in aging and Alzheimer's brain. Brain Res 674: 329-335.
10. Arellano JI, Munoz A, Ballesteros-Yanez I, Sola RG, DeFelipe J. 2004. Histopathology and reorganization of chandelier cells in the human epileptic sclerotic hippocampus. Brain 127: 45-64.
11. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A., Buzsaki G, Cauli B, DeFelipe J, Fairén A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Karube F, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Kisvarday Z, Lambolez B, Lewis D, Marin O, Markram H, Muñoz A, Packer A, Petersen C, Rockland K, Rossier J, Rudy B, Somogyi P, Staiger JF, Tamas G, Thomson AM, Toledo-Rodriguez M, Wang Y, West DC, Yuste R. 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9: 557-568.
12. Beasley CL, Cotter DR, Everall IP. 2002. Density and distribution of white matter neurons in schizophrenia, bipolar disorder and major depressive disorder: no evidence for abnormalities of neuronal migration. Mol Psychiatry 7: 564-570.
13. Benavides-Piccione R, DeFelipe J. 2003. Different populations of tyrosine-hydroxylase-immunoreactive neurons defined by differential expression of nitric oxide synthase in the human temporal cortex. Cereb Cortex 13: 297-307.
14. Benavides-Piccione R, DeFelipe J. 2007. Distribution of neurons expressing tyrosine hydroxylase in the human cerebral cortex. J Anat 211: 212-222.
15. Blazquez-Llorca L, Garcia-Marin V, DeFelipe J. 2010. GABAergic complex basket formations in the human neocortex. J Comp Neurol (in press).
16. Boulland JL, Ferhat L, Tallak Solbu T, Ferrand N, Chaudhry FA, Storm-Mathisen J, Esclapez M. 2007. Changes in vesicular transporters for gamma-aminobutyric acid and glutamate reveal vulnerability and reorganization of hippocampal neurons following pilocarpine-induced seizures. J Comp Neurol 503: 466-485.
17. Bunney WE, Bunney BG. 2000. Evidence for a compromised dorsolateral prefrontal cortical parallel circuit in schizophrenia. Brain Res Brain Res Rev 31: 138-146.
18. Burkhalter A. 2008. Many specialists for suppressing cortical excitation. Front Neurosci 2: 155-167.
19. Cajal SR. 1895. Apuntes para el estudio del bulbo raquídeo, cerebelo y origen de los nervios encefálicos. Anal Soc Esp Hist Nat XXIV: 1-118.
20. Cajal SR. 1896. Beiträge zum Studium der Medulla Oblongata, des kleinhirns und des Ursprungs der gehirnnerven. Leipzig: Verlag von Johann Ambrosius Barth.
21. Cajal SR. 1899- 1904. Textura del Sistema Nervioso del Hombre y de los Vertebrados. Madrid: Imprenta y Libreria de Nicolas Moya.
22. Cajal SR. 1901a. Estudios sobre la corteza cerebral humana IV: Estructura de la corteza cerebral olfativa del hombre y mamíferos. Trab Lab Invest Biol Univ Madrid 1: 1-140.
23. Cajal SR. 1901b. Textura del lóbulo olfativo accesorio. Trab Lab Invest Biol Univ Madrid 1: 141-149.
24. Campbell MJ, Morrison JH. 1989. Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 282: 191-205.
25. Campbell MJ, Hof PR, Morrison JH. 1991. A subpopulation of primate corticocortical neurons is distinguished by somatodendritic distribution of neurofilament protein. Brain Res 539: 133-136.
26. Cauller LJ, Clancy B, Connors BW. 1998. Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I. J Comp Neurol 390: 297-310.
27. Celio MR. 1993. Perineuronal nets of extracellular matrix around parvalbumin-containing neurons of the hippocampus. Hippocampus 3( Spec No.): 55-60.
28. Celio MR, Scharer L, Morrison JH, Norman AW, Bloom FE. 1986. Calbindin immunoreactivity alternates with cytochrome c-oxidase-rich zones in some layers of the primate visual cortex. Nature 323: 715-717.
29. Chan-Palay V, Allen YS, Lang W, Haesler U, Polak JM. 1985. Cytology and distribution in normal human cerebral cortex of neurons immunoreactive with antisera against neuropeptide Y. J Comp Neurol 238: 382-389.
30. Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, Storm-Mathisen J. 1998. The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18: 9733-9750.
31. Chun JJ, Shatz CJ. 1989a. The earliest-generated neurons of the cat cerebral cortex: characterization by MAP2 and neurotransmitter immunohistochemistry during fetal life. J Neurosci 9: 1648-1667.
32. Chun JJ, Shatz CJ. 1989b. Interstitial cells of the adult neocortical white matter are the remnant of the early generated subplate neuron population. J Comp Neurol 282: 555-569.
33. Clancy B, Cauller LJ. 1999. Widespread projections from subgriseal neurons (layer VII) to layer I in adult rat cortex. J Comp Neurol 407: 275-286.
34. Clancy B, Silva-Filho M, Friedlander MJ. 2001. Structure and projections of white matter neurons in the postnatal rat visual cortex. J Comp Neurol 434: 233-252.
35. Clancy B, Teague-Ross TJ, Nagarajan R. 2009. Cross-species analyses of the cortical GABAergic and subplate neural populations. Front Neuroanat 3: 20.
36. Clancy B, Defelipe J, Espinosa A, Fairen A, Jinno S, Kanold P, Luhmann HJ, Rockland KS, Tamamaki N, Yan XX. 2010. Cortical GABAergic neurons: stretching it remarks, main conclusions and discussion. Front Neuroanat 4: 7.
37. Colonnier M. 1981. The electron-microscopic analysis of the neuronal organization of the cerebral cortex. In: Schmitt FO, Worden FG, Adelman G, Dennis SG, editors. The organization of the cerebral cortex. Cambridge, MA: MIT Press. p 125-152.
38. DeFelipe J. 1993. A study of NADPH disphorase-positive axonal plexuses in the human temporal cortex. Brain Res 615: 342-346.
39. DeFelipe J. 1997. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14: 1-19.
40. DeFelipe J, Fairen A. 1993. A simple and reliable method for correlative light and electron microscopic studies. J Histochem Cytochem 41: 769-772.
41. DeFelipe J, Jones E. 1988. Cajal on the cerebral cortex. New York: Oxford University Press.
42. DeFelipe J, Marco P, Busturia I, Merchan-Perez A. 1999. Estimation of the number of synapses in the cerebral cortex: methodological considerations. Cereb Cortex 9: 722-732.
43. DeFelipe J, Ballesteros-Yanez I, Inda MC, Munoz A. 2006. Double-bouquet cells in the monkey and human cerebral cortex with special reference to areas 17 and 18. Prog Brain Res 154: 15-32.
44. del Rio MR, DeFelipe J. 1994. A study of SMI 32-stained pyramidal cells, parvalbumin-immunoreactive chandelier cells, and presumptive thalamocortical axons in the human temporal neocortex. J Comp Neurol 342: 389-408.
45. del Rio MR, DeFelipe J. 1995. A light and electron microscopic study of calbindin D-28k immunoreactive double bouquet cells in the human temporal cortex. Brain Res 690: 133-140.
46. del Rio MR, DeFelipe J. 1997a. Double bouquet cell axons in the human temporal neocortex: relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities. J Chem Neuroanat 13: 243-251.
47. del Rio MR, DeFelipe J. 1997b. Synaptic connections of calretinin-immunoreactive neurons in the human neocortex. J Neurosci 17: 5143-5154.
48. Eastwood SL, Harrison PJ. 2003. Interstitial white matter neurons express less reelin and are abnormally distributed in schizophrenia: toward an integration of molecular and morphologic aspects of the neurodevelopmental hypothesis. Mol Psychiatry 8: 769, 821-831.
49. Eastwood SL, Harrison PJ. 2005. Interstitial white matter neuron density in the dorsolateral prefrontal cortex and parahippocampal gyrus in schizophrenia. Schizophr Res 79: 181-188.
50. Engel JJ, editor. 1987. Surgical treatment of epilepsies. New York: Raven Press.
51. Estrada C, DeFelipe J. 1998. Nitric oxide-producing neurons in the neocortex: morphological and functional relationship with intraparenchymal microvasculature. Cereb Cortex 8: 193-203.
52. Finney EM, Stone JR, Shatz CJ. 1998. Major glutamatergic projection from subplate into visual cortex during development. J Comp Neurol 398: 105-118.
53. Friauf E, McConnell SK, Shatz CJ. 1990. Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex. J Neurosci 10: 2601- 2613.
54. Giguere M, Goldman-Rakic PS. 1988. Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in frontal lobe of rhesus monkeys. J Comp Neurol 277: 195-213.
55. Gonzalez-Albo MC, Elston GN, DeFelipe J. 2001. The human temporal cortex: characterization of neurons expressing nitric oxide synthase, neuropeptides and calcium-binding proteins, and their glutamate receptor subunit profiles. Cereb Cortex 11: 1170-1181.
56. Gray EG. 1959. Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183: 1592-1593.
57. Hanganu IL, Okabe A, Lessmann V, Luhmann HJ. 2009. Cellular mechanisms of subplate-driven and cholinergic input-dependent network activity in the neonatal rat somatosensory cortex. Cereb Cortex 19: 89-105.
58. Hayes TL, Lewis DA. 1992. Nonphosphorylated neurofilament protein and calbindin immunoreactivity in layer III pyramidal neurons of human neocortex. Cereb Cortex 2: 56-67.
59. Hendry SH, Jones EG, Emson PC. 1984. Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex. J Neurosci 4: 2497-2517.
60. Herbison AE, Simonian SX, Norris PJ, Emson PC. 1996. Relationship of neuronal nitric oxide synthase immunoreactivity to GnRH neurons in the ovariectomized and intact female rat. J Neuroendocrinol 8: 73-82.
61. Higo S, Udaka N, Tamamaki N. 2007. Long-range GABAergic projection neurons in the cat neocortex. J Comp Neurol 503: 421-431.
62. Hogan D, Berman NE. 1992. The development of neuropeptide Y immunoreactive neurons in cat visual cortical areas. Brain Res Dev Brain Res 67: 343-369.
63. Inda MC, Defelipe J, Munoz A. 2007. The distribution of chandelier cell axon terminals that express the GABA plasma membrane transporter GAT-1 in the human neocortex. Cereb Cortex 17: 2060-2071.
64. Johnson J, Chen TK, Rickman DW, Evans C, Brecha NC. 1996. Multiple gamma-Aminobutyric acid plasma membrane transporters (GAT-1, GAT-2, GAT-3) in the rat retina. J Comp Neurol 375: 212-224.
65. Jones EG. 1995. Cortical development and neuropathology in schizophrenia. Ciba Found Symp 193: 277-295.
66. Jones EG, DeFelipe J, Hendry SH, Maggio JE. 1988. A study of tachykinin-immunoreactive neurons in monkey cerebral cortex. J Neurosci 8: 1206-1224.
67. Judas M, Sestan N, Kostovic I. 1999. Nitrinergic neurons in the developing and adult human telencephalon: transient and permanent patterns of expression in comparison to other mammals. Microsc Res Techniq 45: 401-419.
68. Kanold PO, Shatz CJ. 2006. Subplate neurons regulate maturation of cortical inhibition and outcome of ocular dominance plasticity. Neuron 51: 627-638.
69. Kirkpatrick B, Conley RC, Kakoyannis A, Reep RL, Roberts RC. 1999. Interstitial cells of the white matter in the inferior parietal cortex in schizophrenia: an unbiased cell-counting study. Synapse 34: 95-102.
70. Kirkpatrick B, Messias NC, Conley RR, Roberts RC. 2003. Interstitial cells of the white matter in the dorsolateral prefrontal cortex in deficit and nondeficit schizophrenia. J Nerv Ment Dis 191: 563-567.
71. Kostovic I, Rakic P. 1980. Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. J Neurocytol 9: 219-242.
72. Kostovic I, Rakic P. 1990. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297: 441-470.
73. Kuljis RO, Rakic P. 1989. Distribution of neuropeptide Y-containing perikarya and axons in various neocortical areas in the macaque monkey. J Comp Neurol 280: 383-392.
74. Luhmann HJ, Kilb W, Hanganu-Opatz IL. 2009. Subplate cells: amplifiers of neuronal activity in the developing cerebral cortex. Front Neuroanat 3: 19.
75. Lund JS, Lewis DA. 1993. Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics. J Comp Neurol 328: 282-312.
76. Luth HJ, Hedlich A, Hilbig H, Winkelmann E, Mayer B. 1994. Morphological analyses of NADPH-diaphorase/nitric oxide synthase positive structures in human visual cortex. J Neurocytol 23: 770-782.
77. Luth HJ, Hedlich A, Hilbig H, Winkelmann E, Mayer B. 1995. Postnatal development of NADPH-diaphorase/nitric oxide synthase positive nerve cells in the visual cortex of the rat. J Hirnforsch 36: 313-328.
78. McConnell SK, Ghosh A, Shatz CJ. 1989. Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245: 978-982.
79. Merchan-Perez A, Rodriguez JR, Ribak CE, DeFelipe J. 2009. Proximity of excitatory and inhibitory axon terminals adjacent to pyramidal cell bodies provides a putative basis for nonsynaptic interactions. Proc Natl Acad Sci U S A 106: 9878-9883.
80. Mesulam M, Geula C. 1991. Differential distribution of a neurofilament protein epitope in acetylcholinesterase-rich neurons of human cerebral neocortex. Brain Res 544: 169-173.
81. Meyer G, Gonzalez-Hernandez T, Galindo-Mireles D, Castaneyra-Perdomo A, Ferres-Torres R. 1991. The efferent projections of neurons in the white matter of different cortical areas of the adult rat. Anat Embryol 184: 99-102.
82. Meyer G, Wahle P, Castaneyra-Perdomo A, Ferres-Torres R. 1992. Morphology of neurons in the white matter of the adult human neocortex. Exp Brain Res 88: 204-212.
83. Meynert T. 1867. Der Bau der Gross-Hirnrinde und seine ortlichen Verschiedenheiten, nebst einem pathologisch-anatomischen Corollarium. Vierteljahrsschr Psychiatr 1: 77-93.
84. Minelli A, Brecha NC, Karschin C, DeBiasi S, Conti F. 1995. GAT-1, a high-affinity GABA plasma membrane transporter, is localized to neurons and astroglia in the cerebral cortex. J Neurosci 15: 7734-7746.
85. Minelli A, Alonso-Nanclares L, Edwards RH, DeFelipe J, Conti F. 2003. Postnatal development of the vesicular GABA transporter in rat cerebral cortex. Neuroscience 117: 337-346.
86. Mizukawa K, Vincent SR, McGeer PL, McGeer EG. 1988. Reduced nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase-positive neurons in cat cerebral white matter. Brain Res 461: 274-281.
87. Okhotin VE, Kalinichenko SG. 2003. Subcortical white matter interstitial cells: their connections, neurochemical specialization, and role in the histogenesis of the cortex. Neurosci Behav Physiol 33: 177-194.
88. Peters A, Jones EG. 1984. Cellular components of the cerebral cortex. Cerebral cortex. New York: Plenum.
89. Peters A, Palay SL, Webster H. 1991. The fine structure of the nervous system. Neurons and their supporting cells. New York: Oxford University Press.
90. Rakic P. 1977. Prenatal development of the visual system in rhesus monkey. Philos Trans R Soc Lond B Biol Sci 278: 245-260
91. Rioux L, Nissanov J, Lauber K, Bilker WB, Arnold SE. 2003. Distribution of microtubule-associated protein MAP2-immunoreactive interstitial neurons in the parahippocampal white matter in subjects with schizophrenia. Am J Psychiatry 160: 149-155.
92. Rojiani AM, Emery JA, Anderson KJ, Massey JK. 1996. Distribution of heterotopic neurons in normal hemispheric white matter: a morphometric analysis. J Neuropathol Exp Neurol 55: 178-183.
93. Sanchez C, Arellano JI, Rodriguez-Sanchez P, Avila J, DeFelipe J, Diez-Guerra FJ. 2001. Microtubule-associated protein 2 phosphorylation is decreased in the human epileptic temporal lobe cortex. Neuroscience 107: 25-33.
94. Sawada K, Barr AM, Nakamura M, Arima K, Young CE, Dwork AJ, Falkai P, Phillips AG, Honer WG. 2005. Hippocampal complexin proteins and cognitive dysfunction in schizophrenia. Arch Gen Psychiatry 62: 263-272.
95. Schmechel DE, Vickrey BG, Fitzpatrick D, Elde RP. 1984. GABAergic neurons of mammalian cerebral cortex: widespread subclass defined by somatostatin content. Neurosci Lett 47: 227-232.
96. Schwaller B, Bruckner G, Celio MR, Hartig W. 1999. A polyclonal goat antiserum against the calcium-binding protein calretinin is a versatile tool for various immunochemical techniques. J Neurosci Methods 92: 137-144.
97. Shering AF, Lowenstein PR. 1994. Neocortex provides direct synaptic input to interstitial neurons of the intermediate zone of kittens and white matter of cats: a light and electron microscopic study. J Comp Neurol 347: 433-443.
98. Silberberg G, Markram H. 2007. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53: 735-746.
99. Simonian SX, Herbison AE. 1996. Localization of neuronal nitric oxide synthase-immunoreactivity within sub-populations of noradrenergic A1 and A2 neurons in the rat. Brain Res 732: 247-252.
100. Smiley JF, Levey AI, Mesulam MM. 1998. Infracortical interstitial cells concurrently expressing m2-muscarinic receptors, acetylcholinesterase and nicotinamide adenine dinucleotide phosphate-diaphorase in the human and monkey cerebral cortex. Neuroscience 84: 755-769.
101. Sola RG, Hernando-Requejo V, Pastor J, Garcia-Navarrete E, DeFelipe J, Alijarde MT, Sanchez A, Dominguez-Gadea L, Martin-Plasencia P, Maestu F, DeFelipe-Oroquieta J, Ramon-Cajal S, Pulido-Rivas P. 2005. [Pharmacoresistant temporal-lobe epilepsy. Exploration with foramen ovale electrodes and surgical outcomes]. Rev Neurol 41: 4-16.
102. Somogyi P, Hodgson AJ, Smith AD, Nunzi MG, Gorio A, Wu JY. 1984. Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin-immunoreactive material. J Neurosci 4: 2590-2603.
103. Suarez-Sola ML, Gonzalez-Delgado FJ, Pueyo-Morlans M, Medina-Bolivar OC, Hernandez-Acosta NC, Gonzalez-Gomez M, Meyer G. 2009. Neurons in the white matter of the adult human neocortex. Front Neuroanat 3: 7.
104. Takamori S, Riedel D, Jahn R. 2000. Immunoisolation of GABA-specific synaptic vesicles defines a functionally distinct subset of synaptic vesicles. J Neurosci 20: 4904- 4911.
105. Thangavel R, Sahu SK, Van Hoesen GW, Zaheer A. 2009. Loss of nonphosphorylated neurofilament immunoreactivity in temporal cortical areas in Alzheimer's disease. Neuroscience 160: 427-433.
106. Tomioka R, Rockland KS. 2007. Long-distance corticocortical GABAergic neurons in the adult monkey white and gray matter. J Comp Neurol 505: 526-538.
107. Tomioka R, Okamoto K, Furuta T, Fujiyama F, Iwasato T, Yanagawa Y, Obata K, Kaneko T, Tamamaki N. 2005. Demonstration of long-range GABAergic connections distributed throughout the mouse neocortex. Eur J Neurosci 21: 1587-1600.
108. Torres-Reveron J, Friedlander MJ. 2007. Properties of persistent postnatal cortical subplate neurons. J Neurosci 27: 9962-9974.
109. Unal-Cevik I, Kilinc M, Gursoy-Ozdemir Y, Gurer G, Dalkara T. 2004. Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res 1015: 169-174.
110. Uylings HB, Delalle I. 1997. Morphology of neuropeptide Y-immunoreactive neurons and fibers in human prefrontal cortex during prenatal and postnatal development. J Comp Neurol 379: 523-540.
111. Valverde F, Facal-Valverde MV. 1988. 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 269: 168-192.
112. Vitellaro-Zuccarello L, Calvaresi N, De Biasi S. 2003. Expression of GABA transporters, GAT-1 and GAT-3, in the cerebral cortex and thalamus of the rat during postnatal development. Cell Tissue Res 313: 245-257.
113. Wahle P, Meyer G. 1987. Morphology and quantitative changes of transient NPY-ir neuronal populations during early postnatal development of the cat visual cortex. J Comp Neurol 261: 165-192.
114. Wahle P, Meyer G, Wu JY, Albus K. 1987. Morphology and axon terminal pattern of glutamate decarboxylase-immunoreactive cell types in the white matter of the cat occipital cortex during early postnatal development. Brain Res 433: 53-61.
115. Wahle P, Lubke J, Naegele JR. 1994. Inverted pyramidal neurons and interneurons in cat cortical subplate zone are labelled by monoclonal antibody SP1. Eur J Neurosci 6: 1167-1178.
116. West MJ, Gundersen HJ. 1990. Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296: 1-22.
117. Yan XX, Garey LJ, Jen LS. 1996a. Prenatal development of NADPH-diaphorase-reactive neurons in human frontal cortex. Cereb Cortex 6: 737-745.
118. Yan XX, Jen LS, Garey LJ. 1996b. NADPH-diaphorase-positive neurons in primate cerebral cortex colocalize with GABA and calcium-binding proteins. Cereb Cortex 6: 524-529.
119. Yanez IB, Munoz A, Contreras J, Gonzalez J, Rodriguez-Veiga E, DeFelipe J. 2005. Double bouquet cell in the human cerebral cortex and a comparison with other mammals. J Comp Neurol 486: 344-360.