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From radial glia to pyramidal-projection neuron

Transcription factor cascades in cerebral cortex development

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Abstract

Pyramidal-projection neurons are glutamatergic neurons that develop from progenitors in the ventricular and subventricular zones of the embryonic cortex. Recently, much has been learned about the cortical progenitor cells and the cellular and molecular mechanisms by which the produce projection neurons. We now know that radial glia are the progenitors of most or all projection neurons and that they generate neurons by two distinct mitotic sequences: direct neurogenesis to produce a single daughter neuron or indirect neurogenesis to produce two to four neurons via intermediate progenitor cells. The underlying genetic programs for proliferation and differentiation are controlled and implemented by specific transcription factors, whose interactions largely determine the cortical surface area, thickness, and neuronal subtype composition. In turn, transcription factor expression is modulated by extrinsic signals from patterning centers and adjacent cells and by intrinsic signals distributed asymmetrically within progenitors and daughter cells. Together, the new findings provide a coherent framework for understanding cortical neurogenesis.

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References

  1. Meinecke D. L. and Peters A. (1987) GABA immunoreactive neurons in rat visual cortex. J. Comp. Neurol. 261, 388–404.

    PubMed  CAS  Google Scholar 

  2. Hendry S. H. C., Schwark H. D., Jones E. G., and Yan J. (1987) Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J. Neurosci. 7, 1503–1519.

    PubMed  CAS  Google Scholar 

  3. Peduzzi J. D. (1988) Genesis of GABA-immunoreactive neurons in the ferret visual cortex. J. Neurosci. 8, 920–931.

    PubMed  CAS  Google Scholar 

  4. Anderson S. A., Eisenstat D. D., Shi L., and Rubenstein J. L. R. (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474–476.

    PubMed  CAS  Google Scholar 

  5. Tan S.-S., Kalloniatis M., Sturm K., Tam P. P., Reese B. E., and Faulkner-Jones B. (1998) Separate progenitors for radial and tangenital cell dispersion during development of the cerebral neocortex. Neuron 21, 295–304.

    PubMed  CAS  Google Scholar 

  6. Marín O. and Rubenstein J. L. R. (2001) A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 2, 780–790.

    PubMed  Google Scholar 

  7. Schuurmans C. and Guillemot F. (2002) Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr. Opin. Neurobiol. 12, 26–34.

    PubMed  CAS  Google Scholar 

  8. Job C. and Tan S.-S. (2003) Constructing the mammalian neocortex; the role of intrinsic factors. Dev. Biol. 257, 221–232.

    PubMed  CAS  Google Scholar 

  9. Fishell G. and Kriegstein A. R. (2003) Neurons from radial glia: the consequences of asymmetric inheritance. Curr. Opin. Neurobiol. 13, 34–41.

    PubMed  CAS  Google Scholar 

  10. Rakic P. (2003a) Elusive radial glial cells: historical and evolutionary perspective. Glia 43, 19–32.

    PubMed  Google Scholar 

  11. Rakic P. (2003b) Developmental and evolutionary adaptations of cortical radial glia. Cereb. Cortex 13, 541–549.

    PubMed  Google Scholar 

  12. Cajal, S. Ramón y (1899, 1904, 1909, 1911) Histology of the Nervous System. (Translated from the French version of the original Spanish by Swanson N. and Swanson L. W.) New York: Oxford University Press 1995), Volume 2, p. 697.

    Google Scholar 

  13. Boulder Committee (1970) Embryonic vertebrate central nervous system: revised terminology. Anat. Rec. 166, 257–261.

    Google Scholar 

  14. Levitt P., Cooper M. L., and Rakic P. (1981) Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J. Neurosci. 1, 27–39.

    PubMed  CAS  Google Scholar 

  15. Levitt P., Cooper M. L., and Rakic P. (1983) Early divergence and changing proportions of neuronal and glial precursor cells in the primate cerebral ventricular zone. Dev. Biol. 96, 472–484.

    PubMed  CAS  Google Scholar 

  16. Rakic P. (1988) Specification of cerebral cortical areas. Science 241, 170–176.

    PubMed  CAS  Google Scholar 

  17. Smart J. H. M. (1973) Proliferative characteristics of the ependymal layer during the early development of the mouse neocortex: a pilot study based on recording the number, location and plane of cleavage of mitotic figures. J. Anat. 116, 67–91.

    PubMed  CAS  Google Scholar 

  18. Takahashi T., Nowakowski R. S., and Caviness V. S. Jr. (1995) Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J. Neurosci. 15, 6058–6068.

    PubMed  CAS  Google Scholar 

  19. Malatesta P., Hartfuss E., and Götz M. (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253–5263.

    PubMed  CAS  Google Scholar 

  20. Noctor S. C., Flint A. C., Weissman T. A., Dammerman R. S., and Kriegstein A. R. (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714–720.

    PubMed  CAS  Google Scholar 

  21. Miyata T., Kawaguchi A., Okano H., and Ogawa M. (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727–741.

    PubMed  CAS  Google Scholar 

  22. Malatesta P., Hack M. A., Hartfuss E., et al. (2003) Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37, 751–764.

    PubMed  CAS  Google Scholar 

  23. Anthony T. E., Klein C., Fishell G., and Heintz N. (2004) Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41, 881–890.

    PubMed  CAS  Google Scholar 

  24. Götz M. and Barde Y. A. (2005) Radial glial cells: defined and major intermediates between embryonic stem cells and CNS neurons. Neuron 46, 369–372.

    PubMed  Google Scholar 

  25. Noctor S. C., Martínez-Cerdeño V., Ivic L., and Kriegstein A. R. (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136–144.

    PubMed  CAS  Google Scholar 

  26. Haubensak W., Attardo A., Denk W., and Huttner W. B. (2004) Neurons arise in the basel neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl. Acad. Sci. USA. 101, 3196–3201.

    PubMed  CAS  Google Scholar 

  27. Miyata T., Kawaguchi A., Saito K., Kawano M., Muto T., and Ogawa M. (2004) Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131, 3133–3145.

    PubMed  CAS  Google Scholar 

  28. Kamel Y., Inagaki N., Nishizawa M., Tsutsumi O., Taketani Y., and Inagaki M. (1998) Visualization of mitotic radial glial lineage cells in the developing rat brain by Cdc2 kinase-phosphorylated vimentin. Glia 23, 191–199.

    Google Scholar 

  29. Tabata H. and Nakajima K. (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J. Neurosci. 23, 9996–10,001.

    PubMed  CAS  Google Scholar 

  30. Nadarajah B., Brunstrom J. E., Grutzendler J., Wong R. O. L., and Pearlman A. L. (2001) Two modes of migration in early development of the cerebral cortex. Nat. Neurosci. 4, 143–150.

    PubMed  CAS  Google Scholar 

  31. Kriegstein A. R. and Noctor S. C. (2004) Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 27, 392–399.

    PubMed  CAS  Google Scholar 

  32. Iacopetti P., Michelini M., Stuckmann I., Oback B., Aaku-Saraste E., and Huttner W. B. (1999) Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc. Natl. Acad. Sci. USA 96, 4639–4644.

    PubMed  CAS  Google Scholar 

  33. Cai L., Hayes N. L., Takahashi T., Caviness V. S. Jr., and Nowakowski R. S. (2002) Size distribution of retrovirally marked lineages matches predictions from population measurements of cell cycle behavior. J. Neurosci. Res. 69, 731–744.

    PubMed  CAS  Google Scholar 

  34. Hartfuss E., Galli R., Heins N., and Götz M. (2001) Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229, 15–30.

    PubMed  CAS  Google Scholar 

  35. Chenn A. and Walsh C. A. (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365–369.

    PubMed  CAS  Google Scholar 

  36. Tarabykin V., Stoykova A., Usman N., and Gruss P. (2001) Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128, 1983–1993.

    PubMed  CAS  Google Scholar 

  37. Roy K., Kuznicki K., Wu Q., et al. (2004) The Tlx gene regulates the timing of neurogenesis in the cortex. J. Neurosci. 24, 8333–8345.

    PubMed  CAS  Google Scholar 

  38. Nieto M., Monuki E. S., Tang H., et al. (2004) Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II–IV of the cerebral cortex. J. Comp. Neurol. 479, 168–180.

    PubMed  CAS  Google Scholar 

  39. Zimmer C., Tiveron M.-C., Bodmer R., and Cremer H. (2004) Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb. Cortex 14, 1408–1420.

    PubMed  Google Scholar 

  40. Britanova O., Akopov S., Lukyanov S., Gruss P., and Tarabykin V. (2005) Novel transcription factor Stab2 interacts with matrix attachment region DNA elements in a tissue-specific manner and demonstrates cell-type-dependent expression in the developing mouse CNS. Eur. J. Neurosci. 21, 658–668.

    PubMed  Google Scholar 

  41. Campbell K. (2005) Cortical neuron specification: it has its time and place. Neuron 46, 373–376.

    PubMed  CAS  Google Scholar 

  42. Stenman J., Yu R. T., Evans R. M., and Campbell K. (2003) Tlx and Pax6 co-operate genetically to establish the pallio-subpallial boundary in the embryonic mouse telencephalon. Development 130, 1113–1122.

    PubMed  CAS  Google Scholar 

  43. Hevner R. F., Shi L., Justice N., et al. (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29, 353–366.

    PubMed  CAS  Google Scholar 

  44. Muzio L., DiBenedetto B., Stoykova A., Boncinelli, E., Gruss P., and Mallamaci A. (2002) Conversion of cerebral cortex into basal ganglia in Emx2 -/-Pax6Sey/Sey double-mutant mice. Nat. Neurosci. 5, 737–745.

    PubMed  CAS  Google Scholar 

  45. Scardigli R., Bäumer N., Gruss P., Guillemot F., and Le Roux I. (2003) Direct and concentration-dependent regulation of the proneural gene Neurogenin 2 by Pax6. Development 130, 3269–3281.

    PubMed  CAS  Google Scholar 

  46. Grove E. A. and Fukuchi-Shimogori T. (2003) Generating the cerebral cortical area map. Annu. Rev. Neurosci. 26, 355–380.

    PubMed  CAS  Google Scholar 

  47. Zaki P. A., Quinn J. C., and Price D. J. (2003) Mouse models of telencephalic development. Curr. Opin. Genet. Devel. 13, 423–437.

    CAS  Google Scholar 

  48. Shimogori, T., Banuchi V., Ng H. Y., Strauss J. B., Grove E. A. (2004) Embryonic signaling centers expressing BMP, WNT and FGF proteins interact to pattern the cerebral cortex. Development 131, 5639–5647.

    PubMed  CAS  Google Scholar 

  49. Bishop K. M., Goudreau G., and O'Leary D. D. M. (2000_ Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 288, 344–349.

    PubMed  CAS  Google Scholar 

  50. Hamasaki T., Leingärtner A., Ringstedt T., and O'Leary D. D. M. (2004) EMX2 regulates size and positioning of the primary sensory and motor areas in neocortex by direct specification of cortical progenitors. Neuron 43, 359–372.

    PubMed  CAS  Google Scholar 

  51. Ross S. F., Greenberg M. E., and Stiles C. D. (2003) Basic helix-loop-helix factors in cortical development. Neuron 39, 13–25.

    PubMed  CAS  Google Scholar 

  52. Sun Y., Nadal-Vicens M., Misono S., et al. (2001) Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104, 365–376.

    PubMed  CAS  Google Scholar 

  53. Heins N., Cremisi F., Malatesta P., et al. (2001) Emx2 promotes symmetric cell divisions and a multipoten tial fate in precursors from the cerebral cortex. Mol. Cell. Neurosci. 18, 485–502.

    PubMed  CAS  Google Scholar 

  54. Heins N., Malatesla P., Cecconi F., et al. (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5, 308–315.

    PubMed  CAS  Google Scholar 

  55. Hirabayashi Y., Itoh Y., Tabata H., et al. (2004) The Wnt/β-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131, 2791–2801.

    PubMed  CAS  Google Scholar 

  56. McConnell S. K. and Kaznowski C. E. (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254, 282–285.

    PubMed  CAS  Google Scholar 

  57. McConnell S. K. (1995) Constructing the cerebral cortex: neurogenesis and fate determination. Neuron 15, 761–768.

    PubMed  CAS  Google Scholar 

  58. Hasegawa H., Ashigaki S., Takamatsu M., et al. (2004) Laminar patterning in the developing neocortex by temporally coordinated fibroblast growth factor signaling. J. Neurosci. 24, 8711–8719.

    PubMed  CAS  Google Scholar 

  59. Hanashima C., Li, S. C., Shen L., Lai E., and Fishell G. (2004) Foxg1 suppresses early cortical cell fate. Science 303, 56–59.

    PubMed  CAS  Google Scholar 

  60. Englund C., Fink A., Lau C., et al. (2005) Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25, 247–251.

    PubMed  CAS  Google Scholar 

  61. Hevner R. F., Daza R. A. M., Rubenstein J. L. R., Stunnenberg H., Olavarria J. F., and Englund C. (2003) Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev. Neurosci. 25, 139–151.

    PubMed  CAS  Google Scholar 

  62. Angevine J. B. and Sidman R. L. (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192, 766–768.

    PubMed  Google Scholar 

  63. Rakic P. (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183, 425–427.

    PubMed  CAS  Google Scholar 

  64. Takahashi T., Goto T., Miyama S., Nowakowski R. S., and Caviness V. S. Jr. (1999) Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J. Neurosci. 19, 10,357–10,371.

    CAS  Google Scholar 

  65. Pearson B. J. and Doe C. Q. (2004) Specification of temporal identity in the developing nervous system. Annu. Rev. Cell Dev. Biol. 20, 619–647.

    PubMed  CAS  Google Scholar 

  66. Zhong W. (2003) Diversifying neural, cells through order of birth and asymmetry of division. Neuron 37, 11–14.

    PubMed  CAS  Google Scholar 

  67. Mizutani K. and Saito T. (2005) Progenitors resume generating neurons after temporary inhibition of neurogenesis by Notch activation in the mammalian cerebral cortex. Development 132, 1295–1304.

    PubMed  CAS  Google Scholar 

  68. Muzio L. and Mallamaci A. (2005) Foxg1 cofines Cajal-Retzius neuronogenesis and hippocampal morphogenesis to the dorsomedial pallium. J. Neurosci. 25, 4435–4441.

    PubMed  CAS  Google Scholar 

  69. Takiguchi Hayashi K., Sekiguchi M., et al. (2004) Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J. Neurosci. 24, 2286–2295.

    PubMed  CAS  Google Scholar 

  70. Ferland R. J., Cherry T. J., Preware P. O., Morrisey E. E., and Walsh C. A. (2003) Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J. Comp. Neurol. 460, 266–279.

    PubMed  CAS  Google Scholar 

  71. Arimatsu Y., Ishida M., Kaneko T., Ichinose S., and Omori A. (2003) Organization and development of corticocortical associative neurons expressing the orphan nuclear receptor Nurr1. J. Comp. Neurol. 466, 180–196.

    PubMed  Google Scholar 

  72. Inoue K., Terashima T., Nishikawa T., and Takumi T. (2004) Fez1 is layer-specifically expressed in the adult mouse neocortex. Eur. J. Neurosci. 20, 2909–2916.

    PubMed  Google Scholar 

  73. Arlotta P., Molyneaux B. J., Chen, J., Inoue J., Kominami R., Macklis J. D. (2005) Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45, 207–221.

    PubMed  CAS  Google Scholar 

  74. Götz M., Stoykova A., and Gruss P. (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21, 1031–1044.

    PubMed  Google Scholar 

  75. Lee, J.-K., Cho J.-H., Hwang W.-S., Lee Y.-D., Reu D.-S., and Suh-Kim H. (2000) Expression of neuroD/BETA2 in mitotic and postmitotic neuronal cells during the development of the nervous system. Dev. Dyn. 217, 361–367.

    PubMed  CAS  Google Scholar 

  76. Nieto M., Schuurmans C., Britz O., and Guillemot F. (2001) Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29, 401–413.

    PubMed  CAS  Google Scholar 

  77. Yun K., Mantani A., Garel S., Rubenstein J., and Israel M. A. (2004) Id4 regulates neural progenitor proliferation and differentiation in vivo. Development 131, 5441–5448.

    PubMed  CAS  Google Scholar 

  78. Desai A. R. and McConnel S. K. (2000) Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127, 2863–2872.

    PubMed  CAS  Google Scholar 

  79. Gaiano N. and Fishell G. (2002) The role of notch in promoting glial and neural stem cell fates. Annu. Rev. Neurosci. 25, 471–490.

    PubMed  CAS  Google Scholar 

  80. Bohner A. P., Akers R. M., and McConnell S. K. (1997) Induction of deep layer cortical neurons in vitro. Development 124, 915–923.

    PubMed  CAS  Google Scholar 

  81. Peterson P. H., Zhou K., Krauss S., and Zhong W. (2004) Continuing role for mouse Numb and Numbl in maintaining progenitor cells during cortical neurogenesis. Nat. Neurosci. 7, 803–811.

    Google Scholar 

  82. Kosodo Y., Röper K., Haubensak W., Marzesco A.-M., Corbeil D., and Huttner W. B. (2004) Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuropithelial cells. EMBO J. 23, 2314–2324.

    PubMed  CAS  Google Scholar 

  83. Sun Y., Goderie S. K., and Temple S. (2005) Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron 45, 873–886.

    PubMed  CAS  Google Scholar 

  84. Schuurmans C., Armant O., Nieto M., et al. (2004) Sequential phases of cortical specification involve Neurogenin-dependent and-independent pathways. EMBO J. 23, 2892–2902.

    PubMed  CAS  Google Scholar 

  85. Toresson H., Potter S. S., and Campbell K. (2000) Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127, 4361–4371.

    PubMed  CAS  Google Scholar 

  86. Yun K., Potter S., and Rubenstein J. L. R. (2001) Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128, 193–205.

    PubMed  CAS  Google Scholar 

  87. Estivill-Torrus G., Pearson H., van Heyningen V., Price D. J., Rashbass P. (2002) Pax6 is required to regulate the cell cycle and the rate of progression from symmetrical to asymmetrical division in mammalian cortical progenitors. Development 129, 455–466.

    PubMed  CAS  Google Scholar 

  88. Haubst N., Berger J., Radjendirane V., et al. (2004) Molecular dissection of Pax6 function: the specific roles of the paired domain and homeodomain in brain development. Development 131, 6131–6140.

    PubMed  CAS  Google Scholar 

  89. Ohtsuka T., Sakamoto M., Guillemot F., and Kageyama R. (2001) Roles of the basic helix-loop-helix genes Hes1 and Hes5 in expansion of neural stem cells of the developping brain. J. Biol. Chem. 276, 30,467–30,474.

    CAS  Google Scholar 

  90. Makamura Y., Sakakibara S., Miyata T., et al. (2000) The bHLH gene Hes1 as a repressor of the neuronal commitment of CNS stem cells. J. Neurosci. 20, 283–293.

    Google Scholar 

  91. Hatakeyama J., Bessho Y., Katoh K., et al. (2004) Hes genes regulate size, shape and histogenesis of the nervous system by control of to genesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131, 5539–5550.

    PubMed  CAS  Google Scholar 

  92. Lyden D., Young A. Z., Zagzag D., et al. (1999) Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401, 670–677.

    PubMed  CAS  Google Scholar 

  93. Bishop K. M., Garel S., Nakagawa Y., Rubenstein J. L. R., and O'Leary D. D. M. (2003) Emx1 and Emx2 cooperate to regulate cortical size, lamination, neuronal differentiation, development of cortical efferents, and thalamocortical pathfinding. J. Comp. Neurol. 457, 345–360.

    PubMed  CAS  Google Scholar 

  94. Hodge R. D., D'Ercole A. J., and O'Kusky J. R. (2004) Insulin-like growth factor-I accelerates the cell cycle by decreasing G1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J. Neurosci. 24, 10,201–10,210.

    CAS  Google Scholar 

  95. Hodge R. D., D'Ercole A. J., and O'Kusky J. R. (2005) Increased expression of insulin-like growth factor-I (IGF-1) during embryonic development produces neocortical overgrowth with differentially greater effects on specific cytoarchitectonic areas and cortical layers. Brain Res. Dev. Brain Res. 154, 227–237.

    PubMed  CAS  Google Scholar 

  96. Ross M. E. and Walsh C. A. (2001) Human brain malformations and their lessons for neuronal migration. Annu. Rev. Neurosci. 24, 1041–1070.

    PubMed  CAS  Google Scholar 

  97. Ellison-Wright Z., Heyman I., Frampton I., et al. (2004) Heterozygous PAX6 mutation, adult brain structure and fronto-striato-thalamic function in a human family. Eur. J. Neurosci. 19, 1505–1512.

    PubMed  Google Scholar 

  98. Chan C.-H., Godinho L. N., Thomaidou D., Tan S.-S., Gulinsano M., and Parnavelas J. G. (2001) Einx1 is a marker for pyramidal neurons of the cerebral cortex. Cereb. Cortx 11, 1191–1198.

    CAS  Google Scholar 

  99. Mallamaci A., Iannone R., Briata P., et al. (1998) EMX2 protein in the developing mouse brain and olfactory area. Mech. Dev. 77, 165–172.

    PubMed  CAS  Google Scholar 

  100. Cecchi C. and Boncinelli E. (2000) Emx homeogenes and mouse brain development. Trends Neurosci. 23, 347–352.

    PubMed  CAS  Google Scholar 

  101. Allen T. and Lobe C. G. (1999) A comparison of Notch, Hes and Grg expression during murine embryonic and post-natal development. Cell. Mol. Biol. 45, 687–708.

    PubMed  CAS  Google Scholar 

  102. Kawaguchi A., Ogawa M., Saito K., Matsuzaki F., Okano H., and Miyata T. (2004) Differential expression of Pax6 and Ngn2 between pairgenerated cortical neurons. J. Neurosci. Res. 78, 784–795.

    PubMed  CAS  Google Scholar 

  103. Fode C., Ma Q., Casarosa S., Ang S.-L., Anderson D. J., and Guillemot F. (2000) A role for neural determination genes in specifying the dorsoventral indentity of telencephalic neurons. Genes Devel. 14, 67–80.

    PubMed  CAS  Google Scholar 

  104. Jen Y., Manova K., and Benezra R. (1997) Each member of the Id gene family exhibits a unique expression pattern in mouse gastrulation and neurogenesis. Dev. Dyn. 208, 92–106.

    PubMed  CAS  Google Scholar 

  105. Schwab M. H., Druffel-Augustin S., Gass P., et al. (1998) Neuronal basic helix-loop-helix proteins (NEX, neuroD, NDRF): spatiotemporal expression and targeted disruption of the NEX gene in transgenic mice. J. Neurosci. 18, 1408–1418.

    PubMed  CAS  Google Scholar 

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Hevner, R.F. From radial glia to pyramidal-projection neuron. Mol Neurobiol 33, 33–50 (2006). https://doi.org/10.1385/MN:33:1:033

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