Evolution and development of the mammalian cerebral cortex

Brain, Behavior and Evolution

Volumn 83, Issue 2, 2014, Pages 126-139

  Molnár, Zoltán ^a   Kaas, Jon H ^b   De Carlos, Juan A ^d   Hevner, Robert F ^c   Lein, Ed ^a   Němec, Pavel ^e  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b VANDERBILT UNIVERSITY   (United States)

^c Center for Integrative Brain Research   (United States)

^d INSTITUTO CAJAL   (Spain)

^e CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Comparative transcriptomics; Cortical arealization; Cortical neurogenesis; Intermediate progenitors; Subterranean vision; Tangential neuronal migration

Indexed keywords

ANIMAL; BRAIN CORTEX; COMPARATIVE STUDY; CYTOLOGY; EVOLUTION; GROWTH, DEVELOPMENT AND AGING; HUMAN; MAMMAL; NEOCORTEX; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT;

ANIMALS; BIOLOGICAL EVOLUTION; CEREBRAL CORTEX; HUMANS; MAMMALS; NEOCORTEX; NEUROGENESIS; NEURONS;

MAMMALIA; PRIMATES;

EID: 84899870753     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000357753     Document Type: Article

References (104)

1. Abrahams BS, Tentler D, Perederiy JV, Oldham MC, Coppola G, Geschwind DH (2007): Genome-wide analyses of human perisylvian cerebral cortical patterning. Proc Natl Acad Sci USA 104: 17849-17854.
2. Anderson SA, Eisenstat DD, Shi L, Rubenstein JLR (1997): Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278: 474-476.
3. Angevine JB, Sidman RL (1961): Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192: 766-768.
4. Assimacopoulos S, Kao T, Issa NP, Grove EA (2012): Fibroblast growth factor 8 organizes the neocortical area map and regulates sensory map topography. J Neurosci 32: 7191-7201.
5. Ayoub AE, Oh S, Xie Y, Leng J, Cotney J, Dominguez MH, Noonan JP, Rakic P (2011): Transcriptional programs in transient embryonic zones of the cerebral cortex defined by highresolution mRNA sequencing. Proc Natl Acad Sci USA 108: 14950-14955.
6. Azevedo FAC, Carvalho LRB, Grinberg LT, Farfel JM, Ferretti REL, Leite REP, Filho WJ, Lent R, Herculano-Houzel S (2009): Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol 513: 532-541.
7. Belgard TG, Marques AC, Oliver PL, Abaan HO, Sirey TM, Hoerder-Suabedissen A, García-Moreno F, Molnár Z, Margulies EH, Ponting CP (2011): A transcriptomic atlas of mouse neocortical layers. Neuron 71: 605-616.
8. Belgard TG, Montiel JF, Wang WZ, García-Moreno F, Margulies EH, Ponting CP, Molnár Z (2013): Adult pallium transcriptomes surprise in not reflecting predicted homologies across diverse chicken and mouse pallial sectors. Proc Natl Acad Sci USA 110:13150-13155.
9. Bernard A, Lubbers LS, Tanis KQ, Luo R, Podtelezhnikov AA, Finney EM, McWhorter MM, Serikawa K, Lemon T, Morgan R, Copeland C, Smith K, Cullen V, Davis-Turak J, Lee CK, Sunkin SM, Loboda AP, Levine DM, Stone DJ, Hawrylycz MJ, Roberts CJ, Jones AR, Geschwind DH, Lein ES (2012): Transcriptional architecture of the primate neocortex. Neuron 73: 1083-1099.
10. Bronchti G, Heil P, Sadka R, Hess A, Scheich H, Wollberg Z (2002): Auditory activation of 'visual' cortical areas in the blind mole rat ( Spalax ehrenbergi ). Eur J Neurosci 16: 311-329.
11. Cameron DA, Middleton FA, Chenn A, Olson EC (2012): Hierarchical clustering of gene expression patterns in the Eomes+ lineage of excitatory neurons during early neocortical development. BMC Neurosci 13: 90.
12. Catania KC, Kaas JH (1995): Organization of the somatosensory cortex of the star-nosed mole. J Comp Neurol 351: 549-567.
13. Catania KC, Remple MS (2002): Somatosensory cortex dominated by the representation of teeth in the naked mole-rat brain. Proc Natl Acad Sci USA 99: 5692-5697.
14. Ceci ML, López-Mascaraque L, de Carlos JA (2010): The influence of the environment on Cajal-Retzius cell migration. Cereb Cortex 20:2348-2360.
15. Ceci ML, Pedraza M, de Carlos JA (2012): The embryonic septum and ventral pallium, new sources of olfactory cortex cells. PLoS One 7:e44716.
16. Cheung AF, Kondo S, Abdel-Mannan O, Chodroff RA, Sirey TM, Bluy LE, Webber N, De-Proto J, Karlen SJ, Krubitzer L, Stolp HB, Saunders NR, Molnár Z (2010): The subventricular zone is the developmental milestone of a 6-layered neocortex: comparisons in metatherian and eutherian mammals. Cereb Cortex 20: 1071-1081.
17. Clowry G, Molnár Z, Rakic P (2010): Renewed focus on the developing human neocortex. J Anat 217: 276-288.
18. Cobos I, Puelles L, Martínez S (2001): The avian telencephalic subpallium originates inhibitory neurons that invade tangentially the pallium (dorsal ventricular ridge and cortical areas). Dev Biol 239: 30-45.
19. Colantuoni C, Lipska BK, Ye T, Hyde TM, Tao R, Leek JT, Colantuoni EA, Elkahloun AG, Herman MM, Weinberger DR, Kleinman JE (2011): Temporal dynamics and genetic control of transcription in the human prefrontal cortex. Nature 478: 519-523.
20. Collins CD, Airey DC, Young NA, Leitch DB, Kaas JH (2010): Neuron densities vary across and within cortical areas in primates. Proc Natl Acad Sci USA 107: 15927-15932.
21. Cooper HM, Herbin M, Nevo E (1993): Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi. J Comp Neurol 328: 313-350.
22. Crish SD, Dengler-Crish CM, Catania KC (2006): Central visual system of the naked mole-rat (Heterocephalus glaber). Anat Rec A Discov Mol Cell Evol Biol 288: 205-212.
23. De Carlos JA, O'Leary DDM (1992): Growth and targeting of subplate axons and establishment of major cortical pathways. J Neurosci 12: 1194-1211.
24. De Carlos JA, López-Mascaraque L, Valverde F (1996): Dynamics of cell migration from the lateral ganglionic eminence in the rat. J Neurosci 16: 6146-6156.
25. Dehay C, Kennedy H (2007): Cell-cycle control and cortical development. Nat Rev Neurosci 8: 438-450.
26. Elsen GE, Hodge RD, Bedogni F, Daza RA, Nelson BR, Shiba N, Reiner SL, Hevner RF (2013): The protomap is propagated to cortical plate neurons through an Eomes-dependent intermediate map. Proc Natl Acad Sci USA 110: 4081-4086.
27. Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF (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.
28. Franco SJ, Gil-Sanz C, Martinez-Garay I, Espinosa A, Harkins-Perry SR, Ramos C, Müller U (2012): Fate-restricted neural progenitors in the mammalian cerebral cortex. Science 337: 746-749.
29. Gal JS, Morozov YM, Ayoub AE, Chatterjee M, Rakic P, Haydar TF (2006): Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J Neurosci 26: 1045-1056.
30. García-Moreno F, López-Mascaraque L, De Carlos JA (2007): Origins and migratory routes of murine Cajal-Retzius cells. J Comp Neurol 500: 419-432.
31. García-Moreno F, López-Mascaraque L, de Carlos JA (2008): Early telencephalic migration topographically converging into the olfactory cortex. Cereb Cortex 18: 1239-1252.
32. García-Moreno F, Vasistha NA, Trevia N, Bourne JA, Molnár Z (2012): Compartmentalization of cerebral cortical germinal zones in a lissencephalic primate and gyrencephalic rodent. Cereb Cortex 22: 482-492.
33. Grant E, Hoerder-Suabedissen A, Molnár Z (2012): Development of the corticothalamic projections. Front Neurosci 6: 53.
34. Haim A, Heth G, Pratt H, Nevo E (1983): Photoperiodic effects on thermoregulation in a 'blind' subterranean mammal. J Exp Biol 107: 59-64.
35. Hansen DV, Rubenstein JL, Kriegstein AR (2011): Deriving excitatory neurons of the neocortex from pluripotent stem cells. Neuron 70: 645-660.
36. Haubensak W, Attardo A, Denk W, Huttner WB (2004): Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 101: 3196-3201.
37. Hawrylycz M, Lein E, Guillozet-Bongaarts AL, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA, van de Lagemaat LN, Smith KA, Ebbert A, Riley ZL, Abajian C, Beckmann CF, Bernard A, Bertagnolli D, Boe AF, Cartagena PM, Chakravarty MM, Chapin M, Chong J, Dalley RA, Daly BD, Dang C, Datta S, Dee N, Dolbeare TA, Faber V, Feng D, Fowler DR, Goldy J, Gregor BW, Haradon Z, Haynor DR, Hohmann JG, Horvath S, Howard RE, Jeromin A, Jochim JM, Kinnunen M, Lau C, Lazarz ET, Lee C, Lemon TA, Li L, Li Y, Morris JA, Overly CC, Parker PD, Parry SE, Reding M, Royall JJ, Schulkin J, Sequeira PA, Slaughterbeck CR, Smith SC, Sodt AJ, Sunkin SM, Swanson BE, Vawter MP, Williams D, Wohnoutka P, Zielke HR, Geschwind DH, Hof PR, Smith SM, Koch C, Grant SG, Jones AR (2012): An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489: 391-399.
38. Heil P, Bronchti G, Wollenberg Z, Scheich H (1991): Invasion of visual cortex by the auditory system in the naturally blind mole rat. Neuroreport 2: 735-738.
39. Henry EC, Remple MS, O'Riain MJ, Catania KC (2006): Organization of somatosensory cortical areas in the naked mole-rat ( Heterocephalus glaber ). J Comp Neurol 495: 434-452.
40. Herculano-Houzel S, Collins C, Wong P, Kaas JH (2007): Cellular scaling rules for primate brains. Proc Natl Acad Sci USA 104: 3562-3567.
41. Hevner RF (2006): From radial glia to pyramidalprojection neuron: transcription factor cascades in cerebral cortex development. Mol Neurobiol 33: 33-50.
42. Hevner RF, Haydar TF (2012): The (not necessarily) convoluted role of basal radial glia in cortical neurogenesis. Cereb Cortex 22: 465-468.
43. Hevner RF, Hodge RD, Daza RA, Englund C (2006): Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci Res 55: 223-233.
44. Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R (2010): Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci 30: 3489-3498.
45. Itoh Y, Moriyama Y, Hasegawa T, Endo TA, Toyoda T, Gotoh Y (2013): Scratch regulates neuronal migration onset via an epithelialmesenchymal transition-like mechanism. Nat Neurosci 16: 416-425.
46. Johnson MB, Kawasawa YI, Mason CE, Krsnik Z, Coppola G, Bogdanovi? D, Geschwind DH, Mane SM, State MW, Sestan N (2009): Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 62: 494-509.
47. Kaas JH (2013): The evolution of brains from early mammals to humans. Wiley Interdiscip Rev Cogn Sci 4: 33-45.
48. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, Li M, Sousa AM, Pletikos M, Meyer KA, Sedmak G, Guennel T, Shin Y, Johnson MB, Krsnik Z, Mayer S, Fertuzinhos S, Umlauf S, Lisgo SN, Vortmeyer A, Weinberger DR, Mane S, Hyde TM, Huttner A, Reimers M, Kleinman JE, Sestan N (2011): Spatio-temporal transcriptome of the human brain. Nature 478: 483-489.
49. Kawaguchi A, Ikawa T, Kasukawa T, Ueda HR, Kurimoto K, Saitou M, Matsuzaki F (2008): Single-cell gene profiling defines differential progenitor subclasses in mammalian neurogenesis. Development 135: 3113-3124.
50. Kelava I, Reillo I, Murayama AY, Kalinka AT, Stenzel D, Tomancak P, Matsuzaki F, Lebrand C, Sasaki E, Schwamborn JC, Okano H, Huttner WB, Borrell V (2012): Abundant occurrence of basal radial glia in the subventricular zone of embryonic neocortex of a lissencephalic primate, the common marmoset Callithrix jacchus. Cereb Cortex 22: 469-481.
51. Kott O, Šumbera R, N?mec P (2010): Light perception in two strictly subterranean rodents: life in the dark or blue? PLoS One 5:e11810.
52. Kowalczyk T, Pontious A, Englund C, Daza RA, Bedogni F, Hodge R, Attardo A, Bell C, Huttner WB, Hevner RF (2009): Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex 19: 2439-2450.
53. Kriegstein A, Noctor S, Martínez-Cerdeno V (2006): Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7: 883-890.
54. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR (2007): Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176.
55. Lui JH, Hansen DV, Kriegstein AR (2011): Development and evolution of the human neocortex. Cell 146: 18-36.
56. Marín-Padilla M (1971): Early prenatal ontogenesis of the cerebral cortex (neocortex) of the cat (Felis domestica). A Golgi study. I. The primordial neocortical organization. Z Anat Entwicklungsgesch 134: 117-145.
57. Martinez-Cerdeno V, Noctor SC, Kriegstein AR (2006): The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. Cereb Cortex 16:i152-i161.
58. McConnell SK, Ghosh A, Shatz CJ (1989): Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245: 978-982.
59. Métin C, Alvarez C, Moudoux D, Vitalis T, Pieau C, Molnár Z (2007): Conserved pattern of tangential neuronal migration during forebrain development. Development 134: 2815-2827.
60. Miquelajáuregui A, Valera-Echavarría A, Ceci ML, García-Moreno F, Ricano I, Hoang K, Frade-Pérez D, Portera-Cailliau C, Tamariz E, De Carlos JA, Westphal H, Zhao Y (2010): LIM-homeobox gene Lhx5 is required for normal development of Cajal-Retzius cells. J Neurosci 30: 10551-10562.
61. Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M (2004): Asymmetric production of surface-dividing and non-surfacedividing cortical progenitor cells. Development 131: 3133-3145.
62. Molnár Z (2011): Evolution of cerebral cortical development. Brain Behav Evol 78: 94-107.
63. Molnár Z, Belgard TG (2012): Transcriptional profiling of layers of the primate cerebral cortex. Neuron 73:1053-1055.
64. Molnár Z, Butt SJB (2013): Best-laid schemes for interneuron origin of mice and men. Nat Neurosci 16: 1512-1514.
65. Molnár Z, Clowry G (2012): Cerebral cortical development in rodents and primates. Prog Brain Res 195: 45-70.
66. Molnár Z, Garel S, López-Bendito G, Maness P, Price DJ (2012): Mechanisms controlling the guidance of thalamocortical axons through the embryonic forebrain. Eur J Neurosci 35: 1573-1585.
67. Murphy WJ, Pevzner PA, O'Brien JO (2004): Mammalian phylogenomics comes of age. Trends Genet 20: 631-639.
68. Necker R, Rehkämper G, Nevo E (1992): Electrophysiological mapping of body representation in the cortex of the blind mole rat. Neuroreport 3: 505-508.
69. Nelson BR, Hodge RD, Bedogni F, Hevner RF (2013): Dynamic interactions between intermediate neurogenic progenitors and radial glia in embryonic mouse neocortex: potential role in Dll1-Notch signaling. J Neurosci 33: 9122-9139.
70. N?mec P, Altmann J, Marhold S, Burda H, Oelschläger HHA (2001): Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal. Science 294: 366-368.
71. N?mec P, Burda H, Peichl L 2004): Subcortical visual system of the African mole-rat Cryptomys anselli: to see or not to see? Eur J Neurosci 20 757-768.
72. N?mec P, Cvekova P, Benada O, Wielkopolska E, Olkowicz S, Turlejski K, Burda H, Bennett NC, Peichl L (2008): The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): retina, subcortical visual nuclei and primary visual cortex. Brain Res Bull 75: 356-364.
73. N?mec P, Cvekova P, Burda H, Benada O, Peichl L (2007): Visual systems and the role of vision in subterranean rodents: diversity of retinal properties and visual system designs; in Begall S, Burda H, Schleich CE (eds): Subterranean Rodents: News from Underground. Heidelberg, Springer, pp 129-160.
74. Nevo E (1999): Mosaic Evolution of Subterranean Mammals: Regression, Progression and Global Convergence. Oxford, Oxford University Press.
75. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001): Neurons derived from radial glial cells establish radial units in neocortex. Nature 409: 714-720.
76. Noctor SC, Martínez-Cerdeno V, Ivic L, Kriegstein AR (2004): Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7: 136-44.
77. Nonaka-Kinoshita M, Reillo I, Artegiani B, Martínez- Martínez MA, Nelson M, Borrell V, Calegari F (2013): Regulation of cerebral cortex size and folding by expansion of basal progenitors. EMBO J 32: 1817-1828.
78. Oelschläger HHA, Nakamura M, Herzog M, Burda H (2000): Visual system labeled by c-Fos immunohistochemistry after light exposure in the 'blind' subterranean Zambian mole-rat (Cryptomys anselli). Brain Behav Evol 55: 209-220.
79. O'Leary DDM, Chou SJ, Sahara S (2007): Area patterning of the mammalian cortex. Neuron 56: 252-269.
80. Pedraza M, De Carlos JA (2012): A further analysis of olfactory cortex development. Front Neuroanat 6: 35.
81. Pedraza M, Hoerder-Suabedissen A, Molnar Z, De Carlos JA (2014): A new extracortical origin of some murine subplate cell population. PNAS (in review).
82. Peichl L, N?mec P, Burda H (2004): Unusual cone and rod properties in subterranean African mole-rats (Rodentia, Bathyergidae). Eur J Neurosci 19: 1545-1558.
83. Pimeisl I-M, Tanriver Y, Daza RA, Vauti F, Hevner RF, Arnold H-H, Arnold SJ (2013): Generation and characterization of a tamoxifen-inducible Eomes CreER mouse line. Genesis 51: 725-733.
84. Pontious A, Kowalczyk T, Englund C, Hevner RF (2008): Role of intermediate progenitor cells in cerebral cortex development. Dev Neurosci 30: 24-32.
85. Rakic P (1972): Mode of cell migration to the superficial layers of the fetal monkey neocortex. J Comp Neurol 145: 61-84.
86. Rakic P (1988): Specification of cerebral cortical areas. Science 241: 170-176.
87. Rash BG, Tomasi S, Lim HD, Suh CY, Vaccarino FM (2013): Cortical gyrification induced by fibroblast growth factor 2 in the mouse brain. J Neurosci 33: 10802-10814.
88. Reillo I, de Juan Romero C, García-Cabezas MÁ, Borrell V (2011): A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb Cortex 21: 1674-1694.
89. Sasaki S, Tabata H, Tachikawa K, Nakajima K (2008): The cortical subventricular zone-specific molecule Svet1 is part of the nuclear RNA coded by the putative netrin receptor gene Unc5d and is expressed in multipolar migrating cells. Mol Cell Neurosci 38: 474-483.
90. Shimogori T, Grove EA (2005): Fibroblast growth factor 8 regulates neocortical guidance of area-specific thalamic innervation. J Neurosci 25: 6550-6560.
91. Smart IH, Dehay C, Giroud P, Berland M, Kennedy H (2002): Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 12: 37-53.
92. Stahl R, Walcher T, De Juan Romero C, Pilz GA, Cappello S, Irmler M, Sanz-Aquela JM, Beckers J, Blum R, Borrell V, Götz M (2013): Trnp1 regulates expansion and folding of the mammalian cerebral cortex by control of radial glial fate. Cell 153: 535-49.
93. Tabata H, Nakajima K (2003): Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 23: 9996-10001.
94. Tamamaki N, Fujimori KE, Takauji R (1997): Origin and routes of tangentially migrating neurons in the developing neocortical intermediate zone. J Neurosci 17: 8313-8323.
95. Tamamaki N, Nakamura K, Okamoto K, Kaneko T (2001): Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci Res 41: 51-60.
96. Tarabykin V, Stoykova A, Usman N, Gruss P (2001): Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128: 1983-1893.
97. Tuorto F, Alifragis P, Failla V, Parnavelas JG, Gulisano M (2003): Tangential migration of cells from the basal to the dorsal telencephalic regions in the chick. Eur J Neurosci 18: 3388-3393.
98. Tyler WA, Haydar TF (2013): Multiplex genetic fate mapping reveals a novel route of neocortical neurogenesis, which is altered in the Ts65Dn mouse model of Down syndrome. J Neurosci 33: 5106-5119.
99. Vasistha NA, Vasistha NA, Garcia-Moreno F, Arora S, Cheung AFP, Arnold SJ, Robertson EJ, Molnár Z (2014): Cortical and clonal contribution of Tbr2 expressing progenitors in the developing mouse brain. Cereb Cortex (in review).
100. Walsh C, Cepko CL (1993): Clonal dispersion in proliferative layers of developing cerebral cortex. Nature 362: 632-635.
101. Wong P, Collins CE, Kaas JH (2010): Overview of sensory systems of Tarsius. Int J Primatol 31: 1002-1031.
102. Yoon KJ, Koo BK, Im SK, Jeong HW, Ghim J, Kwon MC, Moon JS, Miyata T, Kong YY (2008): Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron 58: 519-531.
103. Zeng H, Shen EH, Hohmann JG, Oh SW, Bernard A, Royall JJ, Glattfelder KJ, Sunkin SM, Morris JA, Guillozet-Bongaarts AL, Smith KA, Ebbert AJ, Swanson B, Kuan L, Page DT, Overly CC, Lein ES, Hawrylycz MJ, Hof PR, Hyde TM, Kleinman JE, Jones AR (2012): Large-scale cellular-resolution gene profiling in human neocortex reveals species-specific molecular signatures. Cell 149: 483-496.
104. Zimmer C, Tiveron MC, Bodmer R, 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.