Abstract
Extensive radiation of extant amniotes could have been achieved by the innovation of several unique characteristics in the body plans of their ancestors. In particular, distinct brain regions were enlarged independently to acquire similar functional properties in different amniote lineages. The neocortex and dorsal ventricular ridge (DVR) are a typical case of such parallel brain evolution in mammalian and reptilian lineages. Although these structures have distinct developmental origins, striking functional similarities in the neocortex and DVR have led to long-lasting arguments regarding their evolutionary development from ancestral amniotes. Here, we introduce morphological, neuroanatomical, and developmental aspects of the convergent and divergent features of the neocortex and DVR in amniotes. Furthermore, we discuss possible genetic changes that provided these remarkable brain structures, with special interest in the role of the Pax6 gene, an essential regulator of neural stem/progenitor cell dynamics. Comparative functional analyses of the regulatory genes required for pallial development will provide significant insights into the evolutionary origin of the hallmarks of mammalian and reptilian brains.
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References
Aboitiz F, Zamorano F (2013) Neural progenitors, patterning and ecology in neocortical origins. Front Neuroanat 7:38. doi:10.3389/fnana.2013.00038
Asami M, Pilz GA, Ninkovic J, Godinho L, Schroeder T, Huttner WB, Gotz M (2011) The role of Pax6 in regulating the orientation and mode of cell division of progenitors in the mouse cerebral cortex. Development 138(23):5067–5078. doi:10.1242/dev.074591
Assimacopoulos S, Grove EA, Ragsdale CW (2003) Identification of a Pax6-dependent epidermal growth factor family signaling source at the lateral edge of the embryonic cerebral cortex. J Neurosci 23(16):6399–6403
Belgard TG, Montiel JF, Wang WZ, Garcia-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(32):13150–13155. doi:10.1073/pnas.1307444110
Benton M, Gauthier J, Kluge A, Rowe TB (1988) The early evolution of the Amniota. In: Benton MJ (ed) The phylogeny and classification of the tetrapods. Clarendon, Oxford, pp 103–155
Bernier B, Bar I, D’Arcangelo G, Curran T, Goffinet AM (2000) Reelin mRNA expression during embryonic brain development in the chick. J Comp Neurol 422(3):448–463
Bielle F, Griveau A, Narboux-Neme N, Vigneau S, Sigrist M, Arber S, Wassef M, Pierani A (2005) Multiple origins of Cajal–Retzius cells at the borders of the developing pallium. Nat Neurosci 8(8):1002–1012. doi:10.1038/nn1511
Bielle F, Marcos-Mondejar P, Keita M, Mailhes C, Verney C, Nguyen Ba-Charvet K, Tessier-Lavigne M, Lopez-Bendito G, Garel S (2011) Slit2 activity in the migration of guidepost neurons shapes thalamic projections during development and evolution. Neuron 69(6):1085–1098. doi:10.1016/j.neuron.2011.02.026
Borrell V, Calegari F (2014) Mechanisms of brain evolution: regulation of neural progenitor cell diversity and cell cycle length. Neurosci Res 86:14–24. doi:10.1016/j.neures.2014.04.004
Bulter A, Hodos W (2005) Comparative vertebrate neuroanatomy: evolution and adaptation. Wiley, Hoboken
Cabrera-Socorro A, Hernandez-Acosta NC, Gonzalez-Gomez M, Meyer G (2007) Comparative aspects of p73 and Reelin expression in Cajal-Retzius cells and the cortical hem in lizard, mouse and human. Brain Res 1132(1):59–70. doi:10.1016/j.brainres.2006.11.015
Caric D, Gooday D, Hill RE, McConnell SK, Price DJ (1997) Determination of the migratory capacity of embryonic cortical cells lacking the transcription factor Pax-6. Development 124(24):5087–5096
Carney RS, Alfonso TB, Cohen D, Dai H, Nery S, Stoica B, Slotkin J, Bregman BS, Fishell G, Corbin JG (2006) Cell migration along the lateral cortical stream to the developing basal telencephalic limbic system. J Neurosci 26(45):11562–11574. doi:10.1523/JNEUROSCI.3092-06.2006
Carroll RL (1988) Vertebrate paleontology and evolution. Freeman, New York
Chan YF, Marks ME, Jones FC, Villarreal G Jr, Shapiro MD, Brady SD, Southwick AM, Absher DM, Grimwood J, Schmutz J, Myers RM, Petrov D, Jonsson B, Schluter D, Bell MA, Kingsley DM (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327(5963):302–305. doi:10.1126/science.1182213
Charvet CJ (2010) A reduced progenitor pool population accounts for the rudimentary appearance of the septum, medial pallium and dorsal pallium in birds. Brain Behav Evol 76(3-4):289–300. doi:10.1159/000322102
Charvet CJ, Striedter GF, Finlay BL (2011) Evo-devo and brain scaling: candidate developmental mechanisms for variation and constancy in vertebrate brain evolution. Brain Behav Evol 78(3):248–257. doi:10.1159/000329851
Cheung AF, Pollen AA, Tavare A, DeProto J, Molnár Z (2007) Comparative aspects of cortical neurogenesis in vertebrates. J Anat 211(2):164–176. doi:10.1111/j.1469-7580.2007.00769.x
Dugas-Ford J, Rowell JJ, Ragsdale CW (2012) Cell-type homologies and the origins of the neocortex. Proc Natl Acad Sci USA 109(42):16974–16979. doi:10.1073/pnas.1204773109
Estivill-Torrus G, Pearson H, van Heyningen V, Price DJ, 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(2):455–466
Fernandez AS, Pieau C, Reperant J, Boncinelli E, Wassef M (1998) Expression of the Emx-1 and Dlx-1 homeobox genes define three molecularly distinct domains in the telencephalon of mouse, chick, turtle and frog embryos: implications for the evolution of telencephalic subdivisions in amniotes. Development 125(11):2099–2111
Field DJ, Gauthier JA, King BL, Pisani D, Lyson TR, Peterson KJ (2014) Toward consilience in reptile phylogeny: miRNAs support an archosaur, not lepidosaur, affinity for turtles. Evol Dev 16(4):189–196. doi:10.1111/ede.12081
Fietz SA, Huttner WB (2011) Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr Opin Neurobiol 21(1):23–35. doi:10.1016/j.conb.2010.10.002
Frotscher M (1998) Cajal–Retzius cells, Reelin, and the formation of layers. Curr Opin Neurobiol 8(5):570–575
Galant R, Carroll SB (2002) Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415(6874):910–913. doi:10.1038/nature717
Georgala PA, Carr CB, Price DJ (2011) The role of Pax6 in forebrain development. Dev Neurobiol 71(8):690–709. doi:10.1002/dneu.20895
Goffinet AM, Daumerie C, Langerwerf B, Pieau C (1986) Neurogenesis in reptilian cortical structures: 3H-thymidine autoradiographic analysis. J Comp Neurol 243(1):106–116. doi:10.1002/cne.902430109
Gotz M, Stoykova A, Gruss P (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21(5):1031–1044
Griveau A, Borello U, Causeret F, Tissir F, Boggetto N, Karaz S, Pierani A (2010) A novel role for Dbx1-derived Cajal–Retzius cells in early regionalization of the cerebral cortical neuroepithelium. PLoS Biol 8(7), e1000440. doi:10.1371/journal.pbio.1000440
Guerreiro I, Nunes A, Woltering JM, Casaca A, Novoa A, Vinagre T, Hunter ME, Duboule D, Mallo M (2013) Role of a polymorphism in a Hox/Pax-responsive enhancer in the evolution of the vertebrate spine. Proc Natl Acad Sci USA 110(26):10682–10686. doi:10.1073/pnas.1300592110
Halder G, Callaerts P, Gehring WJ (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267(5205):1788–1792
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(9):3196–3201. doi:10.1073/pnas.0308600100
Hevner RF, Daza RA, Rubenstein JL, Stunnenberg H, Olavarria JF, Englund C (2003) Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev Neurosci 25(24):139–151. doi:72263
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(3):223–233. doi:10.1016/j.neures.2006.03.004
Hicks SP, D’Amato CJ (1968) Cell migrations to the isocortex in the rat. Anat Rec 160(3):619–634. doi:10.1002/ar.1091600311
Hill RE, Favor J, Hogan BL, Ton CC, Saunders GF, Hanson IM, Prosser J, Jordan T, Hastie ND, van Heyningen V (1991) Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354(6354):522–525. doi:10.1038/354522a0
Hirata T, Nomura T, Takagi Y, Sato Y, Tomioka N, Fujisawa H, Osumi N (2002) Mosaic development of the olfactory cortex with Pax6-dependent and -independent components. Brain Res Dev Brain Res 136(1):17–26
Hirata T, Li P, Lanuza GM, Cocas LA, Huntsman MM, Corbin JG (2009) Identification of distinct telencephalic progenitor pools for neuronal diversity in the amygdala. Nat Neurosci 12(2):141–149. doi:10.1038/nn.2241
Holmgren N (1922) Points of view concerning forebrain morphology in lower vertebrates. J Comp Neurol 34:391–459
Holmgren N (1925) Points of view concerning forebrain morphology in higher vertebrates. Acta Zool (Stockh) 6:413–477
Jacob F (1977) Evolution and tinkering. Science 196(4295):1161–1166
Jarvis ED, Gunturkun O, Bruce L, Csillag A, Karten H, Kuenzel W, Medina L, Paxinos G, Perkel DJ, Shimizu T, Striedter G, Wild JM, Ball GF, Dugas-Ford J, Durand SE, Hough GE, Husband S, Kubikova L, Lee DW, Mello CV, Powers A, Siang C, Smulders TV, Wada K, White SA, Yamamoto K, Yu J, Reiner A, Butler AB (2005) Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6(2):151–159. doi:10.1038/nrn1606
Jarvis ED, Yu J, Rivas MV, Horita H, Feenders G, Whitney O, Jarvis SC, Jarvis ER, Kubikova L, Puck AE, Siang-Bakshi C, Martin S, McElroy M, Hara E, Howard J, Pfenning A, Mouritsen H, Chen CC, Wada K (2013) Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns. J Comp Neurol 521(16):3614–3665. doi:10.1002/cne.23404
Jones ME, Cree A (2012) Tuatara. Curr Biol 22(23):R986–R987. doi:10.1016/j.cub.2012.10.049
Jones L, Lopez-Bendito G, Gruss P, Stoykova A, Molnár Z (2002) Pax6 is required for the normal development of the forebrain axonal connections. Development 129(21):5041–5052
Jun S, Desplan C (1996) Cooperative interactions between paired domain and homeodomain. Development 122:2639–2650
Karten H (1969) The organization of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon. Ann NY Acad Sci 167:164–179
Kemp TS (2007) The origin of higher taxa: macroevolutionary processes, and the case of the mammals. Acta Zool (Stockh) 88:3–22
King MC, Wilson AC (1975) Evolution at two levels in humans and chimpanzees. Science 188(4184):107–116
Kirischuk S, Luhmann HJ, Kilb W (2014) Cajal-Retzius cells: update on structural and functional properties of these mystic neurons that bridged the 20th century. Neuroscience 275:33–46. doi:10.1016/j.neuroscience.2014.06.009
Lang D, Powell SK, Plummer RS, Young KP, Ruggeri BA (2007) PAX genes: roles in development, pathophysiology, and cancer. Biochem Pharmacol 73(1):1–14. doi:10.1016/j.bcp.2006.06.024
Laurin M (2004) The evolution of body size, Cope’s rule and the origin of amniotes. Syst Biol 53(4):594–622. doi:10.1080/10635150490445706
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((suppl 1)):i152–i161. doi:10.1093/cercor/bhk017
Medina L, Reiner A (2000) Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23(1):1–12
Medina L, Abellan A, Desfilis E (2013) A never-ending search for the evolutionary origin of the neocortex: rethinking the homology concept. Brain Behav Evol 81(3):150–153. doi:10.1159/000348282
Mi D, Carr CB, Georgala PA, Huang YT, Manuel MN, Jeanes E, Niisato E, Sansom SN, Livesey FJ, Theil T, Hasenpusch-Theil K, Simpson TI, Mason JO, Price DJ (2013) Pax6 exerts regional control of cortical progenitor proliferation via direct repression of Cdk6 and hypophosphorylation of pRb. Neuron 78(2):269–284. doi:10.1016/j.neuron.2013.02.012
Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M (2004) Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131(13):3133–3145. doi:10.1242/dev.01173
Modesto SP, Scott DM, MacDougall MJ, Sues HD, Evans DC, Reisz RR (2015) The oldest parareptile and the early diversification of reptiles. Proc R Soc B Biol Sci 282(1801):1–9. doi:10.1098/rspb.2014.1912
Molnár Z, Butler AB (2002) The corticostriatal junction: a crucial region for forebrain development and evolution. BioEssays 24(6):530–541. doi:10.1002/bies.10100
Molnár Z, Metin C, Stoykova A, Tarabykin V, Price DJ, Francis F, Meyer G, Dehay C, Kennedy H (2006) Comparative aspects of cerebral cortical development. Eur J Neurosci 23(4):921–934. doi:10.1111/j.1460-9568.2006.04611.x
Nagashima H, Hirasawa T, Sugahara F, Takechi M, Usuda R, Sato N, Kuratani S (2013) Origin of the unique morphology of the shoulder girdle in turtles. J Anat 223(6):547–556. doi:10.1111/joa.12116
Nieuwenhuys R (1994) The neocortex. An overview of its evolutionary development, structural organization and synaptology. Anat Embryol 190(4):307–337
Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C (1998) The central nervous system of vertebrates. Springer, Berlin
Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7(2):136–144. doi:10.1038/nn1172
Nomura T, Takahashi M, Hara Y, Osumi N (2008) Patterns of neurogenesis and amplitude of Reelin expression are essential for making a mammalian-type cortex. PLoS One 3(1), e1454. doi:10.1371/journal.pone.0001454
Nomura T, Gotoh H, Ono K (2013a) Changes in the regulation of cortical neurogenesis contribute to encephalization during amniote brain evolution. Nat Commun 4:2206. doi:10.1038/ncomms3206
Nomura T, Kawaguchi M, Ono K, Murakami Y (2013b) Reptiles: a new model for brain evo-devo research. J Exp Zool B Mol Dev Evol 320(2):57–73. doi:10.1002/jez.b.22484
Nomura T, Murakami Y, Gotoh H, Ono K (2014) Reconstruction of ancestral brains: exploring the evolutionary process of encephalization in amniotes. Neurosci Res 86:25–36. doi:10.1016/j.neures.2014.03.004
Nonaka-Kinoshita M, Reillo I, Artegiani B, Martinez-Martinez MA, Nelson M, Borrell V, Calegari F (2013) Regulation of cerebral cortex size and folding by expansion of basal progenitors. EMBO J 32(13):1817–1828. doi:10.1038/emboj.2013.96
Puelles L, Medina L (2002) Field homology as a way to reconcile genetic and developmental variability with adult homology. Brain Res Bull 57(3-4):243–255
Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JL (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424(3):409–438
Pyron RA, Burbrink FT, Wiens JJ (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13:93. doi:10.1186/1471-2148-13-93
Quinn JC, Molinek M, Martynoga BS, Zaki PA, Faedo A, Bulfone A, Hevner RF, West JD, Price DJ (2007) Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev Biol 302(1):50–65. doi:10.1016/j.ydbio.2006.08.035
Quiring R, Walldorf U, Kloter U, Gehring WJ (1994) Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 265(5173):785–789
Rakic P (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18(9):383–388
Romer AS (1957) Origin of the amniote egg. Sci Mon 85(57-63)
Ronshaugen M, McGinnis N, McGinnis W (2002) Hox protein mutation and macroevolution of the insect body plan. Nature 415(6874):914–917. doi:10.1038/nature716
Rowe T (1996) Coevolution of the mammalian middle ear and neocortex. Science 273(5275):651–654
Rowe TB, Macrini TE, Luo ZX (2011) Fossil evidence on origin of the mammalian brain. Science 332(6032):955–957. doi:10.1126/science.1203117
Ruta M, Coates MI, Quicke DL (2003) Early tetrapod relationships revisited. Biol Rev Camb Philos Soc 78(2):251–345
Sanchez-Villagra MR (2010) Developmental palaeontology in synapsids: the fossil record of ontogeny in mammals and their closest relatives. Proc R Soc B Biol Sci 277(1685):1139–1147. doi:10.1098/rspb.2009.2005
Sansom SN, Griffiths DS, Faedo A, Kleinjan DJ, Ruan Y, Smith J, van Heyningen V, Rubenstein JL, Livesey FJ (2009) The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet 5(6), e1000511. doi:10.1371/journal.pgen.1000511
Sekine K, Kubo K, Nakajima K (2014) How does Reelin control neuronal migration and layer formation in the developing mammalian neocortex? Neurosci Res 86:50–58. doi:10.1016/j.neures.2014.06.004
Sessa A, Mao CA, Hadjantonakis AK, Klein WH, Broccoli V (2008) Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 60(1):56–69. doi:10.1016/j.neuron.2008.09.028
Simpson TI, Price DJ (2002) Pax6: a pleiotropic player in development. BioEssays 24(11):1041–1051. doi:10.1002/bies.10174
Stancik EK, Navarro-Quiroga I, Sellke R, Haydar TF (2010) Heterogeneity in ventricular zone neural precursors contributes to neuronal fate diversity in the postnatal neocortex. J Neurosci 30(20):7028–7036. doi:10.1523/JNEUROSCI.6131-09.2010
Sterling JN (2011) The early evolution of archosaurs: relationships and the origin of major clades. Bull Am Mus Nat Hist 352:1–292
Striedter GF (2005) Principle of brain evolution. Sinauer, Sunderland
Suzuki IK, Kawasaki T, Gojobori T, Hirata T (2012) The temporal sequence of the mammalian neocortical neurogenetic program drives mediolateral pattern in the chick pallium. Dev Cell 22(4):863–870. doi:10.1016/j.devcel.2012.01.004
Tabata H, Nakajima K (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 23(31):9996–10001
Takiguchi-Hayashi K, Sekiguchi M, Ashigaki S, Takamatsu M, Hasegawa H, Suzuki-Migishima R, Yokoyama M, Nakanishi S, Tanabe Y (2004) Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J Neurosci 24(9):2286–2295. doi:10.1523/JNEUROSCI.4671-03.2004
Teissier A, Griveau A, Vigier L, Piolot T, Borello U, Pierani A (2010) A novel transient glutamatergic population migrating from the pallial-subpallial boundary contributes to neocortical development. J Neurosci 30(31):10563–10574. doi:10.1523/JNEUROSCI.0776-10.2010
Teissier A, Waclaw RR, Griveau A, Campbell K, Pierani A (2012) Tangentially migrating transient glutamatergic neurons control neurogenesis and maintenance of cerebral cortical progenitor pools. Cereb Cortex 22(2):403–416. doi:10.1093/cercor/bhr122
Tissir F, Lambert De Rouvroit C, Sire JY, Meyer G, Goffinet AM (2003) Reelin expression during embryonic brain development in Crocodylus niloticus. J Comp Neurol 457(3):250–262. doi:10.1002/cne.10573
Tole S, Remedios R, Saha B, Stoykova A (2005) Selective requirement of Pax6, but not Emx2, in the specification and development of several nuclei of the amygdaloid complex. J Neurosci 25(10):2753–2760. doi:10.1523/JNEUROSCI.3014-04.2005
Tosa Y, Hirao A, Matsubara I, Kawaguchi M, Fukui M, Kuratani S, Murakami Y (2015) Development of the thalamo-dorsal ventricular ridge tract in the Chinese soft-shelled turtle, Pelodiscus sinensis. Dev Growth Differ 57(1):40–57. doi:10.1111/dgd.12186
Tsai HM, Garber BB, Larramendi LM (1981) 3H-Thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo: I. Neuronal birthdates of telencephalic compartments in situ. J Comp Neurol 198(2):275–292. doi:10.1002/cne.901980207
Tuoc TC, Radyushkin K, Tonchev AB, Pinon MC, Ashery-Padan R, Molnár Z, Davidoff MS, Stoykova A (2009) Selective cortical layering abnormalities and behavioral deficits in cortex-specific Pax6 knock-out mice. J Neurosci 29(26):8335–8349. doi:10.1523/JNEUROSCI.5669-08.2009
Ulinski PS (1983) Dorsal ventricular ridge: a treatise on forebrain organization in reptiles and birds. Wiley, New York
Ulinski PS (1990) The cerebral cortex of reptiles. In: Cerebral cortex, vol 8A. Plenum Press, New York, pp 139–215
Wang W, Zhong J, Wang YQ (2010) Comparative genomic analysis reveals the evolutionary conservation of Pax gene family. Genes Genet Syst 85(3):193–206
Wang Z, Pascual-Anaya J, Zadissa A, Li W, Niimura Y, Huang Z, Li C, White S, Xiong Z, Fang D, Wang B, Ming Y, Chen Y, Zheng Y, Kuraku S, Pignatelli M, Herrero J, Beal K, Nozawa M, Li Q, Wang J, Zhang H, Yu L, Shigenobu S, Wang J, Liu J, Flicek P, Searle S, Wang J, Kuratani S, Yin Y, Aken B, Zhang G, Irie N (2013) The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nat Genet 45(6):701–706. doi:10.1038/ng.2615
Yoshida M, Assimacopoulos S, Jones KR, Grove EA (2006) Massive loss of Cajal–Retzius cells does not disrupt neocortical layer order. Development 133(3):537–545. doi:10.1242/dev.02209
Zhang X, Huang CT, Chen J, Pankratz MT, Xi J, Li J, Yang Y, Lavaute TM, Li XJ, Ayala M, Bondarenko GI, Du ZW, Jin Y, Golos TG, Zhang SC (2010) Pax6 is a human neuroectoderm cell fate determinant. Cell Stem Cell 7(1):90–100. doi:10.1016/j.stem.2010.04.017
Acknowledgments
We thank Drs. Katsuhiko Ono and Hitoshi Gotoh for providing critical comments and suggestions for the research and Ms. Misato Kawami and Mr. Kazuhiro Arimura for technical support. This work was supported by Grant-in-Aid for Challenging Exploratory Research (#24657158), Scientific Research on Innovative Areas (The Empathetic Systems, #26118510) and PRESTO, JST.
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Yamashita, W., Nomura, T. (2017). The Neocortex and Dorsal Ventricular Ridge: Functional Convergence and Underlying Developmental Mechanisms. In: Shigeno, S., Murakami, Y., Nomura, T. (eds) Brain Evolution by Design. Diversity and Commonality in Animals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56469-0_12
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