Skip to main content
SpringerLink
Log in

Molecular and cellular evolution of corticogenesis in amniotes

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

The cerebral cortex varies dramatically in size and complexity between amniotes due to differences in neuron number and composition. These differences emerge during embryonic development as a result of variations in neurogenesis, which are thought to recapitulate modifications occurred during evolution that culminated in the human neocortex. Here, we review work from the last few decades leading to our current understanding of the evolution of neurogenesis and size of the cerebral cortex. Focused on specific examples across vertebrate and amniote phylogeny, we discuss developmental mechanisms regulating the emergence, lineage, complexification and fate of cortical germinal layers and progenitor cell types. At the cellular level, we discuss the fundamental impact of basal progenitor cells and the advent of indirect neurogenesis on the increased number and diversity of cortical neurons and layers in mammals, and on cortex folding. Finally, we discuss recent work that unveils genetic and molecular mechanisms underlying this progressive expansion and increased complexity of the amniote cerebral cortex during evolution, with a particular focus on those leading to human-specific features. Whereas new genes important in human brain development emerged the recent hominid lineage, regulation of the patterns and levels of activity of highly conserved signaling pathways are beginning to emerge as mechanisms of central importance in the evolutionary increase in cortical size and complexity across amniotes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Goffinet AM (2017) The evolution of cortical development: the synapsid-diapsid divergence. Development 144(22):4061–4077

    PubMed  CAS  Google Scholar 

  2. Benton MJ, Donoghue PC (2007) Paleontological evidence to date the tree of life. Mol Biol Evol 24(1):26–53

    PubMed  CAS  Google Scholar 

  3. De Juan-Romero C, Borrell V (2015) Coevolution of radial glial cells and the cerebral cortex. Glia 63(8):1303–1319

    PubMed  PubMed Central  Google Scholar 

  4. Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268(5217):1578–1584

    PubMed  CAS  Google Scholar 

  5. Puelles L (2001) Thoughts on the development, structure and evolution of the mammalian and avian telencephalic pallium. Philos Trans R Soc Lond B Biol Sci 356(1414):1583–1598

    PubMed  PubMed Central  CAS  Google Scholar 

  6. Rakic P (2009) Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci 10(10):724–735

    PubMed  PubMed Central  CAS  Google Scholar 

  7. Florio M, Huttner WB (2014) Neural progenitors, neurogenesis and the evolution of the neocortex. Development 141(11):2182–2194

    PubMed  CAS  Google Scholar 

  8. Rowe TB, Macrini TE, Luo ZX (2011) Fossil evidence on origin of the mammalian brain. Science 332(6032):955–957

    PubMed  CAS  Google Scholar 

  9. Luzzati F (2015) A hypothesis for the evolution of the upper layers of the neocortex through co-option of the olfactory cortex developmental program. Front Neurosci 9:162

    PubMed  PubMed Central  Google Scholar 

  10. Dugas-Ford J, Ragsdale CW (2015) Levels of homology and the problem of neocortex. Annu Rev Neurosci 38:351–368

    PubMed  CAS  Google Scholar 

  11. Krubitzer L (2009) In search of a unifying theory of complex brain evolution. Ann N Y Acad Sci 1156:44–67

    PubMed  PubMed Central  Google Scholar 

  12. Reillo I, Borrell V (2012) Germinal zones in the developing cerebral cortex of ferret: ontogeny, cell cycle kinetics, and diversity of progenitors. Cereb Cortex 22(9):2039–2054

    PubMed  Google Scholar 

  13. Montiel JF et al (2016) From sauropsids to mammals and back: new approaches to comparative cortical development. J Comp Neurol 524(3):630–645

    PubMed  Google Scholar 

  14. Briscoe SD, Ragsdale CW (2018) Homology, neocortex, and the evolution of developmental mechanisms. Science 362(6411):190–193

    PubMed  CAS  Google Scholar 

  15. Puelles L et al (2019) Concentric ring topology of mammalian cortical sectors and relevance for patterning studies. J Comp Neurol 527:1732–1752

    Google Scholar 

  16. Aboitiz F (2011) Genetic and developmental homology in amniote brains. Toward conciliating radical views of brain evolution. Brain Res Bull 84(2):125–136

    PubMed  Google Scholar 

  17. Tosches MA et al (2018) Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science 360(6391):881–888

    PubMed  CAS  Google Scholar 

  18. Dugas-Ford J, Rowell JJ, Ragsdale CW (2012) Cell-type homologies and the origins of the neocortex. Proc Natl Acad Sci U S A 109(42):16974–16979

    PubMed  PubMed Central  CAS  Google Scholar 

  19. Florio M, Borrell V, Huttner WB (2017) Human-specific genomic signatures of neocortical expansion. Curr Opin Neurobiol 42:33–44

    PubMed  CAS  Google Scholar 

  20. Kaas JH (2011) Neocortex in early mammals and its subsequent variations. Ann N Y Acad Sci 1225:28–36

    PubMed  Google Scholar 

  21. Tzika AC et al (2011) Reptilian-transcriptome v1.0, a glimpse in the brain transcriptome of five divergent Sauropsida lineages and the phylogenetic position of turtles. Evodevo 2(1):19

    PubMed  PubMed Central  CAS  Google Scholar 

  22. Crawford NG et al (2012) More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs. Biol Lett 8(5):783–786

    PubMed  PubMed Central  Google Scholar 

  23. Nomura T et al (2013) Reptiles: a new model for brain evo-devo research. J Exp Zool B Mol Dev Evol 320(2):57–73

    PubMed  Google Scholar 

  24. Nomura T et al (2014) Reconstruction of ancestral brains: exploring the evolutionary process of encephalization in amniotes. Neurosci Res 86:25–36

    PubMed  Google Scholar 

  25. Puelles L (2017) Comments on the updated tetrapartite pallium model in the mouse and chick, featuring a homologous claustro-insular complex. Brain Behav Evol 90(2):171–189

    PubMed  Google Scholar 

  26. Nomura T et al (2008) Patterns of neurogenesis and amplitude of Reelin expression are essential for making a mammalian-type cortex. PLoS One 3(1):e1454

    PubMed  PubMed Central  Google Scholar 

  27. Desfilis E et al (2018) Expression of regulatory genes in the embryonic brain of a lizard and implications for understanding pallial organization and evolution. J Comp Neurol 526(1):166–202

    PubMed  CAS  Google Scholar 

  28. Jarvis ED (2006) Evolution of the pallium in birds and reptiles. In: Binder MD, Hirokawa N, Windhorst U (eds) Encyclopedia of neuroscience. Springer, Berlin, Heidelberg

    Google Scholar 

  29. Kaas JH (2016) Evolution of nervous systems. Academic Press, New York

    Google Scholar 

  30. Puelles L et al (2016) Radial derivatives of the mouse ventral pallium traced with Dbx1-LacZ reporters. J Chem Neuroanat 75(Pt A):2–19

    PubMed  CAS  Google Scholar 

  31. Medina L et al (2004) Expression of Dbx1, Neurogenin 2, Semaphorin 5A, Cadherin 8, and Emx1 distinguish ventral and lateral pallial histogenetic divisions in the developing mouse claustroamygdaloid complex. J Comp Neurol 474(4):504–523

    PubMed  Google Scholar 

  32. Manger PR, Slutsky DA, Molnar Z (2002) Visual subdivisions of the dorsal ventricular ridge of the iguana (Iguana iguana) as determined by electrophysiologic mapping. J Comp Neurol 453(3):226–246

    PubMed  Google Scholar 

  33. Montiel JF, Aboitiz F (2015) Pallial patterning and the origin of the isocortex. Front Neurosci 9:377

    PubMed  PubMed Central  Google Scholar 

  34. Karten HJ (2013) Neocortical evolution: neuronal circuits arise independently of lamination. Curr Biol 23(1):R12–R15

    PubMed  CAS  Google Scholar 

  35. Katz LC, Callaway EM (1992) Development of local circuits in mammalian visual cortex. Annu Rev Neurosci 15:31–56

    PubMed  CAS  Google Scholar 

  36. Jarvis ED et al (2005) Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6(2):151–159

    PubMed  CAS  Google Scholar 

  37. Martinez-Cerdeno V et al (2018) Update on forebrain evolution: from neurogenesis to thermogenesis. Semin Cell Dev Biol 76:15–22

    PubMed  Google Scholar 

  38. Reiner A (1993) Neurotransmitter organization and connections of turtle cortex: implications for the evolution of mammalian isocortex. Comp Biochem Physiol Comp Physiol 104(4):735–748

    PubMed  CAS  Google Scholar 

  39. Molnar Z (2011) Evolution of cerebral cortical development. Brain Behav Evol 78(1):94–107

    PubMed  Google Scholar 

  40. Nomura T et al (2018) Species-specific mechanisms of neuron subtype specification reveal evolutionary plasticity of amniote brain development. Cell Rep 22(12):3142–3151

    PubMed  CAS  Google Scholar 

  41. Jabaudon D (2017) Fate and freedom in developing neocortical circuits. Nat Commun 8:16042

    PubMed  PubMed Central  CAS  Google Scholar 

  42. Herculano-Houzel S et al (2008) The basic nonuniformity of the cerebral cortex. Proc Natl Acad Sci U S A 105(34):12593–12598

    PubMed  PubMed Central  CAS  Google Scholar 

  43. Olkowicz S et al (2016) Birds have primate-like numbers of neurons in the forebrain. Proc Natl Acad Sci U S A 113(26):7255–7260

    PubMed  PubMed Central  CAS  Google Scholar 

  44. Geschwind DH, Rakic P (2013) Cortical evolution: judge the brain by its cover. Neuron 80(3):633–647

    PubMed  PubMed Central  CAS  Google Scholar 

  45. 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

    PubMed  CAS  Google Scholar 

  46. Dehay C, Kennedy H (2007) Cell-cycle control and cortical development. Nat Rev Neurosci 8(6):438–450

    PubMed  CAS  Google Scholar 

  47. Kriegstein A, Noctor S, Martinez-Cerdeno V (2006) Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7(11):883–890

    PubMed  CAS  Google Scholar 

  48. Lewitus E, Kelava I, Huttner WB (2013) Conical expansion of the outer subventricular zone and the role of neocortical folding in evolution and development. Front Hum Neurosci 7:424

    PubMed  PubMed Central  Google Scholar 

  49. Lewitus E et al (2014) An adaptive threshold in Mammalian neocortical evolution. PLoS Biol 12(11):e1002000

    PubMed  PubMed Central  Google Scholar 

  50. Borrell V, Reillo I (2012) Emerging roles of neural stem cells in cerebral cortex development and evolution. Dev Neurobiol 72(7):955–971

    PubMed  Google Scholar 

  51. Llinares-Benadero C, Borrell V (2019) Deconstructing cortical folding: genetic, cellular and mechanical determinants. Nat Rev Neurosci 20(3):161–176

    PubMed  CAS  Google Scholar 

  52. Lodato S, Arlotta P (2015) Generating neuronal diversity in the mammalian cerebral cortex. Annu Rev Cell Dev Biol 31:699–720

    PubMed  PubMed Central  CAS  Google Scholar 

  53. Gelman DM, Marin O (2010) Generation of interneuron diversity in the mouse cerebral cortex. Eur J Neurosci 31(12):2136–2141

    PubMed  Google Scholar 

  54. Uzquiano A et al (2018) Cortical progenitor biology: key features mediating proliferation versus differentiation. J Neurochem 146(5):500–525

    PubMed  CAS  Google Scholar 

  55. Fernandez V, Llinares-Benadero C, Borrell V (2016) Cerebral cortex expansion and folding: what have we learned? EMBO J 35(10):1021–1044

    PubMed  PubMed Central  CAS  Google Scholar 

  56. Garcia-Moreno F et al (2018) Absence of tangentially migrating glutamatergic neurons in the developing avian brain. Cell Rep 22(1):96–109

    PubMed  PubMed Central  CAS  Google Scholar 

  57. Taverna E, Gotz M, Huttner WB (2014) The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex. Annu Rev Cell Dev Biol 30:465–502

    PubMed  CAS  Google Scholar 

  58. Takahashi T, Nowakowski RS, Caviness VS Jr (1995) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15(9):6046–6057

    PubMed  PubMed Central  CAS  Google Scholar 

  59. Gotz M, Huttner WB (2005) The cell biology of neurogenesis. Nature Rev Mol Cell Biol 6:777–788

    Google Scholar 

  60. Noctor SC et al (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409(6821):714–720

    PubMed  CAS  Google Scholar 

  61. Pilz GA et al (2013) Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type. Nat Commun 4:2125

    PubMed  Google Scholar 

  62. Englund 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(1):247–251

    PubMed  PubMed Central  CAS  Google Scholar 

  63. Borrell V et al (2012) Slit/Robo signaling modulates the proliferation of central nervous system progenitors. Neuron 76(2):338–352

    PubMed  PubMed Central  CAS  Google Scholar 

  64. Noctor SC, Martinez-Cerdeno V, Kriegstein AR (2008) Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol 508(1):28–44

    PubMed  PubMed Central  Google Scholar 

  65. Noctor SC et al (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7(2):136–144

    PubMed  CAS  Google Scholar 

  66. Cappello S et al (2006) The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci 9(9):1099–1107

    PubMed  CAS  Google Scholar 

  67. Attardo A et al (2008) Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLoS One 3(6):e2388

    PubMed  PubMed Central  Google Scholar 

  68. Haubensak W et al (2004) Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci U S A 101(9):3196–3201

    PubMed  PubMed Central  CAS  Google Scholar 

  69. Miyata T et al (2004) Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131(13):3133–3145

    PubMed  CAS  Google Scholar 

  70. Kowalczyk T et al (2009) Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex 19(10):2439–2450

    PubMed  PubMed Central  Google Scholar 

  71. Sessa A et al (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

    PubMed  PubMed Central  CAS  Google Scholar 

  72. Cardenas A et al (2018) Evolution of cortical neurogenesis in amniotes controlled by robo signaling levels. Cell 174(3):590–606.e21

    PubMed  PubMed Central  CAS  Google Scholar 

  73. Fietz SA, Huttner WB (2011) Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr Opin Neurobiol 21(1):23–35

    PubMed  CAS  Google Scholar 

  74. Hansen DV et al (2010) Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464(7288):554–561

    CAS  PubMed  Google Scholar 

  75. Reillo I et al (2011) A role for intermediate radial glia in the tangential expansion of the Mammalian cerebral cortex. Cereb Cortex 21(7):1674–1694

    PubMed  Google Scholar 

  76. Betizeau M et al (2013) Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate. Neuron 80(2):442–457

    PubMed  CAS  Google Scholar 

  77. Fietz SA et al (2010) OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci 13(6):690–699

    PubMed  CAS  Google Scholar 

  78. Wang X et al (2011) A new subtype of progenitor cell in the mouse embryonic neocortex. Nat Neurosci 14(5):555–561

    PubMed  PubMed Central  CAS  Google Scholar 

  79. Martinez-Cerdeno V et al (2012) Comparative analysis of the subventricular zone in rat, ferret and macaque: evidence for an outer subventricular zone in rodents. PLoS One 7(1):e30178

    PubMed  PubMed Central  CAS  Google Scholar 

  80. Charvet CJ, Striedter GF (2008) Developmental species differences in brain cell cycle rates between northern bobwhite quail (Colinus virginianus) and parakeets (Melopsittacus undulatus): implications for mosaic brain evolution. Brain Behav Evol 72(4):295–306

    PubMed  Google Scholar 

  81. Docampo-Seara A et al (2018) Study of pallial neurogenesis in shark embryos and the evolutionary origin of the subventricular zone. Brain Struct Funct 223(8):3593–3612

    PubMed  CAS  Google Scholar 

  82. Wullimann MF, Puelles L, Wicht H (1999) Early postembryonic neural development in the zebrafish: a 3-D reconstruction of forebrain proliferation zones shows their relation to prosomeres. Eur J Morphol 37(2–3):117–121

    PubMed  CAS  Google Scholar 

  83. Nomura T, Gotoh H, Ono K (2013) Changes in the regulation of cortical neurogenesis contribute to encephalization during amniote brain evolution. Nat Commun 4:2206

    PubMed  Google Scholar 

  84. Villar-Cheda B et al (2006) Cell proliferation in the forebrain and midbrain of the sea lamprey. J Comp Neurol 494(6):986–1006

    PubMed  Google Scholar 

  85. Martinez-Cerdeno V et al (2015) Evolutionary origin of Tbr2-expressing precursor cells and the subventricular zone in the developing cortex. J Comp Neurol 524:433–447

    PubMed  PubMed Central  Google Scholar 

  86. Borrell V, Calegari F (2014) Mechanisms of brain evolution: regulation of neural progenitor cell diversity and cell cycle length. Neurosci Res 86:14–24

    PubMed  Google Scholar 

  87. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88(1):49–92

    PubMed  CAS  Google Scholar 

  88. 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

    PubMed  CAS  Google Scholar 

  89. Caviness VS Jr., Takahashi T (1995) Proliferative events in the cerebral ventricular zone. Brain Dev 17(3):159–163

    PubMed  Google Scholar 

  90. Calegari F et al (2005) Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J Neurosci 25(28):6533–6538

    PubMed  PubMed Central  CAS  Google Scholar 

  91. Lange C, Huttner WB, Calegari F (2009) Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5(3):320–331

    PubMed  CAS  Google Scholar 

  92. Kornack DR, Rakic P (1998) Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc Natl Acad Sci U S A 95(3):1242–1246

    PubMed  PubMed Central  CAS  Google Scholar 

  93. Martinez-Martinez MA et al (2016) A restricted period for formation of outer subventricular zone defined by Cdh1 and Trnp1 levels. Nat Commun 7:11812

    PubMed  PubMed Central  Google Scholar 

  94. Charvet CJ, Striedter GF (2010) Bigger brains cycle faster before neurogenesis begins: a comparison of brain development between chickens and bobwhite quail. Proc Biol Sci 277(1699):3469–3475

    PubMed  PubMed Central  Google Scholar 

  95. 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

    PubMed  Google Scholar 

  96. Cheung AF et al (2010) The subventricular zone is the developmental milestone of a 6-layered neocortex: comparisons in metatherian and eutherian mammals. Cereb Cortex 20(5):1071–1081

    PubMed  Google Scholar 

  97. Boulder Committee (1970) Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166(2):257–261

    Google Scholar 

  98. Hevner RF et al (2006) Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci Res 55(3):223–233

    PubMed  CAS  Google Scholar 

  99. Hara Y et al (2018) Shark genomes provide insights into elasmobranch evolution and the origin of vertebrates. Nat Ecol Evol 2(11):1761–1771

    PubMed  Google Scholar 

  100. Ferner K, Mess A (2011) Evolution and development of fetal membranes and placentation in amniote vertebrates. Respir Physiol Neurobiol 178(1):39–50

    PubMed  Google Scholar 

  101. Moreno N, Gonzalez A (2017) Pattern of neurogenesis and identification of neuronal progenitor subtypes during pallial development in Xenopus laevis. Front Neuroanat 11:24

    PubMed  PubMed Central  Google Scholar 

  102. Nomura T et al (2016) The evolution of basal progenitors in the developing non-mammalian brain. Development 143(1):66–74

    PubMed  PubMed Central  CAS  Google Scholar 

  103. Clinton BK et al (2014) Radial glia in the proliferative ventricular zone of the embryonic and adult turtle, Trachemys scripta elegans. Neurogenesis (Austin) 1(1):e970905

    Google Scholar 

  104. Cruce WL, Nieuwenhuys R (1974) The cell masses in the brain stem of the turtle Testudo hermanni; a topographical and topological analysis. J Comp Neurol 156(3):277–306

    PubMed  CAS  Google Scholar 

  105. Zardoya R, Meyer A (2001) The evolutionary position of turtles revised. Naturwissenschaften 88(5):193–200

    PubMed  CAS  Google Scholar 

  106. Cheung AF et al (2007) Comparative aspects of cortical neurogenesis in vertebrates. J Anat 211(2):164–176

    PubMed  PubMed Central  Google Scholar 

  107. Charvet CJ, Owerkowicz T, Striedter GF (2009) Phylogeny of the telencephalic subventricular zone in sauropsids: evidence for the sequential evolution of pallial and subpallial subventricular zones. Brain Behav Evol 73(4):285–294

    PubMed  Google Scholar 

  108. Reiner A, Yamamoto K, Karten HJ (2005) Organization and evolution of the avian forebrain. Anat Rec A Discov Mol Cell Evol Biol 287(1):1080–1102

    PubMed  Google Scholar 

  109. Butler AB, Cotterill RM (2006) Mammalian and avian neuroanatomy and the question of consciousness in birds. Biol Bull 211(2):106–127

    PubMed  Google Scholar 

  110. Northcutt RG (2011) Paleontology: evolving large and complex brains. Science 332(6032):926–927

    PubMed  CAS  Google Scholar 

  111. Molnar Z et al (2014) Evolution and development of the mammalian cerebral cortex. Brain Behav Evol 83(2):126–139

    PubMed  Google Scholar 

  112. Rowe TB, Shepherd GM (2016) Role of ortho-retronasal olfaction in mammalian cortical evolution. J Comp Neurol 524(3):471–495

    PubMed  Google Scholar 

  113. Kaas JH (2013) The evolution of brains from early mammals to humans. Wiley Interdiscip Rev Cogn Sci 4(1):33–45

    PubMed  Google Scholar 

  114. Aboitiz F, Montiel JF (2015) Olfaction, navigation, and the origin of isocortex. Front Neurosci 9:402

    PubMed  PubMed Central  Google Scholar 

  115. O’Leary MA et al (2013) The placental mammal ancestor and the post–K–Pg radiation of placentals. Science 339(6120):662–667

    PubMed  Google Scholar 

  116. Kelava I, Lewitus E, Huttner WB (2013) The secondary loss of gyrencephaly as an example of evolutionary phenotypical reversal. Front Neuroanat 7:16

    PubMed  PubMed Central  Google Scholar 

  117. Namba T, Huttner WB (2017) Neural progenitor cells and their role in the development and evolutionary expansion of the neocortex. Wiley Interdiscip Rev Dev Biol 6(1):e256

    Google Scholar 

  118. Shepherd GM, Rowe TB (2017) Neocortical lamination: insights from neuron types and evolutionary precursors. Front Neuroanat 11:100

    PubMed  PubMed Central  Google Scholar 

  119. Ashwell K (2013) Neurobiology of monotremes: brain evolution in our distant mammalian cousins. CSIRO PUBLISHING, Clayton

    Google Scholar 

  120. Ashwell KW, Hardman CD (2012) Distinct development of the cerebral cortex in platypus and echidna. Brain Behav Evol 79(1):57–72

    PubMed  Google Scholar 

  121. Suarez R, Gobius I, Richards LJ (2014) Evolution and development of interhemispheric connections in the vertebrate forebrain. Front Hum Neurosci 8:497

    PubMed  PubMed Central  Google Scholar 

  122. Ashwell KW (2008) Encephalization of Australian and new guinean marsupials. Brain Behav Evol 71(3):181–199

    PubMed  CAS  Google Scholar 

  123. Karlen SJ, Krubitzer L (2007) The functional and anatomical organization of marsupial neocortex: evidence for parallel evolution across mammals. Prog Neurobiol 82(3):122–141

    PubMed  PubMed Central  Google Scholar 

  124. Puzzolo E, Mallamaci A (2010) Cortico-cerebral histogenesis in the opossum Monodelphis domestica: generation of a hexalaminar neocortex in the absence of a basal proliferative compartment. Neural Dev 5:8

    PubMed  PubMed Central  Google Scholar 

  125. Sauerland C et al (2018) The basal radial glia occurs in marsupials and underlies the evolution of an expanded neocortex in therian mammals. Cereb Cortex 28(1):145–157

    PubMed  Google Scholar 

  126. Tarver JE et al (2016) The interrelationships of placental mammals and the limits of phylogenetic inference. Genome Biol Evol 8(2):330–344

    PubMed  PubMed Central  CAS  Google Scholar 

  127. Miller DJ et al (2019) Shared and derived features of cellular diversity in the human cerebral cortex. Curr Opin Neurobiol 56:117–124

    PubMed  CAS  PubMed Central  Google Scholar 

  128. Mihalas AB, Hevner RF (2018) Clonal analysis reveals laminar fate multipotency and daughter cell apoptosis of mouse cortical intermediate progenitors. Development 145(17):dev164335

    PubMed  PubMed Central  Google Scholar 

  129. Elsen GE et al (2018) The epigenetic factor landscape of developing neocortex is regulated by transcription factors Pax6 → Tbr2 → Tbr1. Front Neurosci 12:571

    PubMed  PubMed Central  Google Scholar 

  130. Tarabykin V et al (2001) Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128(11):1983–1993

    PubMed  CAS  Google Scholar 

  131. Mihalas AB et al (2016) Intermediate progenitor cohorts differentially generate cortical layers and require Tbr2 for timely acquisition of neuronal subtype identity. Cell Rep 16(1):92–105

    PubMed  PubMed Central  CAS  Google Scholar 

  132. Hevner RF (2019) Intermediate progenitors and Tbr2 in cortical development. J Anat 235:616–625

    PubMed  CAS  PubMed Central  Google Scholar 

  133. Lukaszewicz A et al (2005) G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47(3):353–364

    PubMed  PubMed Central  CAS  Google Scholar 

  134. Shitamukai A, Konno D, Matsuzaki F (2011) Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J Neurosci 31(10):3683–3695

    PubMed  PubMed Central  CAS  Google Scholar 

  135. Nonaka-Kinoshita M et al (2013) Regulation of cerebral cortex size and folding by expansion of basal progenitors. EMBO J 32(13):1817–1828

    PubMed  PubMed Central  CAS  Google Scholar 

  136. Stahl R et al (2013) Trnp1 regulates expansion and folding of the mammalian cerebral cortex by control of radial glial fate. Cell 153(3):535–549

    PubMed  CAS  Google Scholar 

  137. Florio M et al (2015) Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science 347(6229):1465–1470

    PubMed  CAS  Google Scholar 

  138. Toda T et al (2016) An essential role of SVZ progenitors in cortical folding in gyrencephalic mammals. Sci Rep 6:29578

    PubMed  PubMed Central  CAS  Google Scholar 

  139. Poluch S, Juliano SL (2015) Fine-tuning of neurogenesis is essential for the evolutionary expansion of the cerebral cortex. Cereb Cortex 25(2):346–364

    PubMed  Google Scholar 

  140. Masuda K et al (2015) Pathophysiological analyses of cortical malformation using gyrencephalic mammals. Sci Rep 5:15370

    PubMed  PubMed Central  CAS  Google Scholar 

  141. Ji Q et al (2002) The earliest known eutherian mammal. Nature 416(6883):816–822

    PubMed  CAS  Google Scholar 

  142. Martinez-Martinez MA et al (2018) Extensive branching of radially-migrating neurons in the mammalian cerebral cortex. J Comp Neurol 527:1558–1576

    Google Scholar 

  143. Smart IH et al (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(1):37–53

    PubMed  Google Scholar 

  144. Kelava I et al (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(2):469–481

    PubMed  Google Scholar 

  145. Malatesta P, Hartfuss E, Gotz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127(24):5253–5263

    PubMed  CAS  Google Scholar 

  146. Gotz M, Stoykova A, Gruss P (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21(5):1031–1044

    PubMed  CAS  Google Scholar 

  147. Miyata T et al (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31(5):727–741

    PubMed  CAS  Google Scholar 

  148. Vitali I et al (2018) Progenitor hyperpolarization regulates the sequential generation of neuronal subtypes in the developing neocortex. Cell 174(5):1264–1276.e15

    PubMed  PubMed Central  CAS  Google Scholar 

  149. Govindan S, Jabaudon D (2017) Coupling progenitor and neuronal diversity in the developing neocortex. FEBS Lett 591(24):3960–3977

    PubMed  CAS  Google Scholar 

  150. Vasistha NA et al (2015) Cortical and clonal contribution of Tbr2 expressing progenitors in the developing mouse brain. Cereb Cortex 25(10):3290–3302

    PubMed  Google Scholar 

  151. Imamura F et al (2011) Timing of neurogenesis is a determinant of olfactory circuitry. Nat Neurosci 14(3):331–337

    PubMed  PubMed Central  CAS  Google Scholar 

  152. Sánchez-Guardado L, Lois C (2019) Lineage does not regulate the sensory synaptic input of projection neurons in the mouse olfactory bulb. Elife pii:e46675. https://doi.org/10.7554/eLife.46675

    Article  Google Scholar 

  153. Caviness VS Jr (1982) Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res 256(3):293–302

    PubMed  Google Scholar 

  154. Angevine JB, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766–768

    PubMed  Google Scholar 

  155. Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183(123):425–427

    PubMed  CAS  Google Scholar 

  156. Molyneaux BJ et al (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8(6):427–437

    PubMed  CAS  Google Scholar 

  157. McConnell SK, Kaznowski CE (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254(5029):282–285

    PubMed  CAS  Google Scholar 

  158. Frantz GD, McConnell SK (1996) Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron 17(1):55–61

    PubMed  CAS  Google Scholar 

  159. Desai AR, McConnell SK (2000) Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127(13):2863–2872

    PubMed  CAS  Google Scholar 

  160. Franco SJ et al (2012) Fate-restricted neural progenitors in the mammalian cerebral cortex. Science 337(6095):746–749

    PubMed  PubMed Central  CAS  Google Scholar 

  161. Eckler MJ et al (2015) Cux2-positive radial glial cells generate diverse subtypes of neocortical projection neurons and macroglia. Neuron 86(4):1100–1108

    PubMed  PubMed Central  CAS  Google Scholar 

  162. Guo C et al (2013) Fezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes. Neuron 80(5):1167–1174

    PubMed  CAS  Google Scholar 

  163. Walsh C, Cepko CL (1993) Clonal dispersion in proliferative layers of developing cerebral cortex. Nature 362(6421):632–635

    PubMed  CAS  Google Scholar 

  164. Shen Q et al (2006) The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9(6):743–751

    PubMed  CAS  Google Scholar 

  165. Telley L et al (2016) Sequential transcriptional waves direct the differentiation of newborn neurons in the mouse neocortex. Science 351(6280):1443–1446

    PubMed  CAS  Google Scholar 

  166. Lodato S, Shetty AS, Arlotta P (2014) Cerebral cortex assembly: generating and reprogramming projection neuron diversity. Trends Neurosci 38:117–125

    PubMed  PubMed Central  Google Scholar 

  167. Marin O (2012) Brain development: the neuron family tree remodelled. Nature 490(7419):185–186

    PubMed  CAS  Google Scholar 

  168. Telley L, Jabaudon D (2018) A mixed model of neuronal diversity. Nature 555(7697):452–454

    PubMed  CAS  Google Scholar 

  169. Nowakowski TJ et al (2017) Spatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex. Science 358(6368):1318–1323

    PubMed  PubMed Central  CAS  Google Scholar 

  170. Dehay C et al (2001) Cell-cycle kinetics of neocortical precursors are influenced by embryonic thalamic axons. J Neurosci 21(1):201–214

    PubMed  PubMed Central  CAS  Google Scholar 

  171. Reillo I et al (2017) A complex code of extrinsic influences on cortical progenitor cells of higher mammals. Cereb Cortex 27(9):4586–4606

    PubMed  Google Scholar 

  172. Mayer S et al (2019) Multimodal single-cell analysis reveals physiological maturation in the developing human neocortex. Neuron 102(1):143–158.e7

    PubMed  CAS  PubMed Central  Google Scholar 

  173. Kalebic N et al (2019) Neocortical expansion due to increased proliferation of basal progenitors is linked to changes in their morphology. Cell Stem Cell 24(4):535–550.e9

    PubMed  CAS  Google Scholar 

  174. Suzuki IK et al (2012) The temporal sequence of the mammalian neocortical neurogenetic program drives mediolateral pattern in the chick pallium. Dev Cell 22(4):863–870

    PubMed  CAS  Google Scholar 

  175. Long M et al (2013) New gene evolution: little did we know. Annu Rev Genet 47:307–333

    PubMed  PubMed Central  CAS  Google Scholar 

  176. Deakin JE, Ezaz T (2014) Tracing the evolution of amniote chromosomes. Chromosoma 123(3):201–216

    PubMed  PubMed Central  Google Scholar 

  177. Hill RS, Walsh CA (2005) Molecular insights into human brain evolution. Nature 437(7055):64–67

    PubMed  CAS  Google Scholar 

  178. Chen S, Krinsky BH, Long M (2013) New genes as drivers of phenotypic evolution. Nat Rev Genet 14(9):645–660

    PubMed  PubMed Central  CAS  Google Scholar 

  179. Andersson DI, Jerlstrom-Hultqvist J, Nasvall J (2015) Evolution of new functions de novo and from preexisting genes. Cold Spring Harb Perspect Biol 7(6):a017996

    PubMed  PubMed Central  Google Scholar 

  180. True JR, Carroll SB (2002) Gene co-option in physiological and morphological evolution. Annu Rev Cell Dev Biol 18:53–80

    PubMed  CAS  Google Scholar 

  181. McLysaght A, Guerzoni D (2015) New genes from non-coding sequence: the role of de novo protein-coding genes in eukaryotic evolutionary innovation. Philos Trans R Soc Lond B Biol Sci 370(1678):20140332

    PubMed  PubMed Central  Google Scholar 

  182. Doan RN, Shin T, Walsh CA (2018) Evolutionary changes in transcriptional regulation: insights into human behavior and neurological conditions. Annu Rev Neurosci 41:185–206

    PubMed  CAS  Google Scholar 

  183. Dorus S et al (2004) Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell 119(7):1027–1040

    PubMed  CAS  Google Scholar 

  184. Franchini LF, Pollard KS (2017) Human evolution: the non-coding revolution. BMC Biol 15(1):89

    PubMed  PubMed Central  Google Scholar 

  185. Pollard KS et al (2006) An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443(7108):167–172

    PubMed  CAS  Google Scholar 

  186. Doan RN et al (2016) Mutations in human accelerated regions disrupt cognition and social behavior. Cell 167(2):341–354.e12

    PubMed  PubMed Central  CAS  Google Scholar 

  187. Yamashita W et al (2018) Conserved and divergent functions of Pax6 underlie species-specific neurogenic patterns in the developing amniote brain. Development 145(8):dev159764

    PubMed  PubMed Central  Google Scholar 

  188. Manuel MN et al (2015) Regulation of cerebral cortical neurogenesis by the Pax6 transcription factor. Front Cell Neurosci 9:70

    PubMed  PubMed Central  Google Scholar 

  189. Wong FK et al (2015) Sustained Pax6 expression generates primate-like basal radial glia in developing mouse neocortex. PLoS Biol 13(8):e1002217

    PubMed  PubMed Central  Google Scholar 

  190. Mi D et al (2013) Pax6 exerts regional control of cortical progenitor proliferation via direct repression of Cdk6 and hypophosphorylation of pRb. Neuron 78(2):269–284

    PubMed  PubMed Central  CAS  Google Scholar 

  191. Asami M et al (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

    PubMed  CAS  Google Scholar 

  192. Quinn JC et al (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

    PubMed  PubMed Central  CAS  Google Scholar 

  193. Sansom SN et al (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

    PubMed  PubMed Central  Google Scholar 

  194. Komada M (2012) Sonic hedgehog signaling coordinates the proliferation and differentiation of neural stem/progenitor cells by regulating cell cycle kinetics during development of the neocortex. Congenit Anom (Kyoto) 52(2):72–77

    Google Scholar 

  195. Bertrand N, Dahmane N (2006) Sonic hedgehog signaling in forebrain development and its interactions with pathways that modify its effects. Trends Cell Biol 16(11):597–605

    PubMed  CAS  Google Scholar 

  196. Komada M et al (2008) Hedgehog signaling is involved in development of the neocortex. Development 135(16):2717–2727

    PubMed  CAS  Google Scholar 

  197. Saade M et al (2013) Sonic hedgehog signaling switches the mode of division in the developing nervous system. Cell Rep 4(3):492–503

    PubMed  CAS  Google Scholar 

  198. Pilaz LJ et al (2009) Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc Natl Acad Sci U S A 106(51):21924–21929

    PubMed  PubMed Central  CAS  Google Scholar 

  199. Pierfelice T, Alberi L, Gaiano N (2011) Notch in the vertebrate nervous system: an old dog with new tricks. Neuron 69(5):840–855

    PubMed  CAS  Google Scholar 

  200. Yoon K, Gaiano N (2005) Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat Neurosci 8(6):709–715

    PubMed  CAS  Google Scholar 

  201. Gaiano N, 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 

  202. Kageyama R et al (2008) Dynamic Notch signaling in neural progenitor cells and a revised view of lateral inhibition. Nat Neurosci 11(11):1247–1251

    PubMed  CAS  Google Scholar 

  203. Ables JL et al (2011) Not(ch) just development: notch signalling in the adult brain. Nat Rev Neurosci 12(5):269–283

    PubMed  PubMed Central  CAS  Google Scholar 

  204. Paridaen JT, Huttner WB (2014) Neurogenesis during development of the vertebrate central nervous system. EMBO Rep 15(4):351–364

    PubMed  PubMed Central  CAS  Google Scholar 

  205. LeBon L et al (2014) Fringe proteins modulate Notch-ligand cis and trans interactions to specify signaling states. Elife 3:e02950

    PubMed  PubMed Central  Google Scholar 

  206. Shimojo H, Ohtsuka T, Kageyama R (2011) Dynamic expression of notch signaling genes in neural stem/progenitor cells. Front Neurosci 5:78

    PubMed  PubMed Central  CAS  Google Scholar 

  207. Nandagopal N et al (2018) Dynamic ligand discrimination in the notch signaling pathway. Cell 172(4):869–880.e19

    PubMed  PubMed Central  CAS  Google Scholar 

  208. Kangsamaksin T et al (2015) NOTCH decoys that selectively block DLL/NOTCH or JAG/NOTCH disrupt angiogenesis by unique mechanisms to inhibit tumor growth. Cancer Discov 5(2):182–197

    PubMed  CAS  Google Scholar 

  209. Blockus H, Chedotal A (2014) The multifaceted roles of Slits and Robos in cortical circuits: from proliferation to axon guidance and neurological diseases. Curr Opin Neurobiol 27:82–88

    PubMed  CAS  Google Scholar 

  210. Dickson BJ, Gilestro GF (2006) Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu Rev Cell Dev Biol 22:651–675

    PubMed  CAS  Google Scholar 

  211. Chedotal A (2019) Roles of axon guidance molecules in neuronal wiring in the developing spinal cord. Nat Rev Neurosci 20:380–396

    PubMed  CAS  Google Scholar 

  212. Andrews W et al (2008) The role of Slit-Robo signaling in the generation, migration and morphological differentiation of cortical interneurons. Dev Biol 313(2):648–658

    PubMed  CAS  Google Scholar 

  213. Mehta B, Bhat KM (2001) Slit signaling promotes the terminal asymmetric division of neural precursor cells in the Drosophila CNS. Development 128(16):3161–3168

    PubMed  CAS  Google Scholar 

  214. Nowakowski TJ et al (2016) Transformation of the radial glia scaffold demarcates two stages of human cerebral cortex development. Neuron 91(6):1219–1227

    PubMed  PubMed Central  CAS  Google Scholar 

  215. Vaid S et al (2018) A novel population of Hopx-dependent basal radial glial cells in the developing mouse neocortex. Development 145(20):dev169276

    PubMed  Google Scholar 

  216. Sousa AMM et al (2017) Evolution of the human nervous system function, structure, and development. Cell 170(2):226–247

    PubMed  PubMed Central  CAS  Google Scholar 

  217. Silver DL (2016) Genomic divergence and brain evolution: how regulatory DNA influences development of the cerebral cortex. BioEssays 38(2):162–171

    PubMed  CAS  Google Scholar 

  218. Boyd JL et al (2015) Human-chimpanzee differences in a FZD8 enhancer alter cell-cycle dynamics in the developing neocortex. Curr Biol 25(6):772–779

    PubMed  PubMed Central  CAS  Google Scholar 

  219. Arcila ML et al (2014) Novel primate miRNAs coevolved with ancient target genes in germinal zone-specific expression patterns. Neuron 81(6):1255–1262

    PubMed  PubMed Central  CAS  Google Scholar 

  220. Charrier C et al (2012) Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine maturation. Cell 149(4):923–935

    PubMed  PubMed Central  CAS  Google Scholar 

  221. Guerrier S et al (2009) The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138(5):990–1004

    PubMed  PubMed Central  CAS  Google Scholar 

  222. Fossati M et al (2016) SRGAP2 and Its human-specific paralog co-regulate the development of excitatory and inhibitory synapses. Neuron 91(2):356–369

    PubMed  PubMed Central  CAS  Google Scholar 

  223. Florio M et al (2016) A single splice site mutation in human-specific ARHGAP11B causes basal progenitor amplification. Sci Adv 2(12):e1601941

    PubMed  PubMed Central  Google Scholar 

  224. Kalebic N et al (2018) Human-specific ARHGAP11B induces hallmarks of neocortical expansion in developing ferret neocortex. Elife 7:e41241

    PubMed  PubMed Central  Google Scholar 

  225. Fiddes IT et al (2018) Human-specific NOTCH2NL genes affect notch signaling and cortical neurogenesis. Cell 173(6):1356–1369.e22

    PubMed  PubMed Central  CAS  Google Scholar 

  226. Suzuki IK et al (2018) Human-specific NOTCH2NL genes expand cortical neurogenesis through delta/notch regulation. Cell 173(6):1370–1384

    PubMed  PubMed Central  CAS  Google Scholar 

  227. Ferland RJ et al (2003) Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J Comp Neurol 460(2):266–279

    PubMed  CAS  Google Scholar 

  228. Enard W et al (2002) Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418(6900):869–872

    PubMed  CAS  Google Scholar 

  229. Fisher SE, Scharff C (2009) FOXP2 as a molecular window into speech and language. Trends Genet 25(4):166–177

    PubMed  CAS  Google Scholar 

  230. Lai CS et al (2001) A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413(6855):519–523

    PubMed  CAS  Google Scholar 

  231. Fisher SE (2019) Human genetics: the evolving story of FOXP2. Curr Biol 29(2):R65–R67

    CAS  PubMed  Google Scholar 

  232. Mekel-Bobrov N et al (2005) Ongoing adaptive evolution of ASPM, a brain size determinant in homo sapiens. Science 309(5741):1720–1722

    PubMed  CAS  Google Scholar 

  233. Bond J et al (2002) ASPM is a major determinant of cerebral cortical size. Nat Genet 32(2):316–320

    PubMed  CAS  Google Scholar 

  234. Fujimori A et al (2014) Disruption of Aspm causes microcephaly with abnormal neuronal differentiation. Brain Dev 36(8):661–669

    PubMed  Google Scholar 

  235. Johnson MB et al (2018) ASPM knockout ferret reveals an evolutionary mechanism governing cerebral cortical size. Nature 556(7701):370–375

    PubMed  PubMed Central  CAS  Google Scholar 

  236. Trastoy J, Schuller IK (2018) Criticality in the brain: evidence and implications for neuromorphic computing. ACS Chem Neurosci 9(6):1254–1258

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We apologize to those authors whose primary work could not be cited here owing to space limitations. We thank Magdalena Götz and members of our lab for insightful discussions. Work in our lab is funded by the Spanish Ministry of Science, Innovation and Universities (SAF2015-69168-R; SAF2017-92781-EXP; PGC2018-102172-B-I00), Consejo Superior de Investigaciones Científicas (201820E129) and the “Severo Ochoa” Programme for Centers of Excellence in Research and Development (Reference SEV-2017-0723).

Author information

Authors and Affiliations

  1. Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas y Universidad Miguel Hernández, 03550, Sant Joan d’Alacant, Alicante, Spain

    Adrián Cárdenas & Víctor Borrell

Authors
  1. Adrián Cárdenas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Víctor Borrell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Víctor Borrell.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cárdenas, A., Borrell, V. Molecular and cellular evolution of corticogenesis in amniotes. Cell. Mol. Life Sci. 77, 1435–1460 (2020). https://doi.org/10.1007/s00018-019-03315-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-019-03315-x

Keywords

Search

Navigation