Cited by 75Developmental Biology and Gene RegulationNeurogenesis and neuroplasticity mechanismsEvolution and Paleontology Studies

Evolution of the Chordate Telencephalon

Open access
Briscoe, Steven D., Ragsdale, Clifton W.·2019·Current Biology

Abstract

The dramatic evolutionary expansion of the neocortex, together with a proliferation of specialized cortical areas, is believed to underlie the emergence of human cognitive abilities. In a broader phylogenetic context, however, neocortex evolution in mammals, including humans, is remarkably conservative, characterized largely by size variations on a shared six-layered neuronal architecture. By contrast, the telencephalon in non-mammalian vertebrates, including reptiles, amphibians, bony and cartilaginous fishes, and cyclostomes, features a great variety of very different tissue structures. Our understanding of the evolutionary relationships of these telencephalic structures, especially those of basally branching vertebrates and invertebrate chordates, remains fragmentary and is impeded by conceptual obstacles. To make sense of highly divergent anatomies requires a hierarchical view of biological organization, one that permits the recognition of homologies at multiple levels beyond neuroanatomical structure. Here we review the origin and diversification of the telencephalon with a focus on key evolutionary innovations shaping the neocortex at multiple levels of organization.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.cub.2019.05.026

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The telencephalon contains putative analogues to components of the mammalian limbic system (for example, hippocampus).

    “a brain region that contains putative analogues to components of the mammalian limbic system (for example, hippocampus)2–4”
  • In teleost fish, the location or even existence of the hippocampus is an area of active debate.

    “In teleost fish, which shared a common ancestor with mammals around 450 million years ago18, the location or even existence of the hippocampus is an area of active debate2,19”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 204 · Cited by 75

Research works printed but not linked: 178

  1. [1]Gee H (2018). Across the Bridge: Understanding the Origin of the Vertebrates (Chicago: The University of Chicago Press).
  2. [3]Gans C, and Northcutt RG (1983). Neural crest and the origin of vertebrates: a new head. Science 220, 268– 273. 17732898
  3. [4]Nieuwenhuys R, Donkelaar H.J.t., and Nicholson C (1998). The Central Nervous System of Vertebrates (New York: Springer).
  4. [5]Butler AB, and Hodos W (2005). Comparative Vertebrate Neuroanatomy: Evolution and Adaptation, 2nd Edition. (Hoboken, NJ: Wiley-Interscience).
  5. [8]Nieuwenhuys R (2009). The forebrain of actinopterygians revisited. Brain Behav. Evol 73, 229– 252. 19546532
  6. [9]Dugas-Ford J, and Ragsdale CW (2015). Levels of homology and the problem of neocortex. Annu. Rev. Neurosci 38, 351– 368. 26154980
  7. [10]Striedter GF, and Northcutt RG (1991). Biological hierarchies and the concept of homology. Brain Behav. Evol 38, 177– 189. 1663811
  8. [11]Hall BK (1994). Homology: The Hierarchical Basis of Comparative Biology (San Diego: Academic Press).
  9. [12]Reiner A (1996). Levels of organization and the evolution of isocortex. Trends Neurosci 19, 89– 91. 9054061
  10. [13]Pritz MB (2005). Comparisons and homology in adult and developing vertebrate central nervous systems. Brain Behav. Evol 66, 222– 233. 16254412
  11. [14]Rowitch DH, and Kriegstein AR (2010). Developmental genetics of vertebrate glial-cell specification. Nature 468, 214– 222. 21068830
  12. [15]Taverna E, Gotz M, and 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. 25000993
  13. [16]Heins N, Cremisi F, Malatesta P, Gangemi RM, Corte G, Price J, Goudreau G, Gruss P, and Gotz M (2001). Emx2 promotes symmetric cell divisions and a multipotential fate in precursors from the cerebral cortex. Mol. Cell. Neurosci 18, 485– 502. 11922140
  14. [17]Rash BG, and Grove EA (2006). Area and layer patterning in the developing cerebral cortex. Curr. Opin. Neurobiol 16, 25– 34. 16426837
  15. [18]O’Leary DD, Chou SJ, and Sahara S (2007). Area patterning of the mammalian cortex. Neuron 56, 252– 269. 17964244
  16. [19]Hebert JM, and Fishell G (2008). The genetics of early telencephalon patterning: some assembly required. Nat. Rev. Neurosci 9, 678– 685. 19143049 PMC2669317
  17. [20]Kiecker C, and Lumsden A (2012). The role of organizers in patterning the nervous system. Annu. Rev. Neurosci 35, 347– 367. 22462542
  18. [21]Reiner A, Medina L, and Veenman CL (1998). Structural and functional evolution of the basal ganglia in vertebrates. Brain Res. Rev 28, 235– 285. 9858740
  19. [22]Moreno N, Gonzalez A, and Retaux S (2009). Development and evolution of the subpallium. Semin. Cell Dev. Biol 20, 735– 743. 19374952
  20. [23]Grillner S, and Robertson B (2016). The basal ganglia over 500 million years. Curr. Biol 26, R1088– R1100. 27780050
  21. [24]Reiner A, and Northcutt RG (1987). An immunohistochemical study of the telencephalon of the African lungfish, Protopterus annectens. J. Comp. Neurol 256, 463– 481. 2437161
  22. [25]Northcutt RG, Reiner A, and Karten HJ (1988). Immunohistochemical study of the telencephalon of the spiny dogfish, Squalus acanthias. J. Comp. Neurol 277, 250– 267. 2466059
  23. [26]Reiner A, and Northcutt RG (1992). An immunohistochemical study of the telencephalon of the senegal bichir (Polypterus senegalus). J. Comp. Neurol 319, 359– 386. 1351063
  24. [27]Sugahara F, Pascual-Anaya J, Oisi Y, Kuraku S, Aota S, Adachi N, Takagi W, Hirai T, Sato N, Murakami Y, (2016). Evidence from cyclostomes for complex regionalization of the ancestral vertebrate brain. Nature 531, 97– 100. 26878236
  25. [28]Wamsley B, and Fishell G (2017). Genetic and activity-dependent mechanisms underlying interneuron diversity. Nat. Rev. Neurosci 18, 299– 309. 28381833
  26. [30]Martinez-de-la-Torre M, Pombal MA, and Puelles L (2011). Distal-less-like protein distribution in the larval lamprey forebrain. Neuroscience 178, 270– 284. 21185911
  27. [31]Quintana-Urzainqui I, Rodriguez-Moldes I, Mazan S, and Candal E (2015). Tangential migratory pathways of subpallial origin in the embryonic telencephalon of sharks: evolutionary implications. Brain Struct. Funct 220, 2905– 2926. 25079345
  28. [32]Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, and Jones KR (2002). Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J. Neurosci 22, 6309– 6314. 12151506 PMC6758181
  29. [33]Letinic K, Zoncu R, and Rakic P (2002). Origin of GABAergic neurons in the human neocortex. Nature 417, 645– 649. 12050665
  30. [34]Naumann RK, and Laurent G (2017). Function and evolution of the reptilian cerebral cortex. In Evolution of Nervous Systems, Volume 1, 2nd Edition, Kaas JH and Striedter G, eds. (Oxford: Academic Press), pp. 491– 518.
  31. [35]Harris KD, and Shepherd GM (2015). The neocortical circuit: themes and variations. Nat. Neurosci 18, 170– 81. 25622573 PMC4889215
  32. [37]Ulinski PS (1983). Dorsal Ventricular Ridge: A Treatise on Forebrain Organization in Reptiles and Birds (New York: John Wiley & Sons).
  33. [38]Herrick CJ (1948). The Brain of the Tiger Salamander, Ambystoma Tigrinum (Chicago: The University of Chicago Press).
  34. [39]Braford MR Jr., and Northcutt RG (1974). Olfactory bulb projections in the bichir, Polypterus. J. Comp. Neurol 156, 165– 178. 4418625
  35. [40]Briscoe SD, and Ragsdale CW (2018). Homology, neocortex, and the evolution of developmental mechanisms. Science 362, 190– 193. 30309947 PMC11098553
  36. [41]Wagner GP (2014). Homology, Genes, and Evolutionary Innovation (Princeton: Princeton University Press).
  37. [42]Patterson C (1988). Homology in classical and molecular biology. Mol. Biol. Evol 5, 603– 625. 3065587
  38. [43]Ataman B, Boulting GL, Harmin DA, Yang MG, Baker-Salisbury M, Yap EL, Malik AN, Mei K, Rubin AA, Spiegel I, (2016). Evolution of Osteocrin as an activity-regulated factor in the primate brain. Nature 539, 242– 247. 27830782 PMC5499253
  39. [45]Sousa AMM, Zhu Y, Raghanti MA, Kitchen RR, Onorati M, Tebbenkamp ATN, Stutz B, Meyer KA, Li M, Kawasawa YI, (2017). Molecular and cellular reorganization of neural circuits in the human lineage. Science 358, 1027– 1032. 29170230 PMC5776074
  40. [46]Lui JH, Nowakowski TJ, Pollen AA, Javaherian A, Kriegstein AR, and Oldham MC (2014). Radial glia require PDGFD-PDGFRβ signalling in human but not mouse neocortex. Nature 515, 264– 268. 25391964 PMC4231536
  41. [47]Rakic P (1995). A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18, 383– 388. 7482803
  42. [48]Brodmann K, and Garey LJ (2006). Brodmann’s Localisation in the Cerebral Cortex (New York: Springer).
  43. [49]Nieuwenhuys R, Voogd J, and van Huijzen C (2008). The Human Central Nervous System, 4th Edition. (New York: Springer).
  44. [50]Lui JH, Hansen DV, and Kriegstein AR (2011). Development and evolution of the human neocortex. Cell 146, 18– 36. 21729779 PMC3610574
  45. [51]Sherwood CC, Bauernfeind AL, Bianchi S, Raghanti MA, and Hof PR (2012). Human brain evolution writ large and small. Prog. Brain Res 195, 237– 254. 22230630
  46. [52]Sousa AMM, Meyer KA, Santpere G, Gulden FO, and Sestan N (2017). Evolution of the human nervous system function, structure, and development. Cell 170, 226– 247. 28708995 PMC5647789
  47. [53]Giandomenico SL, and Lancaster MA (2017). Probing human brain evolution and development in organoids. Curr. Opin. Cell Biol 44, 36– 43. 28157638
  48. [54]Mitchell C, and Silver DL (2018). Enhancing our brains: Genomic mechanisms underlying cortical evolution. Semin. Cell Dev. Biol 76, 23– 32. 28864345 PMC5832537
  49. [55]Borrell V, and Calegari F (2014). Mechanisms of brain evolution: regulation of neural progenitor cell diversity and cell cycle length. Neurosci. Res 86, 14– 24. 24786671
  50. [56]Florio M, and Huttner WB (2014). Neural progenitors, neurogenesis and the evolution of the neocortex. Development 141, 2182– 2194. 24866113
  51. [57]Fiddes IT, Lodewijk GA, Mooring M, Bosworth CM, Ewing AD, Mantalas GL, Novak AM, van den Bout A, Bishara A, Rosenkrantz JL, (2018). Human-specific NOTCH2NL genes affect notch signaling and cortical neurogenesis. Cell 173, 1356– 1369.e22. 29856954 PMC5986104
  52. [58]Suzuki IK, Gacquer D, Van Heurck R, Kumar D, Wojno M, Bilheu A, Herpoel A, Lambert N, Cheron J, Polleux F, (2018). Human-specific NOTCH2NL genes expand cortical neurogenesis through Delta/Notch regulation. Cell 173, 1370– 1384 e16. 29856955 PMC6092419
  53. [59]Florio M, Heide M, Pinson A, Brandl H, Albert M, Winkler S, Wimberger P, Huttner WB, and Hiller M (2018). Evolution and cell-type specificity of human-specific genes preferentially expressed in progenitors of fetal neocortex. eLife 7, e32332. 29561261 PMC5898914
  54. [60]Kalebic N, Gilardi C, Albert M, Namba T, Long KR, Kostic M, Langen B, and Huttner WB (2018). Human-specific ARHGAP11B induces hallmarks of neocortical expansion in developing ferret neocortex. eLife 7, e41241. 30484771 PMC6303107
  55. [61]Kronenberg ZN, Fiddes IT, Gordon D, Murali S, Cantsilieris S, Meyerson OS, Underwood JG, Nelson BJ, Chaisson MJP, Dougherty ML, (2018). High-resolution comparative analysis of great ape genomes. Science 360, eaar6343. 29880660 PMC6178954
  56. [62]Prufer K, de Filippo C, Grote S, Mafessoni F, Korlevic P, Hajdinjak M, Vernot B, Skov L, Hsieh P, Peyregne S, (2017). A high-coverage Neandertal genome from Vindija Cave in Croatia. Science 358, 655– 658. 28982794 PMC6185897
  57. [64]Nowakowski TJ, Pollen AA, Sandoval-Espinosa C, and Kriegstein AR (2016). Transformation of the radial glia scaffold demarcates two stages of human cerebral cortex development. Neuron 91, 1219– 1227. 27657449 PMC5087333
  58. [65]Smaers JB, Gomez-Robles A, Parks AN, and Sherwood CC (2017). Exceptional evolutionary expansion of prefrontal cortex in great apes and humans. Curr. Biol 27, 714– 720. 28162899
  59. [66]Sneve MH, Grydeland H, Rosa MGP, Paus T, Chaplin T, Walhovd K, and Fjell AM (2018). High-expanding regions in primate cortical brain evolution support supramodal cognitive flexibility. Cereb. Cortex bhy 268, 1– 11. 30357354
  60. [68]Charrier C, Joshi K, Coutinho-Budd J, Kim JE, Lambert N, de Marchena J, Jin WL, Vanderhaeghen P, Ghosh A, Sassa T, (2012). Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine maturation. Cell 149, 923– 935. 22559944 PMC3357949
  61. [69]Dennis MY, Nuttle X, Sudmant PH, Antonacci F, Graves TA, Nefedov M, Rosenfeld JA, Sajjadian S, Malig M, Kotkiewicz H, (2012). Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell 149, 912– 922. 22559943 PMC3365555
  62. [70]Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, (2009). Uniquely hominid features of adult human astrocytes. J. Neurosci 29, 3276– 3287. 19279265 PMC2819812
  63. [71]Han X, Chen M, Wang F, Windrem M, Wang S, Shanz S, Xu Q, Oberheim NA, Bekar L, Betstadt S, (2013). Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 12, 342– 353. 23472873 PMC3700554
  64. [72]Miller IF, Barton RA, and Nunn CL (2019). Quantitative uniqueness of human brain evolution revealed through phylogenetic comparative analysis. eLife 8, e41250. 30702428 PMC6379089
  65. [75]Lewitus E, and Huttner WB (2015). Neurodevelopmental lincRNA microsyteny conservation and mammalian brain size evolution. PLoS ONE 10, e0131818. 26134977 PMC4489927
  66. [76]Raghanti MA, Munger EL, Wicinski B, Butti C, and Hof PR (2017). Comparative structure of the cerebral cortex in large mammals. In Evolution of Nervous Systems, Volume 2, 2nd Edition, Kaas JH and Herculano-Houzel S, eds. (Oxford: Academic Press), pp. 267– 289.
  67. [78]Martinez-Cerdeno V, and Noctor SC (2016). Cortical evolution 2015: discussion of neural progenitor cell nomenclature. J. Comp. Neurol 524, 704– 709. 26439982 PMC4706766
  68. [79]Smart IH, Dehay C, Giroud P, Berland M, and 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. 11734531 PMC1931430
  69. [80]Fietz SA, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D, Fish JL, Corbeil D, Riehn A, Distler W, Nitsch R, (2010). OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci 13, 690– 699. 20436478
  70. [81]Reillo I, de Juan Romero C, Garcia-Cabezas MA, and Borrell V (2011). A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb. Cortex 21, 1674– 1694. 21127018
  71. [82]Johnson MB, Sun X, Kodani A, Borges-Monroy R, Girskis KM, Ryu SC, Wang PP, Patel K, Gonzalez DM, Woo YM, (2018). Aspm knockout ferret reveals an evolutionary mechanism governing cerebral cortical size. Nature 556, 370– 375. 29643508 PMC6095461
  72. [83]Sauerland C, Menzies BR, Glatzle M, Seeger J, Renfree MB, and Fietz SA (2018). The basal radial glia occurs in marsupials and underlies the evolution of an expanded neocortex in therian mammals. Cereb. Cortex 28, 145– 157. 29253253
  73. [84]Shitamukai A, Konno D, and 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, 3683– 3695. 21389223 PMC6622781
  74. [85]Vaid S, Camp JG, Hersemann L, Eugster Oegema C, Heninger AK, Winkler S, Brandl H, Sarov M, Treutlein B, Huttner WB, (2018). A novel population of Hopx-dependent basal radial glial cells in the developing mouse neocortex. Development 145, dev169276. 30266827
  75. [87]Pollen AA, Nowakowski TJ, Chen J, Retallack H, Sandoval-Espinosa C, Nicholas CR, Shuga J, Liu SJ, Oldham MC, Diaz A, (2015). Molecular identity of human outer radial glia during cortical development. Cell 163, 55– 67. 26406371 PMC4583716
  76. [88]Johnson MB, Wang PP, Atabay KD, Murphy EA, Doan RN, Hecht JL, and Walsh CA (2015). Single-cell analysis reveals transcriptional heterogeneity of neural progenitors in human cortex. Nat. Neurosci 18, 637– 646. 25734491 PMC5568903
  77. [89]Fish JL, Kosodo Y, Enard W, Paabo S, and Huttner WB (2006). Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc. Natl. Acad. Sci. USA 103, 10438– 10443. 16798874 PMC1502476
  78. [90]Montgomery SH, and Mundy NI (2014). Microcephaly genes evolved adaptively throughout the evolution of eutherian mammals. BMC Evol. Biol 14, 120. 24898820 PMC4055943
  79. [91]Arcila ML, Betizeau M, Cambronne XA, Guzman E, Doerflinger N, Bouhallier F, Zhou H, Wu B, Rani N, Bassett DS, (2014). Novel primate miRNAs coevolved with ancient target genes in germinal zone-specific expression patterns. Neuron 81, 1255– 1262. 24583023 PMC4020629
  80. [92]Liu J, Liu W, Yang L, Wu Q, Zhang H, Fang A, Li L, Xu X, Sun L, Zhang J, (2017). The primate-specific gene TMEM14B marks outer radial glia cells and promotes cortical expansion and folding. Cell Stem Cell 21, 635– 649.e8. 29033352
  81. [93]O’Neill AC, Kyrousi C, Klaus J, Leventer RJ, Kirk EP, Fry A, Pilz DT, Morgan T, Jenkins ZA, Drukker M, (2018). A primate-specific isoform of PLEKHG6 regulates neurogenesis and neuronal migration. Cell Rep 25, 2729– 2741.e6. 30517861
  82. [94]Krubitzer LA, and Prescott TJ (2018). The combinatorial creature: Cortical phenotypes within and across lifetimes. Trends Neurosci 41, 744– 762. 30274608
  83. [95]Kaas JH (2013). The evolution of brains from early mammals to humans. Wiley Interdiscip. Rev. Cogn. Sci 4, 33– 45. 23529256 PMC3606080
  84. [96]Klingler E (2017). Development and organization of the evolutionarily conserved three-layered olfactory cortex. eNeuro 4, ENEURO.0193–16.2016. PMC5272922 28144624
  85. [97]Hevner RF (2016). Evolution of the mammalian dentate gyrus. J. Comp. Neurol 524, 578– 594. 26179319 PMC4706817
  86. [98]Falcone C, Wolf-Ochoa M, Amina S, Hong T, Vakilzadeh G, Hopkins WD, Hof PR, Sherwood CC, Manger PR, Noctor SC, (2019). Cortical interlaminar astrocytes across the therian mammal radiation. J. Comp. Neurol, 1654– 1674. 30552685 PMC6465161
  87. [100]Tsuboi M, van der Bijl W, Kopperud BT, Erritzoe J, Voje KL, Kotrschal A, Yopak KE, Collin SP, Iwaniuk AN, and Kolm N (2018). Breakdown of brain-body allometry and the encephalization of birds and mammals. Nat. Ecol. Evol 2, 1492– 1500. 30104752
  88. [102]Azevedo FA, Carvalho LR, Grinberg LT, Farfel JM, Ferretti RE, Leite RE, Jacob Filho W, Lent R, and 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. 19226510
  89. [103]Clayton NS, and Emery NJ (2015). Avian models for human cognitive neuroscience: a proposal. Neuron 86, 1330– 1342. 26087161
  90. [104]Gruber R, Schiestl M, Boeckle M, Frohnwieser A, Miller R, Gray RD, Clayton NS, and Taylor AH (2019). New caledonian crows use mental representations to solve metatool problems. Curr. Biol 29, 686– 692.e3. 30744978 PMC6384166
  91. [105]Briscoe SD, Albertin CB, Rowell JJ, and Ragsdale CW (2018). Neocortical association cell types in the forebrain of birds and alligators. Curr. Biol 28, 686– 696. 29456143 PMC11098552
  92. [106]Dugas-Ford J, Rowell JJ, and Ragsdale CW (2012). Cell-type homologies and the origins of the neocortex. Proc. Natl. Acad. Sci. USA 109, 16974– 16979. 23027930 PMC3479531
  93. [107]Jarvis ED, Yu J, Rivas MV, Horita H, Feenders G, Whitney O, Jarvis SC, Jarvis ER, Kubikova L, Puck AE, (2013). Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns. J. Comp. Neurol 521, 3614– 3665. 23818122 PMC4145244
  94. [110]Butler AB (1994). The evolution of the dorsal pallium in the telencephalon of amniotes: cladistic analysis and a new hypothesis. Brain Res. Rev 19, 66– 101. 8167660
  95. [111]Behroozi M, Billings BK, Helluy X, Manger PR, Gunturkun O, and Strockens F (2018). Functional MRI in the Nile crocodile: a new avenue for evolutionary neurobiology. Proc. Royal Soc. B 285, 20180178. PMC5936729 29695446
  96. [112]Briscoe SD, and Ragsdale CW (2018). Molecular anatomy of the alligator dorsal telencephalon. J. Comp. Neurol 526, 1613– 1646. 29520780 PMC6242290
  97. [113]Tosches MA, Yamawaki TM, Naumann RK, Jacobi AA, Tushev G, and Laurent G (2018). Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science 360, 881– 888. 29724907
  98. [114]Reiner A (2000). A hypothesis as to the organization of cerebral cortex in the common amniote ancestor of modern reptiles and mammals. In Evolutionary Developmental Biology of the Cerebral Cortex, Volume 228, Bock GA and Cardew G, eds. (West Susex, England: John Wiley & Sons), pp. 83– 102. 10929318
  99. [115]Roth G, Laberge F, Muhlenbrock-Lenter S, and Grunwald W (2007). Organization of the pallium in the fire-bellied toad Bombina orientalis. I: Morphology and axonal projection pattern of neurons revealed by intracellular biocytin labeling. J. Comp. Neurol 501, 443– 464. 17245707
  100. [116]Northcutt RG (1981). Evolution of the telencephalon in nonmammals. Annu. Rev. Neurosci 4, 301– 350. 7013637
  101. [117]Northcutt RG, and Ronan M (1992). Afferent and efferent connections of the bullfrog medial pallium. Brain Behav. Evol 40, 1– 16. 1393516
  102. [118]Schmidt A, and Wake MH (1997). Cellular migration and morphological complexity in the caecilian brain. J. Morphol 231, 11– 27. 29852703
  103. [119]Gonzalez A, Lopez JM, Morona R, and Moreno N (2017). The organization of the central nervous system of amphibians. In Evolution of Nervous Systems, Volume 1, 2nd Edition, Kaas JH and Striedter G, eds. (Oxford: Academic Press), pp. 141– 170.
  104. [120]Medina L, and Reiner A (2000). Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23, 1– 12. 10631781
  105. [121]Supin AY, and Guselnikov VI (1965). Representation of visual, auditory and somatosensory systems in frog forebrain. Fed. Proc. Transl. Suppl 24, 357– 62. 14304784
  106. [122]Karamian AI, Vesselkin NP, Belekhova MG, and Zagorulko TM (1966). Electrophysiological characteristics of tectal and thalamo-cortical divisions of the visual system in lower vertebrates. J. Comp. Neurol 127, 559– 576. 5968991
  107. [123]Mudry KM, and Capranica RR (1980). Evoked auditory activity within the telencephalon of the bullfrog (Rana catesbeiana). Brain Res 182, 303– 311. 6965601
  108. [124]Abellan A, Desfilis E, and Medina L (2014). Combinatorial expression of Lef1, Lhx2, Lhx5, Lhx9, Lmo3, Lmo4, and Prox1 helps to identify comparable subdivisions in the developing hippocampal formation of mouse and chicken. Front. Neuroanat 8, 59. 25071464 PMC4082316
  109. [125]Arendt D, Musser JM, Baker CVH, Bergman A, Cepko C, Erwin DH, Pavlicev M, Schlosser G, Widder S, Laubichler MD, (2016). The origin and evolution of cell types. Nat. Rev. Genet 17, 744– 757. 27818507
  110. [126]Ebbesson SO (1980). The parcellation theory and its relation to interspecific variability in brain organization, evolutionary and ontogenetic development, and neuronal plasticity. Cell Tissue Res 213, 179– 212. 7459999
  111. [127]Roth G, Nishikawa KC, Naujoks-Manteuffel C, Schmidt A, and Wake DB (1993). Paedomorphosis and simplification in the nervous system of salamanders. Brain Behav. Evol 42, 137– 170. 8364715
  112. [128]Moreno N, Lopez JM, Morona R, Lozano D, Jimenez S, and Gonzalez A (2018). Comparative analysis of Nkx2.1 and Islet-1 expression in urodele amphibians and lungfishes highlights the pattern of forebrain organization in early tetrapods. Front. Neuroanat 12, 42. 29867380 PMC5968111
  113. [129]Amemiya CT, Alfoldi J, Lee AP, Fan S, Philippe H, Maccallum I, Braasch I, Manousaki T, Schneider I, Rohner N, (2013). The African coelacanth genome provides insights into tetrapod evolution. Nature 496, 311– 316. 23598338 PMC3633110
  114. [130]Northcutt RG (2008). Forebrain evolution in bony fishes. Brain Res. Bull 75, 191– 205. 18331871
  115. [131]Ravi V, and Venkatesh B (2018). The divergent genomes of teleosts. Annu. Rev. Anim. Biosci 6, 47– 68. 29447475
  116. [132]Braasch I, Gehrke AR, Smith JJ, Kawasaki K, Manousaki T, Pasquier J, Amores A, Desvignes T, Batzel P, Catchen J, (2016). The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nat. Genet 48, 427– 437. 26950095 PMC4817229
  117. [133]Ganz J, Kaslin J, Freudenreich D, Machate A, Geffarth M, and Brand M (2012). Subdivisions of the adult zebrafish subpallium by molecular marker analysis. J. Comp. Neurol 520, 633– 655. 21858823
  118. [134]Maruska KP, Butler JM, Field KE, and Porter DT (2017). Localization of glutamatergic, GABAergic, and cholinergic neurons in the brain of the African cichlid fish, Astatotilapia burtoni. J. Comp. Neurol 525, 610– 638. 27507772
  119. [135]Kawaguchi M, Hagio H, Yamamoto N, Matsumoto K, Nakayama K, Akazome Y, Izumi H, Tsuneoka Y, Suto F, Murakami Y, (2019). Atlas of the telencephalon based on cytoarchitecture, neurochemical markers, and gene expressions in Rhinogobius flumineus [Mizuno, 1960]. J. Comp. Neurol 527, 874– 900. 30516281
  120. [136]Braford MR Jr. (2009). Stalking the everted telencephalon: comparisons of forebrain organization in basal ray-finned fishes and teleosts. Brain Behav. Evol 74, 56– 76. 19729896
  121. [137]Nieuwenhuys R (2011). The development and general morphology of the telencephalon of actinopterygian fishes: synopsis, documentation and commentary. Brain Struct. Funct 215, 141– 157. 20976604 PMC3041917
  122. [138]Giassi AC, Harvey-Girard E, Valsamis B, and Maler L (2012). Organization of the gymnotiform fish pallium in relation to learning and memory: I. cytoarchitectonics and cellular morphology. J. Comp. Neurol 520, 3314– 3337. 22430983
  123. [139]Trinh AT, Harvey-Girard E, Teixeira F, and Maler L (2016). Cryptic laminar and columnar organization in the dorsolateral pallium of a weakly electric fish. J. Comp. Neurol 524, 408– 428. 26234725
  124. [140]Elliott SB, Harvey-Girard E, Giassi AC, and Maler L (2017). Hippocampal-like circuitry in the pallium of an electric fish: possible substrates for recursive pattern separation and completion. J. Comp. Neurol 525, 8– 46. 27292574
  125. [141]Striedter GF, and Northcutt RG (2006). Head size constrains forebrain development and evolution in ray-finned fishes. Evol. Dev 8, 215– 222. 16509899
  126. [142]Mueller T, and Wullimann MF (2009). An evolutionary interpretation of teleostean forebrain anatomy. Brain Behav. Evol 74, 30– 42. 19729894
  127. [143]Northcutt RG (2011). Do teleost fishes possess a homolog of mammalian isocortex? Brain Behav. Evol 78, 136– 138. 21952091
  128. [144]Folgueira M, Bayley P, Navratilova P, Becker TS, Wilson SW, and Clarke JD (2012). Morphogenesis underlying the development of the everted teleost telencephalon. Neural Dev 7, 32. 22989074 PMC3520737
  129. [145]Yamamoto N, Ishikawa Y, Yoshimoto M, Xue HG, Bahaxar N, Sawai N, Yang CY, Ozawa H, and Ito H (2007). A new interpretation on the homology of the teleostean telencephalon based on hodology and a new eversion model. Brain Behav. Evol 69, 96– 104. 17230017
  130. [146]Ito H, and Yamamoto N (2009). Non-laminar cerebral cortex in teleost fishes? Biol. Lett 5, 117– 121. 18832057 PMC2657732
  131. [147]Harvey-Girard E, Giassi AC, Ellis W, and Maler L (2012). Organization of the gymnotiform fish pallium in relation to learning and memory: iv. expression of conserved transcription factors and implications for the evolution of dorsal telencephalon. J. Comp. Neurol 520, 3395– 3413. 22430363
  132. [148]Wallach A, Harvey-Girard E, Jun JJ, Longtin A, and Maler L (2018). A time-stamp mechanism may provide temporal information necessary for egocentric to allocentric spatial transformations. eLife 7, e36769. 30465523 PMC6264071
  133. [149]Broglio C, Rodriguez F, Gomez A, Arias JL, and Salas C (2010). Selective involvement of the goldfish lateral pallium in spatial memory. Behav. Brain Res 210, 191– 201. 20178818
  134. [150]Ganz J, Kroehne V, Freudenreich D, Machate A, Geffarth M, Braasch I, Kaslin J, and Brand M (2014). Subdivisions of the adult zebrafish pallium based on molecular marker analysis. F1000Research 3, 308. 25713698 PMC4335597
  135. [151]Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM, Swann JB, Ohta Y, Flajnik MF, Sutoh Y, Kasahara M, (2014). Elephant shark genome provides unique insights into gnathostome evolution. Nature 505, 174– 179. 24402279 PMC3964593
  136. [152]Boisvert CA, Johnston P, Trinajstic K, and Johanson Z (2019). Chondrichthyan evolution, diversity, and senses. In Heads, Jaws, and Muscles: Anatomical, Functional, and Developmental Diversity in Chordate Evolution, Ziermann JM, Diaz RE Jr and Diogo R, eds. (Cham: Springer International Publishing), pp. 65– 91.
  137. [153]Smeets WJAJ, Nieuwenhuys R, and Roberts BL (1983). The Central Nervous System of Cartilaginous Fishes: Structure and Functional Correlations (Berlin; New York: Springer-Verlag).
  138. [155]Yopak KE (2012). Neuroecology of cartilaginous fishes: the functional implications of brain scaling. J. Fish Biol 80, 1968– 2023. 22497414
  139. [157]Schluessel V (2015). Who would have thought that ‘jaws’ also has brains? Cognitive functions in elasmobranchs. Anim. Cogn 18, 19– 37. 24889655
  140. [158]Kuba MJ, Byrne RA, and Burghardt GM (2010). A new method for studying problem solving and tool use in stingrays (Potamotrygon castexi). Anim. Cogn 13, 507– 513. 20020169
  141. [159]Thonhauser KE, Gutnick T, Byrne RA, Kral K, Burghardt GM, and Kuba MJ (2013). Social learning in Cartilaginous fish (stingrays Potamotrygon falkneri). Anim. Cogn 16, 927– 932. 23529289
  142. [160]Guttridge TL, van Dijk S, Stamhuis EJ, Krause J, Gruber SH, and Brown C (2013). Social learning in juvenile lemon sharks, Negaprion brevirostris. Anim. Cogn 16, 55– 64. 22933179
  143. [161]Cohen DH, Duff TA, and Ebbesson SO (1973). Electrophysiological identification of a visual area in shark telencephalon. Science 182, 492– 494. 4744177
  144. [163]Docampo-Seara A, Lagadec R, Mazan S, Rodriguez MA, Quintana-Urzainqui I, and Candal E (2018). Study of pallial neurogenesis in shark embryos and the evolutionary origin of the subventricular zone. Brain Struct. Funct 223, 3593– 3612. 29980930
  145. [164]Gillis JA, Modrell MS, and Baker CV (2013). Developmental evidence for serial homology of the vertebrate jaw and gill arch skeleton. Nat. Commun 4, 1436. 23385581 PMC3600657
  146. [165]Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N, Campbell MS, Yandell MD, Manousaki T, Meyer A, Bloom OE, (2013). Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat. Genet 45, 415– 421. 23435085 PMC3709584
  147. [167]Wicht H, and Northcutt RG (1992). The forebrain of the Pacific hagfish: a cladistic reconstruction of the ancestral craniate forebrain. Brain Behav. Evol 40, 25– 64. 1393518
  148. [168]Heimberg AM, Cowper-Sal·lari R, Sémon M, Donoghue PCJ, and Peterson KJ (2010). MicroRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc. Natl. Acad. Sci. USA 107, 19379. 20959416 PMC2984222
  149. [169]Miyashita T, Coates MI, Farrar R, Larson P, Manning PL, Wogelius RA, Edwards NP, Anné J, Bergmann U, Palmer AR, (2019). Hagfish from the cretaceous tethys sea and a reconciliation of the morphological–molecular conflict in early vertebrate phylogeny. Proc. Natl. Acad. Sci. USA 116, 2146– 2151. 30670644 PMC6369785
  150. [170]Shimeld SM, and Donoghue PCJ (2012). Evolutionary crossroads in developmental biology: cyclostomes (lamprey and hagfish). Development 139, 2091– 2099. 22619386
  151. [171]Wicht H, and Northcutt RG (1994). An immunohistochemical study of the telencephalon and the diencephalon in a Myxinoid jawless fish, the Pacific hagfish, Eptatretus stouti. Brain Behav. Evol 43, 140– 161. 7514941
  152. [172]Wicht H, and Northcutt RG (1998). Telencephalic connections in the Pacific hagfish (Eptatretus stouti), with special reference to the thalamopallial system. J. Comp. Neurol 395, 245– 260. 9603376
  153. [173]Pombal MA, Alvarez-Otero R, Perez-Fernandez J, Solveira C, and Megias M (2011). Development and organization of the lamprey telencephalon with special reference to the GABAergic system. Front. Neuroanat 5, 20. 21442003 PMC3062466
  154. [174]Ocana FM, Suryanarayana SM, Saitoh K, Kardamakis AA, Capantini L, Robertson B, and Grillner S (2015). The lamprey pallium provides a blueprint of the mammalian motor projections from cortex. Curr. Biol 25, 413– 423. 25619762
  155. [175]Suryanarayana SM, Robertson B, Wallen P, and Grillner S (2017). The lamprey pallium provides a blueprint of the mammalian layered cortex. Curr. Biol 27, 3264– 3277.e5. 29056451
  156. [176]Naumann RK, Ondracek JM, Reiter S, Shein-Idelson M, Tosches MA, Yamawaki TM, and Laurent G (2015). The reptilian brain. Curr. Biol 25, R317– R321. 25898097 PMC4406946
  157. [177]Giassi AC, Ellis W, and Maler L (2012). Organization of the gymnotiform fish pallium in relation to learning and memory: iii. intrinsic connections. J. Comp. Neurol 520, 3369– 3394. 22434647
  158. [178]Kokoros JJ, and Northcutt RG (1977). Telencephalic efferents of the tiger salamander Ambystoma tigrinum tigrinum (Green). J. Comp. Neurol 173, 613– 628. 864026
  159. [179]Suárez R, Paolino A, Fenlon LR, Morcom LR, Kozulin P, Kurniawan ND, and Richards LJ (2018). A pan-mammalian map of interhemispheric brain connections predates the evolution of the corpus callosum. Proc. Natl. Acad. Sci. USA 115, 9622. 30181276 PMC6156618
  160. [180]Pani AM, Mullarkey EE, Aronowicz J, Assimacopoulos S, Grove EA, and Lowe CJ (2012). Ancient deuterostome origins of vertebrate brain signalling centres. Nature 483, 289– 294. 22422262 PMC3719855
  161. [181]Hejnol A, and Lowe CJ (2015). Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution. Phil. Trans. R. Soc. B 370, 20150045. 26554039 PMC4650123
  162. [182]Martin-Duran JM, Pang K, Borve A, Le HS, Furu A, Cannon JT, Jondelius U, and Hejnol A (2018). Convergent evolution of bilaterian nerve cords. Nature 553, 45– 50. 29236686 PMC5756474
  163. [183]Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, (2008). The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064– 1071. 18563158
  164. [184]Horie T, Shinki R, Ogura Y, Kusakabe TG, Satoh N, and Sasakura Y (2011). Ependymal cells of chordate larvae are stem-like cells that form the adult nervous system. Nature 469, 525– 528. 21196932
  165. [185]Delsuc F, Brinkmann H, Chourrout D, and Philippe H (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965– 968. 16495997
  166. [186]Northcutt RG (2005). The new head hypothesis revisited. J. Exp. Zool. (Mol. Dev. Evol.) 304B, 274– 297. 16003768
  167. [187]Holland LZ (2015). The origin and evolution of chordate nervous systems. Phil. Trans. R. Soc. B 370, 20150048. 26554041 PMC4650125
  168. [188]Albuixech-Crespo B, Lopez-Blanch L, Burguera D, Maeso I, Sanchez-Arrones L, Moreno-Bravo JA, Somorjai I, Pascual-Anaya J, Puelles E, Bovolenta P, (2017). Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain. PLoS Biol 15, e2001573. 28422959 PMC5396861
  169. [189]Benito Gutierrez E, Stemmer M, Rohr SD, Schumacher LN, Tang J, Marconi A, Jekely G, and Arendt D (2018). Patterning of a telencephalon-like region in the adult brain of amphioxus. bioRxiv, 307629. 10.1101/307629 · DOI
  170. [191]Sugahara F, Aota S, Kuraku S, Murakami Y, Takio-Ogawa Y, Hirano S, and Kuratani S (2011). Involvement of Hedgehog and FGF signalling in the lamprey telencephalon: evolution of regionalization and dorsoventral patterning of the vertebrate forebrain. Development 138, 1217– 1226. 21343370
  171. [192]Oda I, and Saiga H (2001). Hremx, the ascidian homologue of ems/emx, is expressed in the anterior and posterior-lateral epidermis but not in the central nervous system during embryogenesis. Dev. Genes Evol 211, 291– 298. 11466524
  172. [193]Krubitzer L (2007). The magnificent compromise: cortical field evolution in mammals. Neuron 56, 201– 208. 17964240
  173. [194]Miller CT, Hale ME, Okano H, Okabe S, and Mitra P (2019). Comparative principles for next-generation neuroscience. Front. Behav. Neurosci 13, 12. 30787871 PMC6373779
  174. [195]Pollen AA, Dobberfuhl AP, Scace J, Igulu MM, Renn SC, Shumway CA, and Hofmann HA (2007). Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain Behav. Evol 70, 21– 39. 17389793
  175. [196]Haberly LB (1983). Structure of the piriform cortex of the opossum. I. Description of neuron types with Golgi methods. J. Comp. Neurol 213, 163– 187. 6841668
  176. [197]Coleman J, and Clerici WJ (1981). Organization of thalamic projections to visual cortex in opossum. Brain Behav. Evol 18, 41– 59. 7237104
  177. [198]Northcutt RG, and Royce GJ (1975). Olfactory bulb projections in the bullfrog Rana catesbeiana. J. Morphol 145, 251– 267. 1078857
  178. [199]Northcutt RG, and Gonzalez A (2011). A reinterpretation of the cytoarchitectonics of the telencephalon of the comoran coelacanth. Front. Neuroanat 5, 9. 21373374 PMC3046466

Authors
Briscoe, S. D., & Ragsdale, C. W.
Affiliations
  • Max Planck Institute of Molecular Cell Biology and Genetics (DE)
  • University of Chicago (US)
Corresponding author
Briscoe, Steven D.
Venue
Current Biology
Publisher
Elsevier BV
Published
2019-07
Volume
29
Issue
13
Pages
R647-R662
ISSN
0960-9822 (ISSN-L)
OpenAlex
W2956452028
Cited by
75
References
204
Citations by year
2026: 5 · 2025: 8 · 2024: 13 · 2023: 12 · 2022: 12 · 2021: 16 · 2020: 6 · 2019: 3
FWCI
0.82
Type
journal article
Language
en
Open access
Locations
  • Current Biology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
  • Alexander von Humboldt-Stiftung
  • European Molecular Biology Organization (ALTF 1014-2018)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
Keywords
neocortex evolution, chordate phylogeny, non-mammalian vertebrates, reptiles, amphibians, Chondrichthyes, cyclostomes, invertebrate chordates, homology, cortical organization, evolutionary innovation, human cognition
MeSH terms
Animals, Biological Evolution, Telencephalon, Chordata

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review