The subventricular zone is the developmental milestone of a 6-layered neocortex: Comparisons in metatherian and eutherian mammals

Cerebral Cortex

Volumn 20, Issue 5, 2010, Pages 1071-1081

  Cheung, Amanda F P ^a   Kondo, Shinichi ^a   Abdel Mannan, Omar ^a   Chodroff, Rebecca A ^a   Sirey, Tamara M ^a   Bluy, Lisa E ^a   Webber, Natalie ^a   Deproto, Jamin ^a   Karlen, Sarah J ^b   Krubitzer, Leah ^b   Stolp, Helen B ^a,c   Saunders, Norman R ^c   Molnár, Zoltán ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Basal progenitors; Cortical neurogenesis; Cortical unit column; Evolutionary biology of cerebral cortex; Intermediate progenitors; Monodelphis domestica

Indexed keywords

MESSENGER RNA;

ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL DIVISION; COMPARATIVE STUDY; GENE EXPRESSION; MAMMAL; MARSUPIAL; MOUSE; NEOCORTEX; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OPOSSUM; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; RODENT; STEM CELL; SUBVENTRICULAR ZONE; WALLABY;

ANIMALS; ANIMALS, NEWBORN; CELL COUNT; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; LATERAL VENTRICLES; MACROPODIDAE; MITOTIC SPINDLE APPARATUS; MONODELPHIS; NEOCORTEX; NEURONS; PREGNANCY; RATS; RATS, WISTAR;

EID: 77951114376     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp168     Document Type: Article

References (60)

1. Abdel-Mannan O, Cheung AFP, Molnar Z. 2008. Evolution of cortical neurogenesis. Brain Res Bull. 75(2-4):398-404. (Pubitemid 351335168)
2. Anderson SA, Marin O, Horn C, Jennings K, Rubenstein JL. 2001. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development. 128(3):353-363. (Pubitemid 32184376)
3. Arnold SJ, Huang GJ, Cheung AFP, Era T, Nishikawa S, Bikoff EK, Molnar Z, Robertson EJ, Groszer M. 2008. The T-box transcription factor Eomes/Tbr2 regulates neurogenesis in the cortical subven-tricular zone. Genes Dev. 22(18):2479-2484.
4. Bhide PG. 1996. Cell cycle kinetics in the embryonic mouse corpus striatum. J Comp Neurol. 374(4):506-522.
5. Brodmann K. 1909. Vergleichende Localisationslehre der Grosshirnride in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig (Germany): J.A.Barth.
6. Bystron I, Blakemore C, Rakic P. 2008. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci. 9(2):110-122.
7. Carney R. 2005. Thalamocortical development and cell proliferation in fetal primate and rodent cortex [DPhil thesis]. Oxford: University of Oxford.
8. Carney RS, Bystron I, Lopez-Bendito G, Molnar Z. 2007. Comparative analysis of extra-ventricular mitoses at early stages of cortical development in rat and human. Brain Struct Funct. 212(1):37-54. (Pubitemid 47036750)
9. Cheung AFP, Pollen AA, Tavare A, DeProto J, Molnar Z. 2007. Comparative aspects of cortical neurogenesis in vertebrates. J Anat. 211(2):164-176. (Pubitemid 47278549)
10. Cobos I, Puelles L, Martinez S. 2001. The avian telencephalic subpallium originates inhibitory neurons that invade tangentially the pallium (dorsal ventricular ridge and cortical areas). Dev Biol. 239(1):30-45. (Pubitemid 33052051)
11. Cubelos B, Sebastian-Serrano A, Kim S, Moreno-Ortiz C, Redondo JM, Walsh CA, Nieto M. 2008. Cux-2 controls the proliferation of neuronal intermediate precursors of the cortical subventricular zone. Cereb Cortex. 18(8):1758-1770. (Pubitemid 352019896)
12. Dehay C, Kennedy H. 2007. Cell-cycle control and cortical development. Nat Rev Neurosci. 8(6):438-450. (Pubitemid 46789227)
13. Dziegielewska KM, Hinds LA, Møllgard K, Reynolds ML, Saunders NR. 1988. Blood-brain, blood-cerebrospinal fluid and cerebrospinal fluid-brain barriers in a marsupial (Macropus eugenii) during development. J Physiol. 403:367-388.
14. Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF. 2005. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci. 25(1):247-251.
15. Farkas LM, Haffner C, Giger T, Khaitovich P, Nowick K, Birchmeier C, Paabo S, Huttner WB. 2008. Insulinoma-associated 1 has a panneuro-genic role and promotes the generation and expansion of basal progenitors in the developing mouse neocortex. Neuron. 60(1): 40-55.
16. Fish JL, Dehay C, Kennedy H, Huttner WB. 2008. Making bigger brains-the evolution of neural-progenitor-cell division. J Cell Sci. 121(Pt 17):2783-2793.
17. 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. (Pubitemid 38327757)
18. Haug H. 1987. Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). Am J Anat. 180(2):126-142.
19. Herculano-Houzel S, Collins CE, Wong P, Kaas JH, Lent R. 2008. The basic uniformity of the cerebral cortex. Proc Natl Acad Sci USA. 105(34):12593-12598.
20. Kaas JH. 2006. Evolution of the neocortex. Curr Biol. 16(21): R910-R914.
21. 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. (Pubitemid 46829605)
22. Karten HJ. 1969. The organization of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon. Ann New York Acad Sci. 167:164-179.
23. Karten HJ. 1997. Evolutionary developmental biology meets the brain: the origins of mammalian cortex. Proc Natl Acad Sci USA. 94(7): 2800-2804.
24. Konno D, Shioi G, Shitamukai A, Mori A, Kiyonari H, Miyata T, Matsuzaki F. 2008. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat Cell Biol. 10(1):93-101.
25. Kosodo Y, Roper K, Haubensak W, Marzesco AM, Corbeil D, Huttner WB. 2004. Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithe-lial cells. EMBO J. 23(11):2314-2324. (Pubitemid 38833240)
26. Kowalczyk T, Pontious A, Englund C, Daza RA, Bedogni F, Hodge R, Attardo A, Bell C, Huttner WB, Hevner RF. 2009. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex. Advance Access published January 23, doi:10.1093/cercor/ bhn260.
27. Kriegstein S, 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. (Pubitemid 44624180)
28. Kumar SB, Hedges S. 2002. Genomics. Vertebrate genomes compared. Science. 297(5585):1283-1285.
29. Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M, Kennedy H, Dehay C. 2005. G1 phase regulation, area-specific cell-cycle control and cytoarchitectonics in the primate cortex. Neuron. 47(3):353-364. (Pubitemid 41073877)
30. Marin O, Rubenstein J. 2003. Cell migration in the forebrain. Annu Rev Neurosci. 26:441-483. (Pubitemid 37064941)
31. Mark RF, Marotte LR. 1992. Australian marsupials as models for the developing mammalian visual system. Trends in Neurosci. 15(2):51-57.
32. 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.
33. Metin C, Alvarez C, Moudoux D, Vitalis T, Pieau C, Molnar Z. 2007. Conserved pattern of tangential neuronal migration during fore-brain development. Development. 134(15):2815-2827. (Pubitemid 47305056)
34. 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.
35. Molnar Z, Knott GW, Blakemore C, Saunders NR. 1998. Development of thalamocortical projections in the South American grey short-tailed opossum (Monodelphis domestica). J Comp Neurol. 398(4):491-514.
36. Molnar 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.
37. Molnar Z, Tavare A, Cheung AFP. 2006. The origin of neocortex: lessons from comparative embryology. Evolution of Nervous System, Vol.3. In: Kaas JH, Krubitzer LA, editors. The evolution of nervous systems in mammals. Oxford: Elsevier. p. 13-26.
38. Moreno N, Gonzalez A, Retaux S. 2008. Evidences for tangential migrations in Xenopus telencephalon: developmental patterns and cell tracking experiments. Dev Neurobiol. 68(4):504-520.
39. Murphy WJ, Pevzner PA, O'Brien SJ. 2004. Mammalian phylogenomics comes of age. Trends Genet. 20(12):631-639.
40. Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, Khoury SJ, Cunningham J, Gotz M, Walsh CA. 2004. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J Comp Neurol. 479(2):168-180.
41. 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.
42. Northcutt RG, Kaas J. 1995. The emergence and evolution of mammalian neocortex. Trends Neurosci. 18(9):373-379.
43. Parnavelas JG, Nadarajah B. 2001. Radial glial cells. Are they really glia? Neuron. 31(6):881-884.
44. Pontious A, Kowalczyk T, Englund C, Hevner RF. 2007. Role of intermediate progenitor cells in cerebral cortex development. Dev Neurosci. 30(1-3):24-32.
45. Rakic P. 1988. Defects of neuronal migration and the pathogenesis of cortical malformations. Prog Brain Res. 73:15-37.
46. 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.
47. Rakic P. 2008. Confusing cortical columns. Proc Natl Acad Sci USA. 105(34):12099-12100.
48. Reynolds ML, Cavanagh ME, Dziegielewska KM, Hinds LA, Saunders NR, Tyndale-Biscoe CH. 1985. Postnatal development of the telenceph-alon of the tammar wallaby (Macropus eugenii). An accessible model of neocortical differentiation. Anat Embryol (Berl). 173(1):81-94.
49. Rockel AJ, Hiorns RW, Powell TP. 1980. The basic uniformity in structure of the neocortex. Brain. 103(2):221-244.
50. Saunders NR, Adam E, Reader M, Møllgard K. 1989. Monodelphis domestica (grey short-tailed opossum): an accessible model for studies of early neocortical development. Anat Embryol (Berl). 180(3):227-236.
51. 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.
52. Smart IH, Dehay C, Giroud P, Berland M, Kennedy H. 2002. Unique morphological features of the proliferative zones and postmi-totic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex. 12(1): 37-53.
53. Striedter GF, Charvet CJ. 2008. Developmental origins of species differences in telencephalon and tectum size: morphometric comparisons between a parakeet (Melopsittacus undulatus) and a quail (Colinus virgianus). J Comp Neurol. 507(5):1663-1675.
54. Stubbs D, DeProto J, Englund C, Mahmud I, Hevner R, Molnar Z. 2009. Neurovascular congruence during cerebral cortical development. Cereb Cortex. 19(Suppl 1):i32-i41
55. Takahashi T, Nowakowski RS, Caviness VS, Jr. 1995. Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J Neurosci. 15(9):6058-6068.
56. Tarabykin V, Stoykova A, Usman N, Gruss P. 2001. Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development. 128(11):1983-1993.
57. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25(24):4876-4882.
58. Tuorto F, Alifragis P, Failla V, Parnavelas JG, Gulisano M. 2003. Tangential migration of cells from the basal to the dorsal telencephalic regions in the chick. Eur J Neurosci. 18(12):3388-3393.
59. Vidyasagar TR, Wye-Dvorak J, Henry GH, Mark RF. 1992. Cytoarch-itecture and visual field representation in area 17 of the tammar wallaby (Macropus eugenii). J Comp Neurol. 325(2):291-300.
60. Wu SX, Goebbels S, Nakamura K, Nakamura K, Kometani K, Minato N, Kaneko T, Nave KA, Tamamaki N. 2005. Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc Natl Acad Sci USA. 102(47):17172-17177.