Direct and indirect neurogenesis generate a mosaic of distinct glutamatergic projection neuron types in cerebral cortex.

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    • Source:
      Publisher: Cell Press Country of Publication: United States NLM ID: 8809320 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1097-4199 (Electronic) Linking ISSN: 08966273 NLM ISO Abbreviation: Neuron Subsets: MEDLINE
    • Publication Information:
      Original Publication: [Cambridge, Mass. : Cell Press, c1988-
    • Subject Terms:
    • Abstract:
      Variations in size and complexity of the cerebral cortex result from differences in neuron number and composition, rooted in evolutionary changes in direct and indirect neurogenesis (dNG and iNG) that are mediated by radial glia and intermediate progenitors (IPs), respectively. How dNG and iNG differentially contribute to neuronal number, diversity, and connectivity are unknown. Establishing a genetic fate-mapping method to differentially visualize dNG and iNG in mice, we found that while both dNG and iNG contribute to all cortical structures, iNG contributes the largest relative proportions to the hippocampus and neocortex. Within the neocortex, whereas dNG generates all major glutamatergic projection neuron (PN) classes, iNG differentially amplifies and diversifies PNs within each class; the two pathways generate distinct PN types and assemble fine mosaics of lineage-based cortical subnetworks. Our results establish a ground-level lineage framework for understanding cortical development and evolution by linking foundational progenitor types and neurogenic pathways to PN types.
      Competing Interests: Declaration of interests The authors declare no competing interests.
      (Copyright © 2023 Elsevier Inc. All rights reserved.)
    • References:
      Nat Rev Neurosci. 2009 Oct;10(10):724-35. (PMID: 19763105)
      Nature. 2001 Feb 8;409(6821):714-20. (PMID: 11217860)
      Nat Neurosci. 2015 Feb;18(2):170-81. (PMID: 25622573)
      Nat Commun. 2019 Sep 2;10(1):3946. (PMID: 31477701)
      Cell Rep. 2016 Jun 28;16(1):92-105. (PMID: 27320921)
      Development. 2021 Jul 15;148(14):. (PMID: 34170322)
      Development. 2004 Jul;131(13):3133-45. (PMID: 15175243)
      Science. 2018 May 25;360(6391):881-888. (PMID: 29724907)
      Neurosci Res. 2001 Sep;41(1):51-60. (PMID: 11535293)
      Nat Rev Genet. 2016 Dec;17(12):744-757. (PMID: 27818507)
      Elife. 2020 Aug 25;9:. (PMID: 32840212)
      Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3196-201. (PMID: 14963232)
      Neuron. 2016 Oct 19;92(2):555. (PMID: 27764676)
      Cell Mol Life Sci. 2020 Apr;77(8):1435-1460. (PMID: 31563997)
      Cell. 2014 Jun 19;157(7):1552-64. (PMID: 24949968)
      Science. 2018 Oct 12;362(6411):190-193. (PMID: 30309947)
      Curr Opin Cell Biol. 2021 Dec;73:9-18. (PMID: 34098196)
      Cereb Cortex. 2019 Mar 1;29(3):1121-1138. (PMID: 29415216)
      Biol Lett. 2009 Feb 23;5(1):134-7. (PMID: 18842571)
      Neuron. 2001 Sep 13;31(5):727-41. (PMID: 11567613)
      Cereb Cortex. 2010 May;20(5):1071-81. (PMID: 19726493)
      J Neurosci. 2013 Feb 27;33(9):4165-80. (PMID: 23447624)
      Cell. 2018 Aug 23;174(5):1264-1276.e15. (PMID: 30057116)
      J Neurosci. 2015 Apr 15;35(15):6142-52. (PMID: 25878286)
      Cell. 2021 Jun 10;184(12):3222-3241.e26. (PMID: 34004146)
      Development. 2014 Jun;141(11):2182-94. (PMID: 24866113)
      Cereb Cortex. 2015 Oct;25(10):3290-302. (PMID: 24927931)
      Nat Rev Neurosci. 2006 Nov;7(11):883-90. (PMID: 17033683)
      J Anat. 2019 Sep;235(3):616-625. (PMID: 30677129)
      Cereb Cortex. 2006 Jul;16 Suppl 1:i152-61. (PMID: 16766701)
      Cereb Cortex. 2009 Oct;19(10):2439-50. (PMID: 19168665)
      Development. 2018 Sep 14;145(17):. (PMID: 30217810)
      Science. 1971 Jul 16;173(3993):254-6. (PMID: 5087492)
      Brain Behav Evol. 2022;96(4-6):318-333. (PMID: 34192700)
      Brain Sci. 2020 Nov 26;10(12):. (PMID: 33255945)
      Toxicol Pathol. 2017 Aug;45(6):705-744. (PMID: 28891434)
      Nat Neurosci. 2004 Feb;7(2):136-44. (PMID: 14703572)
      Cell. 2018 Jul 26;174(3):590-606.e21. (PMID: 29961574)
      Neuron. 2011 Oct 20;72(2):269-84. (PMID: 22017987)
      Curr Top Dev Biol. 2021;142:1-66. (PMID: 33706916)
      Annu Rev Cell Dev Biol. 2014;30:465-502. (PMID: 25000993)
      J Neurosci. 2002 Aug 1;22(15):6309-14. (PMID: 12151506)
      Development. 2016 Jan 1;143(1):66-74. (PMID: 26732839)
      Science. 2012 Aug 10;337(6095):746-9. (PMID: 22879516)
      Curr Biol. 2015 Feb 16;25(4):413-23. (PMID: 25619762)
      Nature. 2018 Nov;563(7729):72-78. (PMID: 30382198)
      Proc Natl Acad Sci U S A. 2012 Oct 16;109(42):16974-9. (PMID: 23027930)
      Science. 2021 Feb 12;371(6530):. (PMID: 33574185)
      Nature. 2021 Oct;598(7879):182-187. (PMID: 34616069)
    • Grant Information:
      DP1 MH129954 United States MH NIMH NIH HHS; F30 MH108333 United States MH NIMH NIH HHS; F32 NS096877 United States NS NINDS NIH HHS; U19 MH114821 United States MH NIMH NIH HHS
    • Contributed Indexing:
      Keywords: PyNs; dNG; direct neurogenesis; fate mapping; iNG; indirect neurogenesis; neocortex; pallium; pyramidal neurons
    • Publication Date:
      Date Created: 20230622 Date Completed: 20230821 Latest Revision: 20240817
    • Publication Date:
      20240817
    • Accession Number:
      PMC10527425
    • Accession Number:
      10.1016/j.neuron.2023.05.021
    • Accession Number:
      37348506