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Transformation of the Radial Glia Scaffold Demarcates Two Stages of Human Cerebral Cortex Development

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Nowakowski, Tomasz J., Pollen, Alex A., Sandoval-Espinosa, Carmen, Kriegstein, Arnold R.·2016·Neuron

Abstract

The classic view of cortical development, embodied in the radial unit hypothesis highlights the ventricular radial glia (vRG) scaffold as a key architectonic feature of the developing neocortex. The scaffold includes continuous fibers spanning the thickness of the developing cortex during neurogenesis across mammals. However, we find that in humans, the scaffold transforms into a physically discontinuous structure during the transition from infragranular to supragranular neuron production. As a consequence of this transformation, supragranular layer neurons arrive at their terminal positions in the cortical plate along outer radial glia (oRG) cell fibers. In parallel, the radial glia that contact the ventricle develop a distinct “truncated” morphology and a unique gene expression profile. We propose a supragranular layer expansion hypothesis that posits a deterministic role of oRG cells in the radial and tangential expansion of supragranular layers in primates, with implications for patterns of neuronal migration, area patterning, and cortical folding.

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Research works printed but not linked: 51

  1. Betizeau, 2013, Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate, Neuron, 80, 442, 10.1016/j.neuron.2013.09.032 · DOI · Paper page
  2. Borrell, 2010, In vivo gene delivery to the postnatal ferret cerebral cortex by DNA electroporation, J. Neurosci. Methods, 186, 186, 10.1016/j.jneumeth.2009.11.016 · DOI
  3. Camp, 2015, Human cerebral organoids recapitulate gene expression programs of fetal neocortex development, Proc. Natl. Acad. Sci. USA, 112, 15672, 10.1073/pnas.1520760112 · DOI · Paper page
  4. Caviness, 1978, Mechanisms of cortical development: a view from mutations in mice, Annu. Rev. Neurosci., 1, 297, 10.1146/annurev.ne.01.030178.001501 · DOI · Paper page
  5. Chenn, 2002, Regulation of cerebral cortical size by control of cell cycle exit in neural precursors, Science, 297, 365, 10.1126/science.1074192 · DOI · Paper page
  6. de Juan Romero, 2015, Discrete domains of gene expression in germinal layers distinguish the development of gyrencephaly, EMBO J., 34, 1859, 10.15252/embj.201591176 · DOI
  7. deAzevedo, 2003, Cortical radial glial cells in human fetuses: depth-correlated transformation into astrocytes, J. Neurobiol., 55, 288, 10.1002/neu.10205 · DOI · Paper page
  8. Dehay, 1989, Maturation and connectivity of the visual cortex in monkey is altered by prenatal removal of retinal input, Nature, 337, 265, 10.1038/337265a0 · DOI
  9. Dehay, 1996, Contribution of thalamic input to the specification of cytoarchitectonic cortical fields in the primate: effects of bilateral enucleation in the fetal monkey on the boundaries, dimensions, and gyrification of striate and extrastriate cortex, J. Comp. Neurol., 367, 70, 10.1002/(SICI)1096-9861(19960325)367:1<70::AID-CNE6>3.0.CO;2-G · DOI
  10. Dehay, 2001, Cell-cycle kinetics of neocortical precursors are influenced by embryonic thalamic axons, J. Neurosci., 21, 201, 10.1523/JNEUROSCI.21-01-00201.2001 · DOI
  11. Elias, 2007, Gap junction adhesion is necessary for radial migration in the neocortex, Nature, 448, 901, 10.1038/nature06063 · DOI · Paper page
  12. Feng, 2004, Mitotic spindle regulation by Nde1 controls cerebral cortical size, Neuron, 44, 279, 10.1016/j.neuron.2004.09.023 · DOI · Paper page
  13. Florio, 2014, Neural progenitors, neurogenesis and the evolution of the neocortex, Development, 141, 2182, 10.1242/dev.090571 · DOI · Paper page
  14. Frantz, 1996, Restriction of late cerebral cortical progenitors to an upper-layer fate, Neuron, 17, 55, 10.1016/S0896-6273(00)80280-9 · DOI · Paper page
  15. Granger, 1995, Tempo of neurogenesis and synaptogenesis in the primate cingulate mesocortex: comparison with the neocortex, J. Comp. Neurol., 360, 363, 10.1002/cne.903600212 · DOI
  16. Gruber, 2011, MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway, Nat. Cell Biol., 13, 1325, 10.1038/ncb2342 · DOI
  17. Haubensak, 2004, Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis, Proc. Natl. Acad. Sci. USA, 101, 3196, 10.1073/pnas.0308600100 · DOI · Paper page
  18. Haydar, 1999, The role of cell death in regulating the size and shape of the mammalian forebrain, Cereb. Cortex, 9, 621, 10.1093/cercor/9.6.621 · DOI
  19. Hutsler, 2005, Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species, Brain Res., 1052, 71, 10.1016/j.brainres.2005.06.015 · DOI
  20. Kriegstein, 2006, Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion, Nat. Rev. Neurosci., 7, 883, 10.1038/nrn2008 · DOI · Paper page
  21. Lizarraga, 2010, Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors, Development, 137, 1907, 10.1242/dev.040410 · DOI · Paper page
  22. Lukaszewicz, 2005, G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex, Neuron, 47, 353, 10.1016/j.neuron.2005.06.032 · DOI · Paper page
  23. Malik, 2013, Neurogenesis continues in the third trimester of pregnancy and is suppressed by premature birth, J. Neurosci., 33, 411, 10.1523/JNEUROSCI.4445-12.2013 · DOI
  24. McConnell, 1988, Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation, J. Neurosci., 8, 945, 10.1523/JNEUROSCI.08-03-00945.1988 · DOI · Paper page
  25. McConnell, 1991, Cell cycle dependence of laminar determination in developing neocortex, Science, 254, 282, 10.1126/science.1925583 · DOI · Paper page
  26. Mota, 2015, BRAIN STRUCTURE. Cortical folding scales universally with surface area and thickness, not number of neurons, Science, 349, 74, 10.1126/science.aaa9101 · DOI · Paper page
  27. Nowakowski, 2013, Loss of functional Dicer in mouse radial glia cell-autonomously prolongs cortical neurogenesis, Dev. Biol., 382, 530, 10.1016/j.ydbio.2013.08.023 · DOI
  28. Ohtaka-Maruyama, 2015, Molecular pathways underlying projection neuron production and migration during cerebral cortical development, Front. Neurosci., 9, 447, 10.3389/fnins.2015.00447 · DOI
  29. Pawlisz, 2011, Three-dimensional regulation of radial glial functions by Lis1-Nde1 and dystrophin glycoprotein complexes, PLoS Biol., 9, e1001172, 10.1371/journal.pbio.1001172 · DOI
  30. Pollen, 2015, Molecular identity of human outer radial glia during cortical development, Cell, 163, 55, 10.1016/j.cell.2015.09.004 · DOI · Paper page
  31. Rakic, 1978, Neuronal migration and contact guidance in the primate telencephalon, Postgrad. Med. J., 54, 25
  32. Rakic, 2003, Developmental and evolutionary adaptations of cortical radial glia, Cereb. Cortex, 13, 541, 10.1093/cercor/13.6.541 · DOI · Paper page
  33. Rakic, 2003, Elusive radial glial cells: historical and evolutionary perspective, Glia, 43, 19, 10.1002/glia.10244 · DOI · Paper page
  34. Rakic, 1968, Autoradiographic study of supravital DNA synthesis in fetal human brain, J. Neuropathol. Exp. Neurol., 27, 139, 10.1097/00005072-196804000-00006 · DOI
  35. Rakic, 1968, Supravital DNA synthesis in the developing human and mouse brain, J. Neuropathol. Exp. Neurol., 27, 246, 10.1097/00005072-196804000-00006 · DOI
  36. Reillo, 2012, Germinal zones in the developing cerebral cortex of ferret: ontogeny, cell cycle kinetics, and diversity of progenitors, Cereb. Cortex, 22, 2039, 10.1093/cercor/bhr284 · DOI
  37. Reillo, 2011, A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex, Cereb. Cortex, 21, 1674, 10.1093/cercor/bhq238 · DOI · Paper page
  38. Richman, 1975, Mechanical model of brain convolutional development, Science, 189, 18, 10.1126/science.1135626 · DOI · Paper page
  39. Schmechel, 1979, Arrested proliferation of radial glial cells during midgestation in rhesus monkey, Nature, 277, 303, 10.1038/277303a0 · DOI
  40. Sidman, 1973, Neuronal migration, with special reference to developing human brain: a review, Brain Res., 62, 1, 10.1016/0006-8993(73)90617-3 · DOI · Paper page
  41. Stahl, 2013, Trnp1 regulates expansion and folding of the mammalian cerebral cortex by control of radial glial fate, Cell, 153, 535, 10.1016/j.cell.2013.03.027 · DOI · Paper page
  42. Sun, 2014, Growth and folding of the mammalian cerebral cortex: from molecules to malformations, Nat. Rev. Neurosci., 15, 217, 10.1038/nrn3707 · DOI · Paper page
  43. Takahashi, 1993, Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse, J. Neurosci., 13, 820, 10.1523/JNEUROSCI.13-02-00820.1993 · DOI · Paper page
  44. Tallinen, 2016, On the growth and form of cortical convolutions, Nat. Physics., 13, 588, 10.1038/nphys3632 · DOI · Paper page
  45. Thomsen, 2016, Fixed single-cell transcriptomic characterization of human radial glial diversity, Nat. Methods, 13, 87, 10.1038/nmeth.3629 · DOI
  46. Tsai, 2012, Regional astrocyte allocation regulates CNS synaptogenesis and repair, Science, 337, 358, 10.1126/science.1222381 · DOI · Paper page
  47. Van Essen, 1997, A tension-based theory of morphogenesis and compact wiring in the central nervous system, Nature, 385, 313, 10.1038/385313a0 · DOI · Paper page
  48. Wang, 2016, Hedgehog signaling promotes basal progenitor expansion and the growth and folding of the neocortex, Nat. Neurosci., 19, 888, 10.1038/nn.4307 · DOI · Paper page
  49. Workman, 2013, Modeling transformations of neurodevelopmental sequences across mammalian species, J. Neurosci., 33, 7368, 10.1523/JNEUROSCI.5746-12.2013 · DOI · Paper page
  50. Yingling, 2008, Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division, Cell, 132, 474, 10.1016/j.cell.2008.01.026 · DOI · Paper page
  51. Zhang, 2015, MicroRNA-mediated non-cell-autonomous regulation of cortical radial glial transformation revealed by a Dicer1 knockout mouse model, Glia, 63, 860, 10.1002/glia.22789 · DOI

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Metadata

Authors
Nowakowski, T. J., Pollen, A. A., Sandoval-Espinosa, C., & Kriegstein, A. R.
Venue
Neuron
Publisher
Elsevier BV
Published
2016-09
Volume
91
Issue
6
Pages
1219-1227
ISSN
0896-6273 (ISSN-L)
OpenAlex
W2521106965
Cited by
353
References
15
FWCI
11.62
Type
journal article
Language
en
Open access
bronze
Licence

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Nowakowski, T. J., Pollen, A. A., Sandoval-Espinosa, C., & Kriegstein, A. R. (2016). Transformation of the Radial Glia Scaffold Demarcates Two Stages of Human Cerebral Cortex Development. Neuron. https://doi.org/10.1016/j.neuron.2016.09.005

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