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Gliogenesis in the outer subventricular zone promotes enlargement and gyrification of the primate cerebrum
Open accessAbstract
Significance: The formation of cortical convolutions of primates, including humans, is one of the most important subjects in developmental neuroscience, but the underlying mechanisms—considered mostly solved toward the end of the 20th century—have become controversial in the last decade. Recent studies suggest that a stem cell zone called the outer subventricular zone (oSVZ) induces gyri to form directly through neurogenesis. Here, we provide evidence in macaque monkey demonstrating that oSVZ neurogenesis is actually complete before gyrification begins and that a major function of the oSVZ is to produce the glial cells associated with the rapid expansion and folding of the cortical surface.
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“In nonhuman primates and human, glial cells seem to somewhat outnumber neurons in the PFC, albeit with regional variation which is likely to contribute to the formation of secondary and tertiary gyri [77–81].”
From Development of prefrontal cortex (2022) · cites this paper as [77]
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Citations
Cites
Specification of Cerebral Cortical Areas
Rakic, P. (1988) · Science · doi:10.1126/science.3291116 · Cited by 3,127 · cited 3×
“Surgical manipulations including enucleation of the eyes creates changes in white matter ingrowth to the visual cortex, leading to massive changes in the magnitude and pattern of gyrification (2).”
BackgroundMethodSelf-citationCellular Scaling Rules for the Brains of Marsupials: Not as “Primitive” as Expected
Santos, S. E. D., Porfírio, J., Cunha, F., Manger, P. R., Tavares, W. C., Pessôa, L. M., Raghanti, M. A., Sherwood, C. C., & Herculano‐Houzel, S. (2017) · Brain Behavior and Evolution · doi:10.1159/000452856 · Cited by 2,652
Azevedo, F. A. C., Carvalho, L. R. B., Grinberg, L. T., Farfel, J. M., Ferretti, R. E. L., Leite, R. E. P., Filho, W. J., Lent, R., & Herculano‐Houzel, S. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21974 · Cited by 2,337
Mode of cell migration to the superficial layers of fetal monkey neocortex
Rakic, P. (1972) · Journal of Comparative Neurology · doi:10.1002/cne.901450105 · Cited by 2,170
Self-citationNeurons derived from radial glial cells establish radial units in neocortex
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., & Kriegstein, A. R. (2001) · Nature · doi:10.1038/35055553 · Cited by 2,016
A tension-based theory of morphogenesis and compact wiring in the central nervous system
Essen, D. C. V. (1997) · Nature · doi:10.1038/385313a0 · Cited by 1,668
Evolution of the neocortex: a perspective from developmental biology
Rakic, P. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2719 · Cited by 1,565
Self-citationNeurogenic radial glia in the outer subventricular zone of human neocortex
Hansen, D. V., Lui, J. H., Parker, P. R. L., & Kriegstein, A. R. (2010) · Nature · doi:10.1038/nature08845 · Cited by 1,388
Rakic, P. (1974) · Science · doi:10.1126/science.183.4123.425 · Cited by 1,161
Self-citationGleeson, J. G., Allen, K. M., Fox, J. W., Lamperti, E. D., Berkovic, S. F., Scheffer, I. E., Cooper, E. C., Dobyns, W. B., Minnerath, S., Ross, M. E., et al. (1998) · Cell · doi:10.1016/s0092-8674(00)80899-5 · Cited by 1,110
Rakic, P. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)93934-p · Cited by 1,047
Self-citationDevelopment of the human cerebral cortex: Boulder Committee revisited
Bystron, I., Blakemore, C., & Rakic, P. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2252 · Cited by 977
Self-citationMolecular Identity of Human Outer Radial Glia during Cortical Development
Pollen, A. A., Nowakowski, T. J., Chen, J., Retallack, H., Sandoval-Espinosa, C., Nicholas, C. R., Shuga, J., Liu, S. J., Oldham, M. C., Diaz, A., et al. (2015) · Cell · doi:10.1016/j.cell.2015.09.004 · Cited by 908
Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion
Kriegstein, A., Noctor, S., & Martínez-Cerdeño, V. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn2008 · Cited by 738
Schmechel, D. E., & RAKIC, P. T. (1979) · Anatomy and Embryology · doi:10.1007/bf00300010 · Cited by 682
Self-citationCell-cycle control and cortical development
Dehay, C., & Kennedy, H. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2097 · Cited by 655 · cited 1×
“The oSVZ compartment becomes very prominent in primates, including humans, and contains detached RGCs (11), recently renamed as outer radial glia (oRG) or basal radial glia (bRG) (5).”
BackgroundA Role for Intermediate Radial Glia in the Tangential Expansion of the Mammalian Cerebral Cortex
Reillo, I., Romero, C. D. J., García‐Cabezas, M. Á., & Borrell, V. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq238 · Cited by 655
Development of cortical folding during evolution and ontogeny
Zilles, K., Palomero‐Gallagher, N., & Amunts, K. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.01.006 · Cited by 567
Why Does Cerebral Cortex Fissure and Fold?
Welker, W. I. (1990) · Cerebral cortex · doi:10.1007/978-1-4615-3824-0_1 · Cited by 433
Levitt, P. R., Cooper, M., & RAKIC, P. T. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-01-00027.1981 · Cited by 395
Self-citationA functional role for EGFR signaling in myelination and remyelination
Aguirre, A. A., Dupree, J. L., Mangin, J., & Gallo, V. (2007) · Nature Neuroscience · doi:10.1038/nn1938 · Cited by 352
Stahl, R., Walcher, T., Romero, C. D. J., Pilz, G.-A., Cappello, S., Irmler, M., Sanz-Aquela, J. M., Beckers, J., Blum, R., Borrell, V., et al. (2013) · Cell · doi:10.1016/j.cell.2013.03.027 · Cited by 267
Evolutionarily Dynamic Alternative Splicing of GPR56 Regulates Regional Cerebral Cortical Patterning
Bae, B.-I., Tietjen, I., Atabay, K. D., Evrony, G. D., Johnson, M. B., Asare, E., Wang, P. P., Murayama, A. Y., Im, K., Lisgo, S. N., et al. (2014) · Science · doi:10.1126/science.1244392 · Cited by 229 · cited 1×
“, lissencephaly and polymicrogyria (12, 13).”
The development of cortical connections
Price, D. J., Kennedy, H., Dehay, C., Zhou, L., Mercier, M., Jossin, Y., Goffinet, A. M., Tissir, F., Blakey, D., & Molnár, Z. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04620.x · Cited by 223
Asymmetry-Defective Oligodendrocyte Progenitors Are Glioma Precursors
Sugiarto, S., Persson, A. I., González-Muñoz, E., Waldhuber, M., Lamagna, C., Andor, N., Hanecker, P., Ayers-Ringler, J. R., Phillips, J. J., Siu, J. J., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.08.011 · Cited by 223
Kelava, I., Reillo, I., Murayama, A. Y., Kalinka, A. T., Stenzel, D., Tomančák, P., Matsuzaki, F., Lebrand, C., Sasaki, E., Schwamborn, J. C., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr301 · Cited by 217
Asymmetric Distribution of EGFR Receptor during Mitosis Generates Diverse CNS Progenitor Cells
Sun, Y., Goderie, S. K., & Temple, S. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.045 · Cited by 212
Martínez-Cerdeño, V., Cunningham, C. L., Camacho, J., Antczak, J. L., Prakash, A. N., Cziep, M. E., Walker, A. I., & Noctor, S. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030178 · Cited by 203
Reillo, I., & Borrell, V. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr284 · Cited by 184
García‐Moreno, F., Vasistha, N. A., Trévia, N., Bourne, J. A., & Molnár, Z. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr312 · Cited by 154
How Cells Fold the Cerebral Cortex
Borrell, V. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1106-17.2017 · Cited by 143
Cortical Malformations: Lessons in Human Brain Development
Subramanian, L., Calcagnotto, M. E., & Paredes, M. F. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00576 · Cited by 138
Cerebral cortical development in rodents and primates
Molnár, Z., & Clowry, G. J. (2012) · Progress in brain research · doi:10.1016/b978-0-444-53860-4.00003-9 · Cited by 137
How Forces Fold the Cerebral Cortex
Kroenke, C. D., & Bayly, P. V. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1105-17.2017 · Cited by 132
Namba, T., & Huttner, W. Β. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.256 · Cited by 120
Cheung, A. F. P., Kondo, S., Abdel‐Mannan, O., Chodroff, R. A., Sirey, T., Bluy, L. E., Webber, N., DeProto, J., Karlen, S. J., Krubitzer, L. A., et al. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp168 · Cited by 106
Cellular Scaling Rules for the Brains of an Extended Number of Primate Species
Gabi, M., Collins, C. E., Wong, P., Torres, L. B., Kaas, J. H., & Herculano-Houzel, S. (2010) · Brain, Behavior and Evolution · doi:10.1159/000319872 · Cited by 102
FGF Signaling Expands Embryonic Cortical Surface Area by Regulating Notch-Dependent Neurogenesis
Rash, B. G., Lim, H., Breunig, J. J., & Vaccarino, F. M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4439-11.2011 · Cited by 97
Self-citationEvolution and development of the mammalian cerebral cortex
Molnár, Z., Kaas, J. H., de Carlos, J. A., Hevner, R. F., Lein, E., & Němec, P. (2014) · Brain Behavior and Evolution · doi:10.1159/000357753 · Cited by 93
Aguirre, A. A., & Gallo, V. (2007) · Neuron Glia Biology · doi:10.1017/s1740925x08000082 · Cited by 78
Accelerated evolution of oligodendrocytes in the human brain
Berto, S., Mendizabal, I., Usui, N., Toriumi, K., Chatterjee, P., Douglas, C., Tamminga, C. A., Preuss, T. M., Yi, S. V., & Konopka, G. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907982116 · Cited by 78
The (Not Necessarily) Convoluted Role of Basal Radial Glia in Cortical Neurogenesis
Hevner, R. F., & Haydar, T. F. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr336 · Cited by 56
Human fetal radial glia cells generate oligodendrocytes in vitro
Mo, Z., & Zečević, N. (2008) · Glia · doi:10.1002/glia.20775 · Cited by 45
Recent advances in understanding neocortical development
Borrell, V. (2019) · F1000Research · doi:10.12688/f1000research.20332.1 · Cited by 44
Güven, A., Kalebic, N., Long, K. R., Florio, M., Vaid, S., Brandl, H., Stenzel, D., & Huttner, W. Β. (2020) · eLife · doi:10.7554/elife.49808 · Cited by 44
Human brain development through the lens of cerebral organoid models
Andrews, M. G., & Nowakowski, T. J. (2019) · Brain Research · doi:10.1016/j.brainres.2019.146470 · Cited by 35
Cited by
Sorted by citations
Development and arealization of the cerebral cortex
Cadwell, C. R., Bhaduri, A., Mostajo-Radji, M. A., Keefe, M. G., & Nowakowski, T. J. (2019) · Neuron · doi:10.1016/j.neuron.2019.07.009 · Cited by 408
New insights into the development of the human cerebral cortex
Molnár, Z., Clowry, G. J., Šestan, N., Alzu’bi, A., Bakken, T. E., Hevner, R. F., Hüppi, P. S., Kostović, I., RAKIC, P. T., Anton, E. S., et al. (2019) · Journal of Anatomy · doi:10.1111/joa.13055 · Cited by 426
Self-citationDevelopment of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378
Self-citationUzquiano, A., Kedaigle, A. J., Pigoni, M., Paulsen, B. D. S., Adiconis, X., Kim, K., Faits, T., Nagaraja, S., Antón-Bolaños, N., Gerhardinger, C., et al. (2022) · Cell · doi:10.1016/j.cell.2022.09.010 · Cited by 257
Origins and Proliferative States of Human Oligodendrocyte Precursor Cells
Huang, W., Bhaduri, A., Velmeshev, D., Wang, S., Wang, L., Rottkamp, C. A., Álvarez-Buylla, A., Rowitch, D. H., & Kriegstein, A. R. (2020) · Cell · doi:10.1016/j.cell.2020.06.027 · Cited by 243
Metadata
- Authors
- Rash, B. G., Duque, A., Morozov, Y. M., Arellano, J. I., Micali, N., & Rakic, P.
- Affiliations
- Yale University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2019-03-20
- Volume
- 116
- Issue
- 14
- Pages
- 7089-7094
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC6452694
- OpenAlex
- W2923197044
- Semantic Scholar
- 8b7df27ef95b6ee2b283c9946cffa023751cdcb2
- Cited by
- 156
- References
- 46
- Citations by year
- 2026: 11 · 2025: 10 · 2024: 11 · 2023: 26 · 2022: 27 · 2021: 33 · 2020: 26 · 2019: 10
- FWCI
- 9.03
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- NIH (DA02399, EY002593)
- Dorys McConnell Duberg (Endowed Chair)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- outer subventricular zone, gliogenesis, cortical folding, cortical expansion, neurogenesis, glial cells, macaque, primate brain development
- MeSH terms
- PAX6 Transcription Factor, Animals, Astrocytes, Embryo, Mammalian, Macaca, Neurons, Oligodendroglia, Primates, Homeodomain Proteins, Lateral Ventricles, Tumor Suppressor Proteins, Cerebrum, Neurogenesis
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