The DOI matches its Crossref record; 46 of the 46 references it cites were found in a registry or an index.
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.
Overview
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.
Integrity signals
Registry
Cites
Statistics
Verification
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.
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 source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
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
Cited by
Sorted by citations
Items 101–155 of 155
Examining the NEUROG2 lineage and associated gene expression in human cortical organoids
Vasan, L., Chinchalongporn, V., Saleh, F., Zinyk, D. L., Ke, C., Suresh, H., Ghazale, H., Belfiore, L., Touahri, Y., Oproescu, A.-M., et al. (2024) · Development · doi:10.1242/dev.202703 · Cited by 8
Outer radial glia promotes white matter regeneration after neonatal brain injury
Jinnou, H., Rosko, L. M., Yamashita, S., Henmi, S., Prasad, J. D., Lam, V. K., Agaronyan, A., Tu, T., Imamura, Y., Kuboyama, K., et al. (2025) · Cell Reports Medicine · doi:10.1016/j.xcrm.2025.101986 · Cited by 5
Shaping the Neocortex: Radial Glia and Astrocytes in Development and Evolution
Mosti, F., Kawasaki, H., Babbitt, C. C., Benedetto, B. D., Silver, D. L., Kalebic, N., & Falcone, C. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1301-25.2025 · Cited by 5
Natsuyama, T., Okamoto, N., Watanabe, K., Chibaatar, E., Tesen, H., Hayasaki, G., Ikenouchi, A., Kakeda, S., & Yoshimura, R. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.1031386 · Cited by 5
Bobić‐Rasonja, M., Pogledić, I., Mitter, C., Štajduhar, A., Periša, M. M., Trnski, S., Bettelheim, D., Hainfellner, J. A., Judáš, M., Prayer, D., et al. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab030 · Cited by 5
Kriegstein, A. R., Subramanian, L., Obernier, K., & Álvarez-Buylla, A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814405-3.00031-x · Cited by 5
Marmoset Brain ISH Data Revealed Molecular Difference Between Cortical Folding Patterns
Li, X., Liu, T., Li, Y., Li, Q., Wang, X., Hu, X., Guo, L., Zhang, T., & Liu, T. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa317 · Cited by 5
Romero-Morales, A. I., & Gama, V. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.840265 · Cited by 5
Cortical gyrification morphology in PTSD: A neurobiological risk factor for severity?
Gharehgazlou, A., Richardson, J. D., Jetly, R., & Dunkley, B. T. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100299 · Cited by 4
Voltage-Gated Sodium Channels as Drug Targets in Epilepsy-Related Sodium Channelopathies
Wengert, E. R., Miralles, R. M., & Patel, M. K. (2024) · Springer eBooks · doi:10.1007/978-3-031-52197-3_4 · Cited by 4
Truncated radial glia as a common precursor in the late corticogenesis of gyrencephalic mammalsPreprint
Bilgic, M., Wu, Q., Suetsugu, T., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.05.490846 · Cited by 4
Diversity and Evolution of Human Cortical Progenitor Cell Types
Pollen, A. A., & Kriegstein, A. R. (2023) · Wiley eBooks · doi:10.1002/9781119860914.ch2 · Cited by 5
Išasegi, I. Ž., Kopić, J., Smilović, D., Krsnik, Ž., & Kostović, I. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab197 · Cited by 3
Lundin, A., Ricchiuto, P., Clausen, M., Hicks, R., Falk, A., & Herland, A. (2020) · Advanced Biosystems · doi:10.1002/adbi.201900226 · Cited by 3
Tang, J., Xie, Y., Liao, W., Zhang, Y., Yang, F., Zhao, L., Zhou, G., Zhang, Y., Jiang, H. F., & Xing, W. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac199 · Cited by 2
Teleost Fish and Organoids: Alternative Windows Into the Development of Healthy and Diseased Brains
Fasano, G., Compagnucci, C., Dallapiccola, B., Tartaglia, M., & Lauri, A. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.855786 · Cited by 2
Development and Developmental Disorders of the Cerebral Cortex
ten Donkelaar, H. J., Vasung, L., Molnár, Z., Aronica, E., Lammens, M. M. Y., van Bokhoven, H., Ulzen, K. K.-V., & Hori, A. (2023) · Springer eBooks · doi:10.1007/978-3-031-26098-8_10 · Cited by 3
From seed to flower: blossoming of microglia in development and brain repair
Neckles, V. N., & Feliciano, D. M. (2021) · Cell and Tissue Research · doi:10.1007/s00441-021-03486-9 · Cited by 2
Ayoub, A. E., Dominguez, M. H., Benoit, J., Ortega, J. A., Radonjić, N. V., Zečević, N., & RAKIC, P. T. (2019) · Brain Behavior and Evolution · doi:10.1159/000500494 · Cited by 1
Self-citationDuque, A., Barello, P., Greene, L., Burke, E., Mendoza-Silva, V., Morozov, Y. M., & RAKIC, P. T. (2025) · IntechOpen eBooks · doi:10.5772/intechopen.1011631 · Cited by 2
Self-citationSimply complex – the structure of the cerebellar neuronal lineage
Butts, T., & Wingate, R. J. T. (2026) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2026.01.012 · Cited by 1
Arellano, J. I., & RAKIC, P. T. (2023) · doi:10.1002/9781119860914.ch23 · Cited by 1
Self-citationTruncated radial glia as a common precursor in the late corticogenesis of gyrencephalic mammalsPreprint
Bilgic, M., Wu, Q., Suetsugu, T., et al. (2023) · eLife · doi:10.7554/elife.91406.1 · Cited by 1
Lead (Pb) exposure alters neural cell fate in the developing human brainPreprint
Sampson, M. M., Sonsurkar, S., Nieland, L., Pan, L., Kan, R. L., Azizad, D. J., Li, X., Kebede, N., Lane, A. R., D'Souza, P. E., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.14.670354 · Cited by 1
Cortical Thickness and Curvature in Autism and ADHD: A Mega-AnalysisPreprint
Mahmoudi, M., Moore, L. A., Lundquist, J. T., Stier, A., Anderson, M., Fayzullobekova, B., Hermosillo, R. J. M., Houghton, A., Madison, T. J., McCOLLUM, R. E., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.05.697782 · Cited by 1
Micali, N., Kim, S., Diaz-Bustamante, M., Stein-O’Brien, G., Seo, S., Shin, J. H., Rash, B. G., Ma, S., Wang, Y., Olivares, N. A., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/577544
Self-citationNeuroscience of developing axonal strata in the human fetal brain
Išasegi, I. Ž., Krsnik, Ž., & Kostović, I. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817986-4.00026-2
The Importance of Studying Human Brain
Jakovcevski, M., Mitrović, S., & Jakovčevski, I. (2021) · Serbian Journal of Experimental and Clinical Research · doi:10.2478/sjecr-2020-0065 · Cited by 1
Polydendrocytes – undifferentiated cells of the nervous system
Vikhareva, L. V., Novikov, E. I., Novikova, E. S., & Margaryan, A. V. (2022) · Journal of Anatomy and Histopathology · doi:10.18499/2225-7357-2022-11-1-66-73
Nazeri, A., Krsnik, Ž., Kostović, I., Ha, S. M., Kopić, J., Alexopoulos, D. K., Kaplan, S., Meyer, D., Luby, J. L., Warner, B. B., et al. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4094330
Modeling the effect of anesthesia in pregnancy and impact on the fetal brain: Studies in rabbits
Bleeser, T., Devroe, S., der Veeken, L. V., Valenzuela, I. J., de Velde, M. V., Deprest, J. A., & Rex, S. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-89833-1.00010-0
(2022) · Society for Neuroscience eBooks · doi:10.1523/hon.012010
Editorial: Molecular and cellular logic of cerebral cortex development, evolution, and disease
Dell’Anno, M. T., Conti, L., & Onorati, M. (2023) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2023.1242684
Wu, Q., Bilgic, M., & Matsuzaki, F. (2023) · Wiley eBooks · doi:10.1002/9781119860914.ch9
Glass, M. R., Stein, J. L., & Anton, E. S. (2023) · Wiley eBooks · doi:10.1002/9781119860914.ch25
Truncated radial glia as a common precursor in the late corticogenesis of gyrencephalic mammalsPreprint
Bilgic, M., Wu, Q., Suetsugu, T., et al. (2023) · eLife · doi:10.7554/elife.91406.2
Neocortex neurogenesis and maturation in the African greater cane rat
Mustapha, O., Grochow, T., Olopade, J. O., & Fietz, S. A. (2023) · Neural Development · doi:10.1186/s13064-023-00175-x
Human Cultural Evolution Outpaces Biological Evolution
Changeux, J. (2024) · Oxford University Press eBooks · doi:10.1093/med/9780197676592.003.0023
Brain Cortical Functional Gradients Predict Cortical Folding Patterns via Attention Mesh Convolution
Li, Y., He, Z., Zhong, T., Li, C., Zhu, D., Han, J., Liu, T., & Zhang, T. (2024) · Lecture notes in computer science · doi:10.1007/978-3-031-72104-5_14
Schuurmans, I. M. E., Mordelt, A., & de Witte, L. D. (2025) · Handbook of clinical neurology · doi:10.1016/b978-0-443-19104-6.00011-5
Loss of Postnatal Retinal Input Perturbs Cortical Lamination in the Developing Ferret Visual Cortex
Hilts, C., Santiago, S. E., Kroenke, C. D., & Barnes, A. P. (2025) · The Journal of Comparative Neurology · doi:10.1002/cne.70061
Astrocytes in white matter respond to tensile cues during cortical folding: a numerical studyPreprint
Taneja, K., Saito, K., Kawasaki, H., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.17.683172
He, D., Pan, M., Sun, F., Jiang, L., Guo, Q., Wu, P., Li, S., Yang, W., Tu, Z., Li, X.-J., et al. (2025) · Protein & Cell · doi:10.1093/procel/pwaf097
Presicce, P., Beckman, D., Diniz, G. B., Cappelletti, M., Ott, S. P., Bercovici, S., Kale, S. P., Babb, P., Mohole, J., Richardson, L. S., et al. (2026) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03686-y
The effect of astrocyte depletion and repopulation approaches in pathological condition of CNS
Tahmasebi, F., Safarian, A., Asl, E. R., Vahidinia, Z., & Barati, S. (2026) · Acta Neurologica Belgica · doi:10.1007/s13760-026-03005-z
Development and specification of cortical areas in the non human primate
Pace, C. (2020) · theses.fr (ABES) · doi:10.70675/b7094400z9034z4ec5zb776zde051009bafa
Álvarez, G. O. (2020) · theses.fr (ABES) · doi:10.70675/c245dc66z5428z4d00z9ce9z00ea191284cb
Lamination of primary visual cortex in the macaque: Layer 5 subdivisions
Ahmed, B., Duque, A., RAKIC, P. T., & Molnár, Z. (2026) · Journal of Anatomy · doi:10.1111/joa.70137
Self-citationRosenblatt, M., Vandewouw, M. M., Fox-Jurkowitz, H., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.22.733725
Choi, W. W. Y., Muffat, J., & Li, Y. (2026) · Journal of Neurochemistry · doi:10.1111/jnc.70527
ERK signaling integrates multiple mechanisms to drive cortical evolutionary expansionPreprint
Fu, T., Zhang, Z., Zheng, W., Yang, C., Sha, Z., Han, D., Li, J., Yang, F., Yu, J., Li, Z., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.07.28.741115
Non-transport functions of motor proteins in corticogenesis
Mitina, N. N., Medyanik, A. D., Tarabykin, V. S., & Kondakova, E. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2026.1843278
TH/TRs– COL11A2 Axis Mediates Loss of a Differentiated Astrocyte State in Hypogyrified Brains
Zhang, Y., Wang, X., Ma, H., Lyu, P., Tian, S., Zong, R., Chen, J., Ren, G., Yang, Y., Yang, Z., et al. (2026) · Advanced Science · doi:10.1002/advs.77598
Dong, X.-X., Choi, W. W. Y., Ahmed, M., Nishimura, H., Tian, A., Millar, D., Bhattacharya, A., Aggarwal, A., Vu, L., Weng, O. Y., et al. (2026) · Stem Cell Reports · doi:10.1016/j.stemcr.2026.103087
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
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