The DOI matches its Crossref record; 73 of the 73 references it cites were found in a registry or an index.
Role of Intermediate Progenitor Cells in Cerebral Cortex Development
Abstract
Intermediate progenitor cells (IPCs) are a type of neurogenic transient amplifying cells in the developing cerebral cortex. IPCs divide symmetrically at basal (abventricular) positions in the neuroepithelium to produce pairs of new neurons or, in amplifying divisions, pairs of new IPCs. In contrast, radial unit progenitors (neuroepithelial cells and radial glia) divide at the apical (ventricular) surface and produce only single neurons or single IPCs by asymmetric division, or self-amplify by symmetric division. Histologically, IPCs are most prominent during the middle and late stages of neurogenesis, when they accumulate in the subventricular zone, a progenitor compartment linked to the genesis of upper neocortical layers (II–IV). Nevertheless, IPCs are present throughout cortical neurogenesis and produce neurons for all layers. In mice, changes in the abundance of IPCs caused by mutations of Pax6, Ngn2, Id4 and other genes are associated with parallel changes in cortical thickness but not surface area. In gyrencephalic brains, IPCs may play broader roles in determining not only laminar thickness, but also cortical surface area and gyral patterns. We propose that regulation of IPC genesis and amplification across developmental stages and regional subdivisions modulates laminar neurogenesis and contributes to the cytoarchitectonic differentiation of cortical areas.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“Cortical surface area and thickness are controlled by the mechanisms involved in RGC and IPC proliferation and differentiation decisions [99, 100].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [99]
Citations
Cites
Specification of Cerebral Cortical Areas
Rakic, P. (1988) · Science · doi:10.1126/science.3291116 · Cited by 3,127 · cited 1×
“Both the ULH and the IPH contrast with the radial unit hypothesis (RUH) [”
BackgroundNoctor, S. C., Martínez-Cerdeño, V., Ivic, L., & Kriegstein, A. R. (2004) · Nature Neuroscience · doi:10.1038/nn1172 · Cited by 2,229
The cell biology of neurogenesis
Götz, M., & Huttner, W. B. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1739 · Cited by 2,130
Neurons 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
Reduced Apoptosis and Cytochrome c–Mediated Caspase Activation in Mice Lacking Caspase 9
Kuida, K., Haydar, T. F., Kuan, C.-Y., Gu, Y., Taya, C., Karasuyama, H., Su, M. S.-S., Rakic, P., & Flavell, R. A. (1998) · Cell · doi:10.1016/s0092-8674(00)81476-2 · Cited by 1,643
Regulation of Cerebral Cortical Size by Control of Cell Cycle Exit in Neural Precursors
Chenn, A., & Walsh, C. A. (2002) · Science · doi:10.1126/science.1074192 · Cited by 1,431
Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A. M., Bulfone, A., Kowalczyk, T., & Hevner, R. F. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2899-04.2005 · Cited by 1,261
Self-citationHaubensak, W. E., Attardo, A., Denk, W. T., & Huttner, W. Β. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308600100 · Cited by 1,004
Asymmetric Inheritance of Radial Glial Fibers by Cortical Neurons
Miyata, T., Kawaguchi, A., Okano, H., & Ogawa, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00420-2 · Cited by 892
Flagged first, then by citations
Cited by
Sorted by citations
Items 301–384 of 384
Huang, Y.-T., Mason, J. O., & Price, D. J. (2017) · BMC Neuroscience · doi:10.1186/s12868-017-0365-0 · Cited by 5
“Most of them divide just once to generate two postmitotic neurons that migrate into the developing cortical plate (the future cortex) [2, 5, 6].”
BackgroundGerstmann, K., Kindbeiter, K., Telley, L., Bozon, M., Charoy, C., Jabaudon, D., Moret, F., & Castellani, V. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.20.106526 · Cited by 5
Slapø, N. B., Jørgensen, K. N., Elvsåshagen, T., Nerland, S., Roelfs, D., Valstad, M., Timpe, C. M. F., Richard, G., Beck, D., Sæther, L. S., et al. (2023) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2023.111633 · Cited by 6
“heritable traits, but differ phenotypically and genetically and result from different ontogenetic stages during cortical development (Grasby et al., 2020; Norbom et al., 2021; Panizzon et al., 2009; Pontious et al., 2008; Strike et al., 2019; Wierenga et al., 2014).”
Neurodegenerative Diseases and Cell Reprogramming
Sallam, A., & Mousa, S. A. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-02039-5 · Cited by 4
Pretzsch, C. M., & Ecker, C. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-816393-1.00013-0 · Cited by 4
Neurobiological Clusters Are Associated With Trajectories of Overall Psychopathology in Youth
Wang, C. K., Hayes, R. A., Roeder, K., & Jalbrzikowski, M. (2023) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2023.04.007 · Cited by 6
Growth in a Turing Model of Cortical Folding
Toole, G., & Hurdal, M. K. (2012) · BIOMATH · doi:10.11145/j.biomath.2012.09.252 · Cited by 4
“IPCs and hence cortical folding are regulated via a genetic chemical gradient; namely, Pax6and Wnt have been shown to affect the number of IPCs and proper cortical development in mice [22].”
BackgroundDiversity 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
Hong, W., Zhang, X., Liu, Z., Li, M., Yu, Z., Zhao, G., Wang, Y., Sun, C., Yang, B., Xu, R. H., et al. (2022) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.28542 · Cited by 3
Breunig, J. J., & Nelson, B. R. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814405-3.00013-8 · Cited by 2
Xie, Y., Jacobs, E. C., & Fisher, R. S. (2009) · ASN NEURO · doi:10.1042/an20090038 · Cited by 3
“…organization in primitive and mature neocortex, with a superficial lamina embedded in layer I, a prominent middle lamina engulfed by layers V–VI, and a deep lamina that persists in mature subplate were identified (Landry et al., 1998; Xie et al., 2002: Jacobs et al., 2007; Pontious et al., 2008).”
BackgroundVasculature-guided neural migration in mouse cerebellum
Xi, Y., Chen, W. J., Deng, J., Cui, Z., Liu, H. L., Yan, M., deng, J., & Wu, P. (2014) · The European Zoological Journal · doi:10.1080/11250003.2014.977359 · Cited by 3
“However, through asymmetric division, some post-mitotic newborn neurons can be produced by cell differentiation (Pontious et al. 2008), and these postmitotic newborn neurons have strong migration ability.”
BackgroundNeuronal Migration and Brain Patterning
Griveau, A., Borello, U., & Pierani, A. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397266-8.00036-3 · Cited by 3
Graffunder, A. S., Bresser, A. A. J., Vallone, V. B. F., Megges, M., Stachelscheid, H., Kühnen, P., & Opitz, R. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.16.567497 · Cited by 3
Loss of Pax6 Causes Regional Changes in Dll1 Expression in Developing Cerebral Cortex
Dorà, E., Price, D. J., & Mason, J. O. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00078 · Cited by 2
“In the mouse, most IPCs divide symmetrically to produce two neurons, but a small proportion divide asymmetrically to give rise to one progenitor and one neuron (Haubensak et al., 2004; Noctor et al., 2004; Pontious et al., 2008).”
BackgroundZhang, P., Wan, X., Jiang, J., Liu, Y., Wang, D., Ai, K., Liu, G., Zhang, X.-D., & Zhang, J. (2024) · Cerebral Cortex · doi:10.1093/cercor/bhae337 · Cited by 2
Zhang, X., Peng, Y., Li, D., Hou, A., Liang, M., & Yu, C. (2025) · NeuroImage · doi:10.1016/j.neuroimage.2025.121118 · Cited by 3
“In addition to the assumption that CT is determined by neuronal output from radial unit progenitors, the radial amplification hypothesis emphasizes that the genesis and amplification of intermediate progenitor cells modulate neuronal output (Pontious et al., 2008).”
Real-time Bioluminescence Imaging of Notch Signaling Dynamics during Murine Neurogenesis
Shimojo, H., & Kageyama, R. (2019) · Journal of Visualized Experiments · doi:10.3791/60455 · Cited by 4
Sanes, D. H., Reh, T. A., Harris, W. A., & Landgraf, M. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-803996-0.00003-4 · Cited by 2
Fisher, R. S., & Xie, Y. (2010) · ASN NEURO · doi:10.1042/an20100022 · Cited by 1
Cell Cycle Regulation in Brain Construction
Crespo, M., & Ross, M. E. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397265-1.00094-0 · Cited by 1
Tsiarli, M. A. (2014) · D-Scholarship@Pitt (University of Pittsburgh) · Cited by 1
Sanes, D. H., Reh, T. A., & Harris, W. A. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-374539-2.00007-0 · Cited by 1
Breunig, J. J., & Nelson, B. R. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397265-1.00070-8 · Cited by 1
Siegenthaler, J. A., & Pleasure, S. J. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397265-1.00087-3 · Cited by 1
Cerebral Organoids in Developmental Neuroscience
Forero, A., & Cappello, S. (2022) · Springer eBooks · doi:10.1007/978-3-030-88832-9_179 · Cited by 1
Kiszka, K. A. (2019) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7790 · Cited by 1
Singh, J., Daniels, N. J., Pirozzi, F., Wynshaw-Boris, A. J., Lopez-Gonzalez, R., & Padgett, R. A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.29.520610 · Cited by 1
“Radial glia fiber are crucial for proper migration of newly formed neurons to their final cortical destination, as described previously (84-86).”
BackgroundIntermediate Progenitors in Neocortical Development and Evolution
Hevner, R. F. (2023) · doi:10.1002/9781119860914.ch3 · Cited by 1
Self-citationMolecular development and laminar distribution of GABAergic interneurons of the cerebral cortex
Lodato, S. (2011) · Università degli Studi di Napoli Federico II · doi:10.6092/unina/fedoa/8450
Role of Robo1 receptor in semaphorin signalling systemand cortical interneuron migration
Hernandez-Miranda, L. R. (2010) · UCL Discovery (University College London)
Barber, M. (2009) · OpenGrey (Institut de l'Information Scientifique et Technique)
Brealy, J. (2015) · ORCA Online Research @Cardiff (Cardiff University)
Mills, B. D. (2012) · CSUN ScholarWorks (California State University, Northridge)
The Cellular and Molecular Properties of Multipotent Neural Stem Cells
Hutton, S. R., & Pevny, L. (2012) · Springer eBooks · doi:10.1007/978-1-4614-3801-4_3
Hutton, S. R. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/871b-ky64
The Brain’s Structural and Functional Relationships with Language Ability in Preschool Children
Walton, M. (2016) · Libraries and Cultural Resources (University of Calgary) · doi:10.11575/prism/28019
Cortical surface area hyperexpansion in infants: A promising biomarker for autism spectrum disorder
Patra, S. (2017) · Asian Journal of Psychiatry · doi:10.1016/j.ajp.2017.02.025
SCRATCH2 na diferenciação neural em embriões e em células-tronco.
Kanno, T. Y. N. (2016) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.42.2016.tde-10112016-090637
Molecular Mechanisms Regulating Mammalian Forebrain Development
Tsui, D. C. C. (2014) · TSpace (University of Toronto)
Trought, K. (2017) · TSpace (University of Toronto)
Patel, S. (2019) · TSpace (University of Toronto)
Cortical patterning and neuronal migration are under the guide of BAF complex functionality
Sokpor, G. (2020) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7927
Tremblay, P., Perron, M., & Vaillancourt, J. (2021) · Research Square · doi:10.21203/rs.3.rs-507257/v1
Rosa, P. G. P. (2020) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.5.2020.tde-14092021-152603
Slapø, N. B., Jørgensen, K. N., Elvsåshagen, T., Nerland, S., Roelfs, D., Valstad, M., Timpe, C. M. F., Richard, G., Beck, D., Sæther, L. S., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-990586/v1
Faculty Opinions recommendation of Cell-type-specific 3D epigenomes in the developing human cortex.
Sharrocks, A. D. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.738832662.793581292
Ben‐Ari, Y. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733499087.793568939
Cerebral Organoids in Developmental Neuroscience
Forero, A., & Cappello, S. (2022) · Springer eBooks · doi:10.1007/978-1-4614-6434-1_179-1
Sato, Y., Asahi, T., & Kataoka, K. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.11.528152
“Because IPC is believed to contribute to cortical expansion in 330 primates [42,43], the upregulation of EOMES at 65 days possibly induced organoid expansion.”
BackgroundTan, W. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-815234-8.00008-2
Yang, X., Wang, D., Shen, C., Chen, X., Yang, H., Zhou, X., Guo, C.-R., Tian, Y., Zhu, M. X., & Ye, Y. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.01.10.632374
Wang, Y., Egert, A., Schenke, M., Smirnova, L., & Kincaid, B. (2025) · Elsevier eBooks · doi:10.1016/b978-0-323-95488-4.00187-x
Additional file 8 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636634
Additional file 14 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636652
Additional file 5 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636625
Additional file 10 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636640
Additional file 6 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636628
Additional file 11 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636643
Additional file 12 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636646
Additional file 4 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636622
Additional file 7 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636631
Additional file 13 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636649
Additional file 9 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636637
Additional file 1 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636613
Additional file 15 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636655
Additional file 2 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636616
Additional file 3 of Integrative single-cell RNA-seq analysis of vascularized cerebral organoids
Sato, Y., Asahi, T., & Kataoka, K. (2024) · Figshare · doi:10.6084/m9.figshare.26636619
Role of G1 phase regulators during corticogenesis
Pilaz, L. (2009) · theses.fr (ABES) · doi:10.70675/9f47e9acz5e06z4d39z83b5za3e00f543c58
Betizeau, M. (2013) · theses.fr (ABES) · doi:10.70675/96b2fd4ez61cfz4afeza473z7811a8b1fda6
Study of Exon Junction Complex in mouse neural stem cells
Mishra, R. (2016) · theses.fr (ABES) · doi:10.70675/763ca66az53efz4562zb337z755d833bb64d
Maladies à prions : vers le développement d'une thérapie génique et cellulaire
Souder, C. L. (2017) · theses.fr (ABES) · doi:10.70675/2b878862z67daz4e3azab26z026e8344ce30
Penisson, M. (2020) · theses.fr (ABES) · doi:10.70675/ad2c850ezf9cfz4390za05azc0cd02a0c5f0
Cornelius, J. A., Shivakumar, M., Kim, T., Cervantes, O., Kapur, R. P., Huang, H., Zhao, H., Rosario, B. D., Li, A., Li, R., et al. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2026.1785001
Huang, G., Lu, C., Jin, Z., Huang, Y., Du, X., Hu, X., Peng, H., Wang, S., Wen, L., Qiu, J., et al. (2026) · Bioengineering & Translational Medicine · doi:10.1002/btm2.70164
“21 In humans and other primates, the lateral part of the SVZ further differentiates into a distinct outer subventricular zone (OSVZ), which is enriched with outer radial glial cells (oRGs) and constitutes a significant progenitor cell population in the human cortex.”
Ross, M. E. (2011) · Cambridge University Press eBooks · doi:10.1017/cbo9780511921001.052
Metadata
- Authors
- Pontious, A., Kowalczyk, T., Englund, C., & Hevner, R. F.
- Affiliations
- University of Washington (US)
- ORCID
- Hevner, Robert F.
- Venue
- Developmental Neuroscience
- Publisher
- S. Karger AG
- Published
- 2007-12-13
- Volume
- 30
- Issue
- 1-3
- Pages
- 24-32
- ISSN
- 0378-5866 (ISSN-L)
- 1421-9859
- OpenAlex
- W2012470399
- Cited by
- 378
- References
- 73
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 18 · 2023: 13 · 2022: 15 · 2021: 18 · 2020: 22 · 2019: 22 · 2018: 18 · 2017: 19 · 2016: 20 · 2015: 22 · 2014: 30 · 2013: 31 · 2012: 28
- FWCI
- 2.07
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Developmental Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Keywords
- intermediate progenitor cells, cortical development, cortical neurogenesis, subventricular zone, radial glia, neuroepithelial cells, cortical lamination, cortical thickness, cortical surface area, Pax6, Ngn2, Id4, cytoarchitecture, gyrencephaly
- MeSH terms
- Animals, Cell Differentiation, Cerebral Cortex, Humans, Nerve Growth Factors, Nervous System Malformations, Neural Pathways, Neurons, Stem Cells, Signal Transduction, Gene Expression Regulation, Developmental, Mice
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