The DOI matches its Crossref record; 47 of the 49 references it cites were found in a registry or an index.
Comparative Analysis of the Subventricular Zone in Rat, Ferret and Macaque: Evidence for an Outer Subventricular Zone in Rodents
Open accessAbstract
The mammalian cerebral cortex arises from precursor cells that reside in a proliferative region surrounding the lateral ventricles of the developing brain. Recent work has shown that precursor cells in the subventricular zone (SVZ) provide a major contribution to prenatal cortical neurogenesis, and that the SVZ is significantly thicker in gyrencephalic mammals such as primates than it is in lissencephalic mammals including rodents. Identifying characteristics that are shared by or that distinguish cortical precursor cells across mammalian species will shed light on factors that regulate cortical neurogenesis and may point toward mechanisms that underlie the evolutionary expansion of the neocortex in gyrencephalic mammals. We immunostained sections of the developing cerebral cortex from lissencephalic rats, and from gyrencephalic ferrets and macaques to compare the distribution of precursor cell types in each species. We also performed time-lapse imaging of precursor cells in the developing rat neocortex. We show that the distribution of Pax6+ and Tbr2+ precursor cells is similar in lissencephalic rat and gyrencephalic ferret, and different in the gyrencephalic cortex of macaque. We show that mitotic Pax6+ translocating radial glial cells (tRG) are present in the cerebral cortex of each species during and after neurogenesis, demonstrating that the function of Pax6+ tRG cells is not restricted to neurogenesis. Furthermore, we show that Olig2 expression distinguishes two distinct subtypes of Pax6+ tRG cells. Finally we present a novel method for discriminating the inner and outer SVZ across mammalian species and show that the key cytoarchitectural features and cell types that define the outer SVZ in developing primates are present in the developing rat neocortex. Our data demonstrate that the developing rat cerebral cortex possesses an outer subventricular zone during late stages of cortical neurogenesis and that the developing rodent cortex shares important features with that of primates.
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?
In the citing paper
“oRGs are present in large numbers in gyrencephalic primates22,23,40–44 and are considered pivotal to the evolutionary increase in human cortex size and complexity45,46.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [44]
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 1×
“: [43]), but remain to be fully understood.”
BackgroundNoctor, S. C., Martínez-Cerdeño, V., Ivic, L., & Kriegstein, A. R. (2004) · Nature Neuroscience · doi:10.1038/nn1172 · Cited by 2,229
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
Self-citationA 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
Neurogenic 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
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
Rakic, P. (1974) · Science · doi:10.1126/science.183.4123.425 · Cited by 1,161
Haubensak, 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
OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling
Fietz, S. A., Kelava, I., Vogt, J., Wilsch-Bräuninger, M., Stenzel, D., Fish, J. L., Corbeil, D., Riehn, A., Distler, W., Nitsch, R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2553 · Cited by 830
Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells
Miyata, T., Kawaguchi, A., Saito, K., Kawano, M., Muto, T., & Ogawa, M. (2004) · Development · doi:10.1242/dev.01173 · Cited by 791
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
Self-citationEmbryonic vertebrate central nervous system: Revised terminology
Angevine, J. B., Bodian, D., Coulombre, A. J., Edds, M. V., Hamburger, V., Jacobson, M., Lyser, K. M., Prestige, M. C., Sidman, R. L., Varon, S. S., et al. (1970) · The Anatomical Record · doi:10.1002/ar.1091660214 · Cited by 727
Smart, I. H. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.37 · Cited by 687
Schmechel, D. E., & RAKIC, P. T. (1979) · Anatomy and Embryology · doi:10.1007/bf00300010 · Cited by 682
Pax6 Controls Radial Glia Differentiation in the Cerebral Cortex
Götz, M., Stoykova, A., & Gruß, P. (1998) · Neuron · doi:10.1016/s0896-6273(00)80621-2 · Cited by 665
A 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
Noctor, S. C., Flint, A. C., Weissman, T. A., Wong, W. S., Clinton, B. K., & Kriegstein, A. R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-08-03161.2002 · Cited by 647
Self-citationNieto, M., Monuki, E. S., Tang, H., Imitola, J., Haubst, N., Khoury, S. J., Cunningham, J., Götz, M., & Walsh, C. A. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20322 · Cited by 569
Herculano-Houzel, S., & Lent, R. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4526-04.2005 · Cited by 551
Voigt, T. B. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890106 · Cited by 549
A new subtype of progenitor cell in the mouse embryonic neocortex
Wang, X., Tsai, J.-W., LaMonica, B., & Kriegstein, A. R. (2011) · Nature Neuroscience · doi:10.1038/nn.2807 · Cited by 507
Shitamukai, A., Konno, D., & Matsuzaki, F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4773-10.2011 · Cited by 474
Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis
Noctor, S. C., Martínez‐Cerdeño, V., & Kriegstein, A. R. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21669 · Cited by 444
Self-citationCellular scaling rules for primate brains.
Herculano-Houzel, S., Collins, C. E., Wong, P., & Kaas, J. H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611396104 · Cited by 422
Neural stem and progenitor cells shorten S-phase on commitment to neuron production
Arai, Y., Pulvers, J. N., Haffner, C., Schilling, B., Nüsslein, I., Calegari, F., & Huttner, W. Β. (2011) · Nature Communications · doi:10.1038/ncomms1155 · Cited by 399
Hendelman, W. J. (1992) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1992.4.2.175 · Cited by 364
Cortical upper layer neurons derive from the subventricular zone as indicated bySvet1gene expression
Tarabykin, V. S., Stoykova, A., Usman, N. Y., & Gruß, P. (2001) · Development · doi:10.1242/dev.128.11.1983 · Cited by 336
Role of Sox2 in the development of the mouse neocortex
Bani‐Yaghoub, M., Tremblay, R. G., Lei, J. X., Zhang, D., Zurakowski, B., Sandhu, J. K., Smith, B., Ribecco‐Lutkiewicz, M., Kennedy, J. A., Walker, P. R., et al. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.03.007 · Cited by 271
Olig2 Directs Astrocyte and Oligodendrocyte Formation in Postnatal Subventricular Zone Cells
Marshall, C. A. G., Novitch, B. G., & Goldman, J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1924-05.2005 · Cited by 249
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
Reillo, I., & Borrell, V. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr284 · Cited by 184
Cortical radial glial cells in human fetuses: Depth‐correlated transformation into astrocytes
deAzevedo, L. C., Fallet‐Bianco, C., Moura‐Neto, V., Daumas‐Duport, C., Hedin‐Pereira, C., & Lent, R. (2003) · Journal of Neurobiology · doi:10.1002/neu.10205 · Cited by 162
Bentivoglio, M., & Mazzarello, P. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00065-9 · Cited by 162
Neurogenic Radial Glial Cells in Reptile, Rodent and Human: from Mitosis to Migration
Weissman, T. A. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.6.550 · Cited by 158
García‐Moreno, F., Vasistha, N. A., Trévia, N., Bourne, J. A., & Molnár, Z. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr312 · Cited by 154
Kamei, Y., Inagaki, N., Nishizawa, M., Tsutsumi, O., Taketani, Y., & Inagaki, M. (1998) · Glia · doi:10.1002/(sici)1098-1136(199807)23:3 · Cited by 114
An efficient method for estimating the total number of neurons in rat brain cortex
Korbo, L., Pakkenberg, B., Ladefoged, O., Gundersen, H. J. G., Arlien-Søborg, P., & Pakkenberg, H. (1990) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(90)90153-7 · Cited by 108
Takahashi, T., Misson, J., & Caviness, V. S. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903020103 · Cited by 108
Samuelsen, G. B. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.2.115 · Cited by 95
Premutation CGG-repeat expansion of the Fmr1 gene impairs mouse neocortical development
Cunningham, C. L., Martínez‐Cerdeño, V., Porras, E. N., Prakash, A. N., Angelastro, J. M., Willemsen, R., Hagerman, P. J., Pessah, I. N., Berman, R. F., & Noctor, S. C. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq432 · Cited by 81
Self-citationNeocortical and hippocampal neuron and glial cell numbers in the rhesus monkey
Christensen, J. R., Larsen, K. B., Lisanby, S. H., Scalia, J., Arango, V., Dwork, A. J., & Pakkenberg, B. (2007) · The Anatomical Record · doi:10.1002/ar.20504 · Cited by 71
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
Carney, R. S. E., Bystron, I., López‐Bendito, G., & Molnár, Z. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0142-4 · Cited by 46
Mooney, S. M., & Napper, R. M. A. (2005) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000158936.40150.5a · Cited by 32
Judson, M. C., Amaral, D. G., & Levitt, P. R. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq223 · Cited by 32
Huttenlocher (1997) · doi:10.1002/(sici)1096-9861(19971020)387:2
Self-citation
Flagged first, then by citations
2 of the 49 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Microglia Regulate the Number of Neural Precursor Cells in the Developing Cerebral Cortex
Cunningham, C. L., Martínez-Cerdeño, V., & Noctor, S. C. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3441-12.2013 · Cited by 976
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
Molecular logic of neocortical projection neuron specification, development and diversity
Greig, L. C., Woodworth, M. B., Galazo, M. J., Padmanabhan, H., & Macklis, J. D. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3586 · Cited by 863
The use of brain organoids to investigate neural development and disease
Di Lullo, E., & Kriegstein, A. R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.107 · Cited by 788
Neural progenitors, neurogenesis and the evolution of the neocortex
Florio, M., & Huttner, W. Β. (2014) · Development · doi:10.1242/dev.090571 · Cited by 654
Metadata
- Authors
- Martínez-Cerdeño, V., Cunningham, C. L., Camacho, J., Antczak, J. L., Prakash, A. N., Cziep, M. E., Walker, A. I., & Noctor, S. C.
- Affiliations
- University of California, Davis (US)
- Shriners Hospitals for Children - Northern California (US)
- Brigham Young University (US)
- University of California Davis Medical Center (US)
- Corresponding author
- Noctor, Stephen C.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-01-17
- Volume
- 7
- Issue
- 1
- Pages
- e30178
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3260244
- OpenAlex
- W2030135612
- Cited by
- 203
- References
- 49
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 10 · 2023: 9 · 2022: 11 · 2021: 14 · 2020: 16 · 2019: 18 · 2018: 16 · 2017: 16 · 2016: 20 · 2015: 18 · 2014: 18 · 2013: 21 · 2012: 4
- FWCI
- 6.56
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Science Foundation
- MIND Institute, University of California, Davis
- Children's Miracle Network Hospitals
- University of California, Davis
- National Institute of Mental Health (R01MH094681)
- 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
- subventricular zone, outer subventricular zone, cortical neurogenesis, radial glia, Pax6, Tbr2, Olig2, lissencephaly, gyrencephaly, neocortex evolution, cortical development, rats, ferrets, macaque
- MeSH terms
- PAX6 Transcription Factor, Anatomy, Comparative, Animals, Cell Count, Cerebral Cortex, Embryo, Mammalian, Eye Proteins, Female, Ferrets, Immunohistochemistry, Macaca mulatta, Male, Mitosis, Neurons, Pregnancy, Repressor Proteins, Somatosensory Cortex, Time Factors, Rats, Sprague-Dawley, Homeodomain Proteins, Neocortex, T-Box Domain Proteins, Mice, Rats, Paired Box Transcription Factors, Neurogenesis, Neural Stem Cells
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
