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Comparative Analysis of the Subventricular Zone in Rat, Ferret and Macaque: Evidence for an Outer Subventricular Zone in Rodents
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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.
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“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]
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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
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