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Subcortical origins of human and monkey neocortical interneurons
Abstract
Cortical GABAergic inhibitory interneurons have crucial roles in the development and function of the cerebral cortex. In rodents, nearly all neocortical interneurons are generated from the subcortical ganglionic eminences. In humans and nonhuman primates, however, the developmental origin of neocortical GABAergic interneurons remains unclear. Here we show that the expression patterns of several key transcription factors in the developing primate telencephalon are very similar to those in rodents, delineating the three main subcortical progenitor domains (the medial, lateral and caudal ganglionic eminences) and the interneurons tangentially migrating from them. On the basis of the continuity of Sox6, COUP-TFII and Sp8 transcription factor expression and evidence from cell migration and cell fate analyses, we propose that the majority of primate neocortical GABAergic interneurons originate from ganglionic eminences of the ventral telencephalon. Our findings reveal that the mammalian neocortex shares basic rules for interneuron development, substantially reshaping our understanding of the origin and classification of primate neocortical interneurons.
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“However, several recent studies have shown strong evidence that, as with rodents, primate interneurons are generated extracortically in the GEs11,14.”
From Transcriptional landscape of the prenatal human brain (2014) · cites this paper as [11]
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Javier‐Torrent, M., & Nguyen, L. (2023) · Wiley eBooks · doi:10.1002/9781119860914.ch17
Brain cell types and distribution
Kooijmans, R. N. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-820480-1.00198-4
The Development of the Central Nervous System and Human Neural Stem Cells
Ávila, A., Ascenzi, B. M., & Vidal, P. M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-822404-5.00001-2
Development of the Hippocampal Formation
Lavenex, P., Amaral, D. G., Lavenex, P. B., Guillemot, F., Insausti, R., & Urbán, N. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780190065324.003.0004
Lenherr, C., Neves, G., Oliveira, M. G., & Burrone, J. (2025) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041506
Yang, Y., Booker, S. A., Clegg, J. M., Urzainqui, I. Q., Sumera, A., Kozić, Z., Dando, O., Lorenzo, S. M., Hérault, Y., Kind, P. C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26562655
Additional file 4 of Prenatal alcohol exposure is a leading cause of interneuronopathy in humans
Marguet, F., Friocourt, G., Brosolo, M., Sauvestre, F., Marcorelles, P., Lesueur, C., Marret, S., Gonzalez, B. J., & Laquerrière, A. (2020) · Figshare · doi:10.6084/m9.figshare.13310404
Metadata
- Authors
- Ma, T., Wang, C., Wang, L., Zhou, X., Tian, M., Zhang, Q., Zhang, Y., Li, J., Liu, Z., Cai, Y., Liu, F., You, Y., Chen, C., Campbell, K., Song, H., Ma, L., Rubenstein, J. L., & Yang, Z.
- Affiliations
- Fudan University (CN)
- Shanghai Medical College of Fudan University (CN)
- Hebei Medical University (CN)
- Children's Hospital of Fudan University (CN)
- Cincinnati Children's Hospital Medical Center (US)
- Johns Hopkins University (US)
- University of California, San Francisco (US)
- Corresponding author
- Yang, Zhengang
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2013-10-06
- Volume
- 16
- Issue
- 11
- Pages
- 1588-1597
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2085806268
- Cited by
- 322
- References
- 50
- Citations by year
- 2026: 17 · 2025: 22 · 2024: 19 · 2023: 27 · 2022: 23 · 2021: 33 · 2020: 31 · 2019: 28 · 2018: 19 · 2017: 27 · 2016: 21 · 2015: 21 · 2014: 31 · 2013: 3
- FWCI
- 9.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Chinese Academy of Sciences
- Fudan University
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- neocortical interneurons, GABAergic interneurons, ganglionic eminence, transcription factors, SOX6, COUP-TFII, Sp8, tangential migration, human brain development, ventral telencephalon
- MeSH terms
- Adult, Age Factors, Animals, Animals, Newborn, Bromodeoxyuridine, Cell Count, Cell Movement, Cells, Cultured, Embryo, Mammalian, gamma-Aminobutyric Acid, Humans, Interneurons, Macaca mulatta, Male, Nerve Tissue Proteins, Organ Culture Techniques, Transcription Factors, Transfection, Gene Expression Regulation, Developmental, Neocortex, Green Fluorescent Proteins, Mice
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