Cited by 328Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationCongenital heart defects research

Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences

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Hansen, David V, Lui, Jan H, Flandin, Pierre, Yoshikawa, Kazuaki, Rubenstein, John L, Alvarez-Buylla, Arturo, Kriegstein, Arnold R·2013·Nature Neuroscience

Abstract

GABAergic cortical interneurons underlie the complexity of neural circuits and are particularly numerous and diverse in humans. In rodents, cortical interneurons originate in the subpallial ganglionic eminences, but their developmental origins in humans are controversial. We characterized the developing human ganglionic eminences and found that the subventricular zone (SVZ) expanded massively during the early second trimester, becoming densely populated with neural stem cells and intermediate progenitor cells. In contrast with the cortex, most stem cells in the ganglionic eminence SVZ did not maintain radial fibers or orientation. The medial ganglionic eminence exhibited unique patterns of progenitor cell organization and clustering, and markers revealed that the caudal ganglionic eminence generated a greater proportion of cortical interneurons in humans than in rodents. On the basis of labeling of newborn neurons in slice culture and mapping of proliferating interneuron progenitors, we conclude that the vast majority of human cortical interneurons are produced in the ganglionic eminences, including an enormous contribution from non-epithelial SVZ stem cells.

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  • Several recent studies provide strong evidence that primate interneurons are generated extracortically in the ganglionic eminences, as with rodents.

    “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 [14]

  • GABAergic inhibitory interneurons mostly originate from the ganglionic eminences of the ventral telencephalon.

    “which recent studies have shown mostly originate from the ganglionic eminences of the ventral telencephalon (i.e., the subpallium) (Fertuzinhos et al., 2009; Hansen et al., 2013; Hansen et al., 2010; Ma et al., 2013).”
  • Human GABAergic interneurons are largely generated ventrally from the ganglionic eminences in the basal ganglia primordia and migrate tangentially into the cortical plate.

    “human GABAergic interneurons are largely generated ventrally from the ganglionic eminences in the basal ganglia primordia and migrate tangentially into the CP (Fertuzinhos et al., 2009; Hansen et al., 2013; Hansen et al., 2010; Ma et al., 2013; Radonjic et al., 2014).”
  • The subpallium of rodents and primates, including humans, can be subdivided into progenitor domains each characterized by a specific combination of transcription factors.

    “The subpallium of rodents and primates, including humans, can be subdivided into several progenitor domains each characterized by the expression of a specific combination of transcription factors”

    From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Hansen et al., 2013

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Authors
Hansen, D. V., Lui, J. H., Flandin, P., Yoshikawa, K., Rubenstein, J. L., Alvarez-Buylla, A., & Kriegstein, A. R.
Affiliations
  • University of California, San Francisco (US)
  • Institute for Protein Research, The University of Osaka (JP)
Corresponding author
  • Rubenstein, John L
  • Kriegstein, Arnold R
Venue
Nature Neuroscience
Published
2013-10-06
Volume
16
Issue
11
Pages
1576-1587
ISSN
  • 1097-6256 (ISSN-L)
  • 1546-1726
OpenAlex
W2087531974
Cited by
328
References
53
Citations by year
2026: 24 · 2025: 29 · 2024: 24 · 2023: 23 · 2022: 23 · 2021: 27 · 2020: 31 · 2019: 26 · 2018: 17 · 2017: 23 · 2016: 24 · 2015: 24 · 2014: 28 · 2013: 5
FWCI
10.02
Type
journal article
Language
en
Open access
Locations
  • Nature Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • University of California, San Francisco
  • Japan Society for the Promotion of Science (24300134)
  • National Institute of Mental Health (R37MH049428)
  • National Institute of Neurological Disorders and Stroke (R01NS021223)
  • California National Primate Research Center
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
cortical interneurons, GABAergic neurons, ganglionic eminence, subventricular zone, neural stem cells, intermediate progenitor cells, human brain development, medial ganglionic eminence, caudal ganglionic eminence, radial glia
MeSH terms
Animals, Cell Differentiation, Cell Movement, Cerebral Ventricles, Fetus, Humans, Interneurons, Nerve Tissue Proteins, Organ Culture Techniques, RNA, Messenger, Transcription Factors, Gene Expression Regulation, Developmental, Neocortex, Multipotent Stem Cells, Mice, GABAergic Neurons, LIM-Homeodomain Proteins

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