The origin and specification of cortical interneurons

Wonders, Carl P.; Anderson, Stewart A.

doi:10.1038/nrn1954

Cited by 980Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationNeuroscience and Neuropharmacology Research

The origin and specification of cortical interneurons

Wonders, Carl P., Anderson, Stewart A.·2006·Nature Reviews Neuroscience

DOI 10.1038/nrn1954

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Abstract

GABA-containing interneurons are crucial to both the development and function of the cerebral cortex. Unlike cortical projection neurons, which have a relatively conserved set of characteristics, interneurons include multiple phenotypes that vary on morphological, physiological and neurochemical axes. This diversity, and the relatively late, context-dependent maturation of defining features, has challenged efforts to uncover the transcriptional control of cortical interneuron development. Here, we discuss recent data that are beginning to illuminate the origins and specification of distinct subgroups of cortical interneurons.

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The parvalbumin fate of PV-INs appears to be established at their origin as progenitors leave the cell cycle.
“Their 'parvalbumin' fate seems to be established at their origin, as the progenitors leave the cell cycle [127, 128].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [127]
Martinotti cells and 5-HT3AR-lacking O-LM cells arise from MGE progenitors with specification driven by the homeodomain transcription factor Nkx2.1 (10% of MGE-derived hippocampal interneurons based on assumptions outlined above combined with the fact that O-LMs represent 40% of SST interneurons).
“In contrast, Martinotti cells and 5-HT3AR-lacking O-LM cells arise from MGE progenitors with specification driven by the homeodomain transcription factor Nkx2.1 (10% of MGE-derived hippocampal interneurons based on assumptions outlined above combined with the fact that O-LMs represent 40% of SST interneurons) (102, 203, 651, 794, 1042, 1134, 1138, 1213).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1213]
Over-expression of Maf at the peak of PV neurogenesis (E14.5) represses PV+ interneuron fates.
“We also observed that over-expression of Maf at the peak of PV neurogenesis (E14.5) (23) repress PV+ interneuron fates (fig. S24, D and E).”
From Early emergence of cortical interneuron diversity in the mouse embryo (2018) · cites this paper as [23]

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Neuronal subtype specification in the cerebral cortex
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Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons
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Development and Functional Diversification of Cortical Interneurons
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Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses
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Fusion of Regionally Specified hPSC-Derived Organoids Models Human Brain Development and Interneuron Migration
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Differential attention-dependent response modulation across cell classes in macaque visual area V4
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The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors
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Area Patterning of the Mammalian Cortex
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Fate mapping Nkx2.1‐lineage cells in the mouse telencephalon
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Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes
Flames, N., Pla, R., Gelman, D. M., Rubenstein, J. L. R., Puelles, L., & Marín, O. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2750-07.2007 · Cited by 560 · see citing works
Genetic Fate Mapping Reveals That the Caudal Ganglionic Eminence Produces a Large and Diverse Population of Superficial Cortical Interneurons
Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J. B., Battiste, J., Johnson, J. E., Machold, R. P., & Fishell, G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4515-09.2010 · Cited by 559 · see citing works
Hardwiring the Brain: Endocannabinoids Shape Neuronal Connectivity
Berghuis, P., Rajnicek, A. M., Morozov, Y. M., Ross, R. A., Mulder, J., Urbán, G. M., Monory, K., Marsicano, G., Matteoli, M., Canty, A. J., et al. (2007) · Science · doi:10.1126/science.1137406 · Cited by 551 · see citing works
Chromatin and gene-regulatory dynamics of the developing human cerebral cortex at single-cell resolution
Trevino, A. E., Müller, F., Andersen, J., Sundaram, L., Kathiria, A., Shcherbina, A., Farh, K., Chang, H. Y., Pașca, A. M., Kundaje, A., et al. (2021) · Cell · doi:10.1016/j.cell.2021.07.039 · Cited by 478 · see citing works
Single-cell methylomes identify neuronal subtypes and regulatory elements in mammalian cortex
Luo, C., Keown, C. L., Kurihara, L., Zhou, J., He, Y., Li, J., Castanon, R., Lucero, J., Nery, J. R., Sandoval, J. P., et al. (2017) · Science · doi:10.1126/science.aan3351 · Cited by 545 · see citing works
Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies
Heanue, T. A., & Pachnis, V. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2137 · Cited by 529 · see citing works
Experience-Dependent Transfer of Otx2 Homeoprotein into the Visual Cortex Activates Postnatal Plasticity
Sugiyama, S., Di Nardo, A. A., Aizawa, S., Matsuo, I., Volovitch, M., Prochiantz, A., & Hensch, T. K. (2008) · Cell · doi:10.1016/j.cell.2008.05.054 · Cited by 491 · see citing works
Generation and assembly of human brain region-specific three-dimensional cultures
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The rise of three-dimensional human brain cultures
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Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia
Hashimoto, T., Arion, D., Unger, T., Maldonado-Avilés, J. G., Morris, H. M., Volk, D. W., Mirnics, K., & Lewis, D. A. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002011 · Cited by 490 · see citing works
Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling
Fazzari, P., Paternain, A. V., Valiente, M., Pla, R., Luján, R., Lloyd, K., Lerma, J., Marín, O., & Rico, B. (2010) · Nature · doi:10.1038/nature08928 · Cited by 501 · see citing works
Directing Astroglia from the Cerebral Cortex into Subtype Specific Functional Neurons
Heinrich, C., Blum, R., Gascón, S., Masserdotti, G., Tripathi, P., Sánchez, R., Tiedt, S., Schroeder, T., Götz, M., & Berninger, B. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000373 · Cited by 490 · see citing works
Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia
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Npas4 regulates excitatory-inhibitory balance within neural circuits through cell-type-specific gene programs
Spiegel, I., Mardinly, A. R., Gabel, H. W., Bazinet, J. E., Couch, C. H., Tzeng, C. P., Harmin, D. A., & Greenberg, M. E. (2014) · Cell · doi:10.1016/j.cell.2014.03.058 · Cited by 416 · see citing works
“…neuronal cultures highly enriched for these neurons by taking advantage of the fact that, early in their development, inhibitory neurons are localized to specialized regions of the embryonic brain, the ganglionic eminences, that are devoid of excitatory neurons (Wonders and Anderson, 2006).”
The emerging functions of endocannabinoid signaling during CNS development
Harkany, T., Guzmán, M., Galve‐Roperh, I., Berghuis, P., Devi, L. A., & Mackie, K. (2007) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2006.12.004 · Cited by 432 · see citing works
Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex
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The Level of the Transcription Factor Pax6 Is Essential for Controlling the Balance between Neural Stem Cell Self-Renewal and Neurogenesis
Sansom, S. N., Griffiths, D. S., Faedo, A., Kleinjan, D., Ruan, Y., Smith, J. C., van Heyningen, V., Rubenstein, J. L. R., & Livesey, F. J. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000511 · Cited by 401 · see citing works
New insights into the development of the human cerebral cortex
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Authors: Wonders, C. P., & Anderson, S. A.
Affiliations: Cornell University (US)
Corresponding author: Anderson, Stewart A.
ORCID: Anderson, Stewart A.
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2006-08-02
Volume: 7
Issue: 9
Pages: 687-696
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/nrn1954
OpenAlex: W2007034511
Cited by: 980
References: 142
Citations by year: 2026: 32 · 2025: 49 · 2024: 39 · 2023: 47 · 2022: 32 · 2021: 42 · 2020: 66 · 2019: 53 · 2018: 43 · 2017: 52 · 2016: 49 · 2015: 49 · 2014: 53 · 2013: 54 · 2012: 50
FWCI: 3.02
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of Mental Health
National Institute of Neurological Disorders and Stroke
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 › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: cortical interneurons, interneuron specification, GABAergic neurons, cortical development, transcriptional regulation, interneuron subtypes, neuronal maturation
MeSH terms: Animals, Cell Differentiation, Cell Movement, Cerebral Cortex, Humans, Interneurons, Nerve Tissue Proteins, Stem Cells, Telencephalon, Biomarkers, Gene Expression Regulation, Developmental, Cell Lineage

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The origin and specification of cortical interneurons

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