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

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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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Self-citation
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Self-citation
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Background
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Selective induction of neocortical GABAergic neurons by the PDK1-Akt pathway through activation of Mash1
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“Subpopulations of GABAergic neurons generated in the ventral telencephalon migrate to the NCX, olfactory bulb, and striatum (11, 12), and a large proportion of neocortical interneurons are produced in a Mash1-dependent manner (16).”
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Modeling neuropsychiatric disorders using human induced pluripotent stem cells
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Human pallial MGE-type GABAergic interneuron cell therapy for chronic focal epilepsy
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Synaptophysin Immunoreactivity in the Human Hippocampus and Neocortex From 6 to 41 Weeks of Gestation
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“Calretinin reactivity in 10% of cortical neurons that represent a major subset of GABAergic interneurons (28, 29) was seen at earlier time points than”
Influential
Selective loss of parvalbumin-positive GABAergic interneurons in the cerebral cortex of maternally stressed Gad1-heterozygous mouse offspring
Uchida, T., Furukawa, T., Iwata, S., Yanagawa, Y., & Fukuda, A. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.13 · Cited by 74
Hypothesis on the Dual Origin of the Mammalian Subplate
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“…is at the border of the intermediate zone and SVZ and smaller streams of migrating cells are present in the subplate and the upper part of marginal zone (Anderson et al., 1997; Pleasure et al., 2000; Molnár et al., 2006; Wonders and Anderson, 2006; Heng et al., 2007; Métin et al., 2007, 2008).”
Neonatal Estradiol Stimulation Prevents Epilepsy in Arx Model of X-Linked Infantile Spasms Syndrome
Olivetti, P. R., Maheshwari, A., & Noebels, J. L. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3007231 · Cited by 73
Deficient or Excess Folic Acid Supply During Pregnancy Alter Cortical Neurodevelopment in Mouse Offspring
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“…cerebral neocortex, the site of higher-order capacities of the human brain, six horizontal layers can be distinguished, each populated by excitatory and inhibitory neurons of distinct identities and functions (Gupta et al. 2002; Wonders and Anderson 2006; Kwan et al. 2012; DeFelipe et al. 2013).”
The plasticitome of cortical interneurons
McFarlan, A. R., Chou, C. Y. C., Watanabe, A., Cherepacha, N., Haddad, M. G., Owens, H., & Sjöström, P. J. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00663-9 · Cited by 74
Imbalance of Excitatory/Inhibitory Neuron Differentiation in Neurodevelopmental Disorders with an NR2F1 Point Mutation
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Recent advances in gene therapy for neurodevelopmental disorders with epilepsy
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“An additional constraint is that gene therapy for NDD+E may need to be administered within a critical period before mature circuits are in place, possibly even embryonically, to rescue all aspects of the pathogenic phenotype (Wykes & Lignani 2018) (Table 2).”
Background
Girdin Is an Intrinsic Regulator of Neuroblast Chain Migration in the Rostral Migratory Stream of the Postnatal Brain
Wang, Y., Kaneko, N., Asai, N., Enomoto, A., Isotani-Sakakibara, M., Kato, T., Asai, M., Murakumo, Y., Ota, H., Hikita, T., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1130-11.2011 · Cited by 72
“The data suggest that Girdin appears to be required for either cortical interneuron migration from their birthplace (the ganglionic eminence of the basal telencephalon) toward the developing neocortex (Wonders and Anderson, 2006) or for the acquisition of a GABAergic phenotype at later times.”
Background
LSD1 co-repressor Rcor2 orchestrates neurogenesis in the developing mouse brain
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Lack of Cdkl5 Disrupts the Organization of Excitatory and Inhibitory Synapses and Parvalbumin Interneurons in the Primary Visual Cortex
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Radial glia in the ventral telencephalon
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Optimizing neuronal differentiation from induced pluripotent stem cells to model ASD
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“In contrast to STT and PVexpressing GABAergic neurons, which mostly originate from the MGE, the developmental mechanism of calreticulin (CR)-type interneurons that arise mostly in the CGE was not well-known.”
BackgroundInfluential
Differential neuronal reprogramming induced by NeuroD1 from astrocytes in grey matter versus white matter
Li, W., Chen, G., Liu, M., Zheng, J., Xu, Y., & He, Q. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.265185 · Cited by 72
“This is consistent with the native distribution pattern of more PV neurons in the cortex than in the striatum (Wonders and Anderson, 2006; Tepper et al., 2018).”
Background
Glutamatergic neuron-targeted loss of LGI1 epilepsy gene results in seizures
Boillot, M., Huneau, C., Marsan, E., Lehongre, K., Navarro, V., Ishida, S., Dufresnois, B., Özkaynak, E., Garrigue, J., Miles, R., et al. (2014) · Brain · doi:10.1093/brain/awu259 · Cited by 67
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An SNP in an ultraconserved regulatory element affects Dlx5/Dlx6 regulation in the forebrain
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“These four markers were specifically chosen on the basis of previous findings showing that most CB+, PV+ and SOM+ interneurons originate from the MGE, whereas the CGE is one major origin of CR+ interneurons (Fogarty et al., 2007; Wonders and Anderson, 2006; Wonders et al., 2008).”
Background
Local Thyroid Hormone Action in Brain Development
Alcaide, M. A., & Mayerl, S. E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512352 · Cited by 70
“5 in the ganglionic eminences of the ventral telencephalon in a temporally and spatially tightly regulated process [15,95].”
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Synaptic and cellular organization of layer 1 of the developing rat somatosensory cortex
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Postnatal Development of 2 Microcircuits Involving Fast-Spiking Interneurons in the Mouse Prefrontal Cortex
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In Vitro Development of Human iPSC-Derived Functional Neuronal Networks on Laser-Fabricated 3D Scaffolds
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Regionalized Loss of Parvalbumin Interneurons in the Cerebral Cortex of Mice with Deficits in GFRα1 Signaling
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“…have analyzed the effects of mutations in genes affecting large numbers, if not the majority, of GABAergic neurons or their progenitors, and found reductions in the number of interneurons across large areas of the cortex (Levitt et al., 2004; Wonders and Anderson, 2006; Liodis et al., 2007).”
Background
Subventricular Zone-Derived Neuroblasts Use Vasculature as a Scaffold to Migrate Radially to the Cortex in Neonatal Mice
Magueresse, C. L., Alfonso, J., Bark, C., Eliava, M., Khrulev, S., & Monyer, H. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr302 · Cited by 66
Dynamics of the leading process, nucleus, and Golgi apparatus of migrating cortical interneurons in living mouse embryos
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Behavior and lineage progression of neural progenitors in the mammalian cortex
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“In the ventral telencephalon, RGPs generate g-aminobutyric acid (GABA)-ergic inhibitory interneurons and glia that migrate tangentially to the future cerebral cortex [1].”
Background
Mafb and c-Maf Have Prenatal Compensatory and Postnatal Antagonistic Roles in Cortical Interneuron Fate and Function
Pai, E. L.-L., Vogt, D. L., Clemente-Perez, A., McKinsey, G. L., Cho, F. S., Hu, J. S., Wimer, M., Paul, A., Darbandi, S. F., Pla, R., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.031 · Cited by 66
“1-Cre (Xu et al., 2008) alleles, whose expression in the MGE and POA begins on embryonic day (E) ~9.5.”
BackgroundInfluential
Generating Human Neurons In Vitro and Using Them to Understand Neuropsychiatric Disease
Pașca, S. P., Panagiotakos, G., & Dolmetsch, R. E. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170328 · Cited by 68
“This complexity emerges from a sequence of elaborately coordinated developmental processes that result in the generation of distinct neuronal cell types at specific times and locations (Farkas & Huttner 2008, Okano & Temple 2009, Tiberi et al. 2012, Wonders & Anderson 2006).”
Background
Somatostatin interneurons delineate the inner part of the external plexiform layer in the mouse main olfactory bulb
Lepousez, G., Csaba, Z., Bernard, V., Loudes, C., Videau, C., Lacombe, J., Epelbaum, J., & Viollet, C. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22317 · Cited by 63
“…origin: hippocampal and cortical SRIF interneurons both originate from the median ganglionic eminence (Danglot et al., 2006; Métin et al., 2006; Wonders and Anderson, 2006), whereas most bulbar interneurons originate from the lateral ganglionic eminence and the dorsal telencephalon (Bovetti…”
Background
Prefrontal cognitive deficits in mice with altered cerebral cortical GABAergic interneurons
Bissonette, G. B., Bae, M. H., Suresh, T., Jaffe, D. E., & Powell, E. M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.10.051 · Cited by 64
“molecules [9].”
Adaptation, Expertise, and Giftedness: Towards an Understanding of Cortical, Subcortical, and Cerebellar Network Contributions
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“However, approximately 25–30% of cortical connections include inhibitory interneurons, which modulate cortical activity [92].”
Background
Functional impact of interneuronal inhibition in the cerebral cortex of behaving animals
Merchant, H., de Lafuente, V., Peña‐Ortega, F., & Larriva-Sahd, J. A. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.08.005 · Cited by 63
Foxp2 regulates neuronal differentiation and neuronal subtype specification
Chiu, Y.-C., Li, M., Liu, Y., Ding, J., Yu, J., & Wang, T. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22166 · Cited by 61
Conserved rules in embryonic development of cortical interneurons
Laclef, C., & Métin, C. (2018) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2017.09.017 · Cited by 57
“They are produced in different MGE regions, with SST(+) interneurons induced by higher level of SHH signaling in the dorsal MGE [17,69-71], Review in [72].”
The LIM Homeodomain Protein Lhx6 Regulates Maturation of Interneurons and Network Excitability in the Mammalian Cortex
Neves, G., Shah, M. M., Liodis, P., Achimastou, A., Denaxa, M., Roalfe, G., Sesay, A. K., Walker, M. C., & Pachnis, V. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs159 · Cited by 62
“Here, we characterize a novel hypomorphic allele of Lhx6 and demonstrate that reduced activity of this locus leads to widespread differentiation defects in Sst+ interneurons, but relatively minor and localized changes in Pva+ interneurons.”
Background
Aristaless-related homeobox gene disruption leads to abnormal distribution of GABAergic interneurons in human neocortex: evidence based on a case of X-linked lissencephaly with abnormal genitalia (XLAG)
Okazaki, S., Ohsawa, M., Kuki, I., Kawawaki, H., Koriyama, T., Ri, S., Ichiba, H., Hai, E., Inoue, T., Nakamura, H., et al. (2008) · Acta Neuropathologica · doi:10.1007/s00401-008-0382-2 · Cited by 61
“Among them, CR- or CCK-containing cells migrate from the caudal lateral ganglionic eminence (CGE and LGE) and NPY- or PVcontaining cells originate from the medial ganglionic eminence (MGE) [ 27 ].”
Background
Differential effects of BMP signaling on parvalbumin and somatostatin interneuron differentiation
Mukhopadhyay, A., McGuire, T. L., Peng, C., & Kessler, J. A. (2009) · Development · doi:10.1242/dev.034439 · Cited by 60
“1 (KCNC1 – Mouse Genome Informatics) and SST+ interneurons coexpress CR or NPY (Kawaguchi and Kondo, 2002; Wonders and Anderson, 2006).”
Background
Stem cell-derived interneuron transplants as a treatment for schizophrenia: preclinical validation in a rodent model
Donegan, J. J., Tyson, J. A., Branch, S. Y., Beckstead, M. J., Anderson, S. A., & Lodge, D. J. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.121 · Cited by 60
“This effect is thought to be due to sonic hedgehog (Shh) signaling, which occurs in a gradient in the MGE, with higher levels of Shh in the dorsal versus ventral areas of the MGE 32 .”
InfluentialSelf-citation

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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