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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Background
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Background
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Background
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Background
Loss of Dopamine D2 Receptors Increases Parvalbumin-Positive Interneurons in the Anterior Cingulate Cortex
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Background
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Background
Cell-type specific pallial circuits shape categorical tuning responses in the crow telencephalon
Ditz, H. M., Fechner, J., & Nieder, A. (2022) · Communications Biology · doi:10.1038/s42003-022-03208-z · Cited by 19
Neural Circuit Mechanisms Involved in Animals’ Detection of and Response to Visual Threats
Wu, Q., & Zhang, Y. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-023-01021-0 · Cited by 21
“One interesting fact about these neurons is that they are excitatory and not inhibitory, unlike most PV+ neurons [134].”
Background
Default Patterning Produces Pan-cortical Glutamatergic and CGE/LGE-like GABAergic Neurons from Human Pluripotent Stem Cells
Floruta, C. M., Du, R., Kang, H., Stein, J. L., & Weick, J. P. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.09.023 · Cited by 19
“In vivo, MGE-derived INs are thought to comprise approximately 60% of cortical interneurons with CGE- derived interneurons supplying an additional 30% (Wonders and Anderson, 2006).”
BackgroundInfluential
Hyperactive MEK1 Signaling in Cortical GABAergic Neurons Promotes Embryonic Parvalbumin Neuron Loss and Defects in Behavioral Inhibition
Holter, M. C., Hewitt, L. T., Nishimura, K. J., Knowles, S. J., Bjorklund, G. R., Shah, S., Fry, N., Rees, K. P., Gupta, T. A., Daniels, C. W., et al. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa413 · Cited by 22
“ganglionic eminence (MGE) and migrate tangentially into the cortex (Tamamaki et al. 1997; Lavdas et al. 1999; Marin and Rubenstein 2003; Wonders and Anderson 2006; Gelman and Marín 2010).”
Background
Interneuron origins in the embryonic porcine medial ganglionic eminence
Casalia, M. L., Li, T., Ramsay, H. J., Ross, P. J., Paredes, M. F., & Baraban, S. C. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2738-20.2021 · Cited by 19
Examining the genetic and neural components of cognitive flexibility using mice
Brigman, J. L., Powell, E. M., Mittleman, G., & Young, J. W. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.12.024 · Cited by 17
“The forebrain GABAergic interneurons originate embryonically from subcortical sources, in the precursor to the dorsal striatum [23].”
Background
Early Postnatal Migration and Development of Layer II Pyramidal Neurons in the Rodent Cingulate/Retrosplenial Cortex
Zgraggen, E., Boitard, M., Roman, I., Kanemitsu, M., Potter, G., Salmon, P., Vutskits, L., Dayer, A. G., & Kiss, J. Z. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr097 · Cited by 19
“Although the majority of cortical interneurons are arising from the medial ganglionic eminence (MGE) and reach the cortex after tangential migration (Wonders and Anderson 2006; Gelman and Marin 2010), the dorsal SVZ in mice may also be the source of precursors for calretinin-positive GABAergic…”
Background
ARX polyalanine expansion mutations lead to migration impediment in the rostral cortex coupled with a developmental deficit of calbindin-positive cortical GABAergic interneurons
Lee, K., Ireland, K., Bleeze, M., & Shoubridge, C. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.06.010 · Cited by 18
Dynamic properties of mitochondria during human corticogenesis
Baum, T., & Gama, V. (2021) · Development · doi:10.1242/dev.194183 · Cited by 20
Migratory Behavior of Presumptive Interneurons Is Affected by AMPA Receptor Activation in Slice Cultures of Embryonic Mouse Neocortex
Yozu, M., Tabata, H., König, N., & Nakajima, K. (2007) · Developmental Neuroscience · doi:10.1159/000109856 · Cited by 19
“…tangentially into the cortex [Anderson et al., 1997; Tamamaki et al., 1997; Parnavelas, 2000; Corbin et al., 2001; Marin and Rubenstein, 2001; Nadarajah and Parnavelas, 2002; Marin and Rubenstein, 2003; Tanaka et al., 2003; Metin et al., 2006; Wonders and Anderson, 2006; Nakajima, in press].”
Background
Developmental Differences in Neocortex Neurogenesis and Maturation Between the Altricial Dwarf Rabbit and Precocial Guinea Pig
Kalusa, M., Heinrich, M. D., Sauerland, C., Morawski, M., & Fietz, S. A. (2021) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2021.678385 · Cited by 19
“Intriguingly, these axonal extensions were mostly oriented parallel to the ventricular surface (Figures 8C–E,J, 9D), thus, supporting previous studies that have identified the IZ to be populated by interneurons that migrate tangentially from the ventral into the dorsal telencephalon during early embryonic development…”
Result
Transcranial Magnetic Stimulation and Neocortical Neurons: The Micro-Macro Connection
Tian, D., & Izumi, S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.866245 · Cited by 18
Development and Regeneration of Projection Neuron Subtypes of the Cerebral Cortex
Tomassy, G. S., Lodato, S., Trayes-Gibson, Z., & Arlotta, P. (2010) · Science Progress · doi:10.3184/003685010x12705764469952 · Cited by 20
Cilia
Métin, C., & Pedraza, M. (2014) · The Neuroscientist · doi:10.1177/1073858414543151 · Cited by 20
Asymmetry of Radial and Symmetry of Tangential Neuronal Migration Pathways in Developing Human Fetal Brains
Miyazaki, Y., Song, J. W., & Takahashi, E. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00002 · Cited by 18
Cell-based therapies for the treatment of schizophrenia
Donegan, J. J., & Lodge, D. J. (2016) · Brain Research · doi:10.1016/j.brainres.2016.08.010 · Cited by 19
“1 is down-regulated and Lhx6 expression increases and is maintained throughout the life of the cell (Wonders and Anderson, 2006).”
Background
Progressive divisions of multipotent neural progenitors generate late-born chandelier cells in the neocortex
Sultan, K. T., Liu, W. A., Li, Z.-L., Shen, Z., Li, Z., Zhang, X., Dean, O. R., Ma, J., & Shi, S. (2018) · Nature Communications · doi:10.1038/s41467-018-07055-7 · Cited by 20
PDK1 regulates the survival of the developing cortical interneurons
Wei, Y., Han, X., & Zhao, C. (2020) · Molecular Brain · doi:10.1186/s13041-020-00604-6 · Cited by 18
“Cell counting showed that total numbers of PH3+ cells in the VZ and SVZ of the MGE were comparable (Fig.”
Influential
Postnatal differentiation of cortical interneuron signalling
Sauer, J., & Bartos, M. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07872.x · Cited by 18
“Most cortical GABAergic cells are born at embryonic stages in the subpallial ganglionic eminences, from where precursors migrate tangentially into the cortex (Anderson et al., 1997; Pleasure et al., 2000; Wonders & Anderson, 2006).”
Background
Characterization of a subpopulation of developing cortical interneurons from human iPSCs within serum-free embryoid bodies
Nestor, M. W., Jacob, S., Sun, B. Q., Prè, D., Sproul, A. A., Hong, S. I., Woodard, C. M., Zimmer, M., Chinchalongporn, V., Arancio, O., et al. (2014) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00263.2014 · Cited by 17
“In the mouse, 50–60% of all interneurons originate in the MGE and 30–40% originate in the CGE (2, 49).”
BackgroundInfluential
Development of Cortical GABAergic Innervation
Jovanovic, J. N., & Thomson, A. M. (2011) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2011.00014 · Cited by 20
“Parvalbumin-positive interneurons originate from the ventral area of the MGE (Wonders and Anderson, 2006) and their development relies on the activity of the Lhx6 transcription factor which is itself controlled by the Nkx2.”
Influential
Sociability development in mice with cell-specific deletion of the NMDA receptor NR1 subunit gene
Ferri, S. L., Pallathra, A. A., Kim, H., Dow, H. C., Raje, P., McMullen, M., Bilker, W. B., Siegel, S. J., Abel, T., & Brodkin, E. S. (2020) · Genes, Brain and Behavior · doi:10.1111/gbb.12624 · Cited by 15
“Specifically, mice with a floxed NR1 allele were crossed with mice with Cre recombinase expression in postnatal pyramidal cells of the forebrain, driven by the calcium/calmodulin-dependent kinase IIα (CaMKIIα) promoter, or with mice with Cre recombinase expression driven by the parvalbumin (PV) promoter, which constit…”
Background
The Principle of Cortical Development and Evolution
Yang, Z. (2024) · Neuroscience Bulletin · doi:10.1007/s12264-024-01259-2 · Cited by 19
Cortical and Commissural Defects Upon HCF‐1 Loss in Nkx2.1‐Derived Embryonic Neurons and Glia
Minocha, S., & Herr, W. (2019) · Developmental Neurobiology · doi:10.1002/dneu.22704 · Cited by 17
“These cells ensure proper cortical development and function, and commissure formation (Wonders and Anderson, 2006; Lindwall et al., 2007; Minocha et al., 2015b).”
Background
Probing the molecular and cellular pathological mechanisms of schizophrenia using human induced pluripotent stem cell models
Sebastian, R., Song, Y., & Pak, C. (2022) · Schizophrenia Research · doi:10.1016/j.schres.2022.06.028 · Cited by 16
Imbalance of interneuron distribution between neocortex and basal ganglia: Consideration of epileptogenesis of focal cortical dysplasia
Sakakibara, T., Sukigara, S., Otsuki, T., Takahashi, A., Kaneko, Y., Kaido, T., Saito, Y., Sato, N., Nakagawa, E., Sugai, K., et al. (2012) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2012.08.035 · Cited by 17
“1‐expressing domain of the medial ganglionic eminence [24].”
Background
Thyroid hormone insufficiency alters the expression of psychiatric disorder-related molecules in the hypothyroid mouse brain during the early postnatal period
Uchida, K., Hasuoka, K., Fuse, T., KOBAYASHI, K. P., Moriya, T., Suzuki, M., Katayama, N., & Itoi, K. (2021) · Scientific Reports · doi:10.1038/s41598-021-86237-8 · Cited by 17
MET signaling in GABAergic neuronal precursors of the medial ganglionic eminence restricts GDNF activity in cells that express GFRα1 and a new transmembrane receptor partner
Perrinjaquet, M., Sjöstrand, D., Moliner, A., Zechel, S., Lamballe, F., Maina, F., & Ibáñez, C. F. (2011) · Journal of Cell Science · doi:10.1242/jcs.083717 · Cited by 16
“Introduction The inhibitory (GABAergic) interneurons of the cerebral cortex are born in transient neurogenic zones located in the ventral telencephalon known as the ganglionic eminences (Corbin et al., 2001; Levitt et al., 2004; Marín and Rubenstein, 2003; Wonders and Anderson, 2006).”
Background
In vivo two-photon imaging of the embryonic cortex reveals spontaneous ketamine-sensitive calcium activity
Yuryev, M. V., Andriichuk, L., Leiwe, M. N., Jokinen, V. P., Carabalona, A., & Rivera, C. (2018) · Scientific Reports · doi:10.1038/s41598-018-34410-x · Cited by 17
Contributions of Glutamate and GABA Systems to the Neurobiology and Treatment of Schizophrenia
Krystal, J. H., & Moghaddam, B. (2010) · Wiley eBooks · doi:10.1002/9781444327298.ch21 · Cited by 17
Application of Medial Ganglionic Eminence Cell Transplantation in Diseases Associated With Interneuron Disorders
Li, D., Wu, Q., & Han, X. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.939294 · Cited by 17
“PV+ interneurons rapidly spike and target the initial segment of axons and cell bodies to regulate the discharge of pyramidal cells; interneurons containing SST exhibit slow-firing patterns and synaptic formation in the distal dendrites of pyramidal cells (Perez et al., 2019).”
BackgroundInfluential
Perturbations in cortical development and neuronal network excitability arising from prenatal exposure to benzodiazepines in mice
Haas, M., Qu, Z., Kim, T. H., Vargas, E., Campbell, K., Petrou, S., Tan, S., Reid, C. A., & Heng, J. I. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12167 · Cited by 16
“by investigating the distribution of interneurons that show mutually exclusive expression of parvalbumin and calretinin (Wonders and Anderson 2006).”
BackgroundInfluential
Efficient Generation of Corticofugal Projection Neurons from Human Embryonic Stem Cells
Zhu, X., Ai, Z., Hu, X., & Li, T. (2016) · Scientific Reports · doi:10.1038/srep28572 · Cited by 16
“1038/srep28572 rise to mature neurons and integrate well into brains, and (5) regenerate CfuPNs and inhibitory interneurons in vitro and in vivo at a cellular level.”
Background
Postnatal development of GABAergic interneurons and perineuronal nets in mouse temporal cortex subregions
Ueno, H., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Okamoto, M., Aoki, S., & Ishihara, T. (2017) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.08.003 · Cited by 18
“In the mouse primary sensory cortex, CR neurons were present at P0 and decreased with postnatal development (Wonders and Anderson, 2006; Gonchar et al., 2008).”
Background
A Method to Culture GABAergic Interneurons Derived from the Medial Ganglionic Eminence
Franchi, S. A., Macco, R., Astro, V., Tonoli, D., Savino, E., Valtorta, F., Sala, K., Botta, M., & de Curtis, I. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00423 · Cited by 20
“Most cortical and hippocampal GABAergic cells originate from ganglionic eminences, transitory embryonic structures of the ventral telencephalon (Wonders and Anderson, 2006).”
BackgroundMethod
Understanding the impact of ZBTB18 missense variation on transcription factor function in neurodevelopment and disease
Heng, J. I., Viti, L., Pugh, K., Marshall, O. J., & Agostino, M. (2022) · Journal of Neurochemistry · doi:10.1111/jnc.15572 · Cited by 11
“…along distinct paths, guided by cell- intrinsic transcriptional regulatory mechanisms as well as by attractive and repulsive molecular cues within the tissue environment (Hu, Vogt, Sandberg, & Rubenstein, 2017; Lim, Mi, Llorca, & Marin, 2018; Southwell et al., 2014; Wonders & Anderson, 2006).”
Background
The Future of Research in Tourette Syndrome
Cavanna, A. E., Kavanagh, C., & Robertson, M. M. (2013) · Behavioural Neurology · doi:10.1155/2013/249820 · Cited by 15
Cell type-specific DNA methylome signatures reveal epigenetic mechanisms for neuronal diversity and neurodevelopmental disorder
Jin, Y., Su, K., Kong, H. E., Ma, W., Wang, Z., Li, Y., Li, R., Allen, E. G., Wu, H., & Jin, P. (2022) · Human Molecular Genetics · doi:10.1093/hmg/ddac189 · Cited by 16
microRNA-dependent regulation of gene expression in GABAergic interneurons
Kołosowska, K., Schratt, G. M., & Winterer, J. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1188574 · Cited by 16
“However, the role of miRNA-181a-5p regulation of PV IN function and its contribution to the excitatory-inhibitory balance warrants further investigation. miRNA-24 The transcription factor Sox6 is crucial for subtype determination of MGE-derived postmitotic INs by suppression of PV IN specification while inducing speci…”
BackgroundInfluential
SIMS: A deep-learning label transfer tool for single-cell RNA sequencing analysis
Gonzalez-Ferrer, J., Lehrer, J., O’Farrell, A., Paten, B., Teodorescu, M., Haussler, D. H., Jönsson, V. D., & Mostajo-Radji, M. A. (2024) · Cell Genomics · doi:10.1016/j.xgen.2024.100581 · Cited by 16
Divergent opioid-mediated suppression of inhibition between hippocampus and neocortex across species and development
Caccavano, A., Vlachos, A., McLean, N., Kimmel, S., Kim, J. H., Vargish, G. A., Mahadevan, V., Hewitt, L. T., Rossi, A. M., Spineux, I., et al. (2024) · Neuron · doi:10.1016/j.neuron.2025.03.005 · Cited by 15
“PV-INs throughout the forebrain have common developmental origins in the medial ganglionic eminence (MGE) 38 and are often treated as monolithic with common circuit motif functionality, leading to textbook observations of neuromodulatory control of inhibitory microcircuits that may not generalize…”
Influential
Neurogenesis in the Basal Ganglia
Rubenstein, J. L. R., & Campbell, K. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397265-1.00097-6 · Cited by 14

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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