Genetic Fate Mapping Reveals That the Caudal Ganglionic Eminence Produces a Large and Diverse Population of Superficial Cortical Interneurons
Open accessAbstract
By combining an inducible genetic fate mapping strategy with electrophysiological analysis, we have systematically characterized the populations of cortical GABAergic interneurons that originate from the caudal ganglionic eminence (CGE). Interestingly, compared with medial ganglionic eminence (MGE)-derived cortical interneuron populations, the initiation [embryonic day 12.5 (E12.5)] and peak production (E16.5) of interneurons from this embryonic structure occurs 3 d later in development. Moreover, unlike either pyramidal cells or MGE-derived cortical interneurons, CGE-derived interneurons do not integrate into the cortex in an inside-out manner but preferentially (75%) occupy superficial cortical layers independent of birthdate. In contrast to previous estimates, CGE-derived interneurons are both considerably greater in number (approximately 30% of all cortical interneurons) and diversity (comprised by at least nine distinct subtypes). Furthermore, we found that a large proportion of CGE-derived interneurons, including the neurogliaform subtype, express the glycoprotein Reelin. In fact, most CGE-derived cortical interneurons express either Reelin or vasoactive intestinal polypeptide. Thus, in conjunction with previous studies, we have now determined the spatial and temporal origins of the vast majority of cortical interneuron subtypes.
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NPY+ multipolar interneurons and Meis2+ interstitial GABAergic neurons express 5HT3aR; NPY+ multipolar cells have irregular spiking and are abundant at the layer 1/2 boundary, while Meis2+ neurons reside in white matter and extend axons to deep cortex and striatum.
“Two additional types of interneuron express 5HT3aR: NPY+ multipolar cells and Meis2+ interstitial GABAergic neurons. NPY+ multipolar interneurons exhibit irregular spiking properties and are particularly abundant at the boundary between layers 1 and 2”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Miyoshi et al., 2010
A temporal sequence has been described for the generation of neuronal diversity in the CGE.
“a temporal sequence has also been described for the generation of neuronal diversity in the CGE”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Miyoshi et al., 2010
E13.5 MGE and E14.5 CGE/LGE correspond to peak neurogenesis in these structures.
“We manually dissected the embryonic day (E)13.5 MGE or E14.5 CGE and LGE from wild type mouse embryos, timepoints corresponding to peak neurogenesis in these structures7,8”
From Developmental diversification of cortical inhibitory interneurons (2018) · cites this paper as [8]
Reelin is frequently coexpressed with SST in O-LM and Martinotti cells, but is not selective for or necessarily comprehensively expressed by these interneurons.
“Reelin is frequently coexpressed with SST in O-LM and Martinotti cells, but is not selective for or necessarily comprehensively expressed by these interneurons (203, 367, 651, 796, 899).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
Neocortical NGFCs have singular origins within the CGE.
“In contrast, neocortical NGFCs have singular origins within the CGE (651, 796, 1179).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
Molecular markers associated with NGFCs include NPY, reelin, neuronal nitric oxide synthase (nNOS), α-actinin 2, and COUP transcription factor 2 (COUPTF2).
“Molecular markers associated with NGFCs include NPY, reelin, neuronal nitric oxide synthase (nNOS), α-actinin 2, and COUP transcription factor 2 (COUPTF2) (48, 367, 549, 796, 858, 926, 1137).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
Temporal dynamics significantly impact mature interneuron fate.
“Complementing the spatial control of interneuron specification within the GEs is a temporal dynamic that has significant impact on mature interneuron fate”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
In both neocortex and hippocampus, CR- and VIP-expressing ISIs represent subsets of 5-HT3AR-expressing interneurons and have singular origin in the CGE (combined ISIs represent 30% of CGE-derived interneurons based on assumptions outlined above).
“In both neocortex and hippocampus, CR- and VIP-expressing ISIs represent subsets of 5-HT3AR-expressing interneurons and have singular origin in the CGE (combined ISIs represent 30% of CGE-derived interneurons based on assumptions outlined above) (102, 203, 651, 796, 1138, 1179).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
CGE interneuronogenesis lags that of the MGE both for initial generation (E12.5 for CGE vs. E9.5 for MGE) and peak generation (E16.5 for CGE vs. E13.5 for MGE).
“CGE interneuronogenesis was demonstrated to lag that of the MGE both for initial (E12.5 for CGE vs. E9.5 for MGE) and peak (E16.5 for CGE vs. E13.5 for MGE) generation”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
In the neocortex, NGFCs, ISIs, and CCK-expressing interneurons are derived from CGE progenitors.
“In the neocortex NGFCs (reelin-expressing, SST negative), ISIs (VIP- and CR-expressing), and CCK-expressing interneurons (e.g., CCKBCs) are derived from CGE progenitors”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
The CGE produces approximately 30% of neocortical and hippocampal interneurons.
“The CGE produces ~30% of neocortical and hippocampal interneurons”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
In contrast to the MGE, the subtypes of neocortical interneurons generated within the CGE do not change significantly over time, with similar proportions of reelin-expressing NGFCs and VIP/CR-expressing ISIs generated across CGE neurogenesis.
“in contrast to the MGE, the subtypes of neocortical interneurons generated within the CGE do not change significantly over time with similar proportions of reelin-expressing NGFCs and VIP/CR-expressing ISIs generated across CGE neurogenesis”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
In cortex, MGE-derived cells are biased towards deep layers and CGE-derived cells towards superficial layers.
“In cortex, MGE- and CGE-derived cells are biased towards the deep and superficial layers, respectively”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
CGE-derived interneurons lack correlation with birth order; their attraction to superficial layers is dominant regardless of birthdate.
“CGE-derived interneurons lack any such correlation with birth order; rather, their attraction to the superficial layers is dominant regardless of birthdate”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
The majority of CGE-derived interneurons that did not express reelin expressed VIP.
“The majority of CGE-derived interneurons that did not express reelin expressed VIP.”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
All nine identified cell types largely exhibit a continuum of intrinsic parameters.
“Close inspection of the electrophysiological properties of these cells, however, highlight few features that are distinct to one or few cell types, with only minor exceptions, and all nine identified cell types largely exhibit a continuum of intrinsic parameters.”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
Miyoshi et al. observed that a divergent population of CGE-derived cells parsed into nine distinct subtypes based on morphology, cell layer positioning, firing patterns, and other intrinsic properties.
“They observed that this divergent population of CGE-derived cells parsed into nine distinct subtypes based on morphology, cell layer positioning, firing patterns, and other intrinsic properties.”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [796]
Interneurons derived from the CGE tend to occupy the expanded upper layers of the neocortex.
“because CGE-derived interneurons preferentially occupy the expanded upper neocortical layers49”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [49]
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“03 for the NDNF/nonNPY and 7 populations respectively; for statistics, see Table 3), resembling the “fast-adapting” VIP INs previously described in layers 1–3 (Lee et al., 2010; Miyoshi et al., 2010; Prönneke et al., 2015).”
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Maturation-Promoting Activity of SATB1 in MGE-Derived Cortical Interneurons
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Self-citation
- Authors
- Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J. B., Battiste, J., Johnson, J. E., Machold, R. P., & Fishell, G.
- Affiliations
- New York University (US)
- Imperial College London (GB)
- The University of Texas Southwestern Medical Center (US)
- NYU Langone Health (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-02-03
- Volume
- 30
- Issue
- 5
- Pages
- 1582-1594
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2826846
- OpenAlex
- W1975767398
- Cited by
- 559
- References
- 81
- Citations by year
- 2026: 14 · 2025: 20 · 2024: 23 · 2023: 26 · 2022: 25 · 2021: 34 · 2020: 54 · 2019: 42 · 2018: 30 · 2017: 37 · 2016: 37 · 2015: 40 · 2014: 38 · 2013: 53 · 2012: 38
- FWCI
- 13.98
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Simons Foundation
- New York State Stem Cell Science
- National Institutes of Health (GAD67)
- Japan Society for the Promotion of Science
- National Institute of Mental Health (R01MH071679, R37MH071679)
- National Institute of Neurological Disorders and Stroke (R01NS039007)
- 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
- caudal ganglionic eminence, cortical interneurons, GABAergic interneurons, interneuron subtypes, reelin, vasoactive intestinal peptide, medial ganglionic eminence, cortical development
- MeSH terms
- Reelin Protein, Animals, Cell Differentiation, Cerebral Cortex, Genetic Markers, Genetic Techniques, Interneurons, Male, Nerve Tissue Proteins, Serine Endopeptidases, Cell Adhesion Molecules, Neuronal, Extracellular Matrix Proteins, Prosencephalon, Patch-Clamp Techniques, Cell Lineage, Body Patterning, Mice
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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