The embryonic preoptic area is a novel source of cortical GABAergic interneurons
Open accessAbstract
GABA-containing (GABAergic) interneurons play an important role in the function of the cerebral cortex. Through mostly inhibitory mechanisms, interneurons control hyperexcitability and synchronize and shape the spatiotemporal dynamics of cortical activity underlying various brain functions. Studies over the past 10 years have demonstrated that, in most mammals, interneurons originate during development from the subcortical telencephalon--the subpallium--and reach the cerebral cortex through tangential migration. Until now, interneurons have been demonstrated to derive exclusively from two subpallial regions, the medial ganglionic eminence and the caudal ganglionic eminence. Here, we show that another subpallial structure, the preoptic area, is a novel source of cortical GABAergic interneurons in the mouse. In utero labeling and genetic lineage-tracing experiments demonstrate that neurons born in this region migrate to the neocortex and hippocampus, where they differentiate into a distinct population of GABAergic interneurons with relatively uniform neurochemical, morphological, and electrophysiological properties.
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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 Gelman et al., 2009
Neurogliaform cells and multipolar NPY+ interneurons are born in the preoptic region.
“Neurogliaform cells and multipolar NPY+ interneurons are born in the preoptic region”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Gelman et al., 2009
The POA is estimated to produce approximately 10% of neocortical and hippocampal interneurons.
“The POA is estimated to produce ~10% of neocortical and hippocampal interneurons”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [391]
Mature cortical interneurons derived from the POA are highly diverse, consisting of small fractions of PV-, SST-, NPY-, and reelin-expressing interneurons.
“Mature cortical interneurons derived from the POA are highly diverse consisting of small fractions of PV-, SST-, NPY-, and reelin-expressing interneurons”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [391]
Two subdomains are found in the POA based on nonoverlapping expression profiles for Dbx1 and Nkx5.1.
“Two subdomains are found in the POA based on nonoverlapping expression profiles for Dbx1 and Nkx5.1”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [391]
GIFM studies using Nkx5.1-Cre mice revealed primarily superficial multipolar mature cortical interneurons expressing NPY and reelin, but not PV, SST, CR, or VIP.
“GIFM studies using Nkx5.1-Cre mice revealed primarily superficial multipolar mature cortical interneurons expressing NPY and reelin, but not other typical interneuron markers such as PV, SST, CR, and VIP”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [391]
Most interneuron precursors emerging from the POA do not rely on downstream activation of Lhx6 to specify PV and SST interneurons.
“most interneuron precursors emerging from the POA do not rely on downstream activation of Lhx6 to specify PV and SST interneurons”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [391]
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References 63 · Cited by 280
- Authors
- Gelman, D. M., Martini, F. J., Nóbrega-Pereira, S., Pierani, A., Kessaris, N., & Marín, O.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- Centre National de la Recherche Scientifique (FR)
- University College London (GB)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2009-07-22
- Volume
- 29
- Issue
- 29
- Pages
- 9380-9389
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6665570
- OpenAlex
- W1970400919
- Cited by
- 280
- References
- 63
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 5 · 2023: 14 · 2022: 9 · 2021: 17 · 2020: 22 · 2019: 19 · 2018: 13 · 2017: 14 · 2016: 17 · 2015: 17 · 2014: 13 · 2013: 33 · 2012: 17
- FWCI
- 7.94
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, other-oa)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- European Commission (005139)
- Ministerio de Ciencia e Innovación (CSD2007-00023)
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- GABAergic interneurons, preoptic area, subpallium, tangential migration, medial ganglionic eminence, caudal ganglionic eminence, hippocampus, neocortex, neuronal lineage tracing
- MeSH terms
- Animals, Brain, Cell Movement, Cerebral Cortex, gamma-Aminobutyric Acid, Hippocampus, Immunohistochemistry, Interneurons, Mice, Transgenic, Preoptic Area, RNA, Messenger, Stem Cells, In Situ Hybridization, Electroporation, Patch-Clamp Techniques, Cell Lineage, Mice, In Vitro Techniques
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