Common Origins of Hippocampal Ivy and Nitric Oxide Synthase Expressing Neurogliaform Cells
Open accessAbstract
GABAergic interneurons critically regulate cortical computation through exquisite spatiotemporal control over excitatory networks. Precision of this inhibitory control requires a remarkable diversity within interneuron populations that is largely specified during embryogenesis. Although interneurons expressing the neuronal isoform of nitric oxide synthase (nNOS) constitute the largest hippocampal interneuron cohort their origin and specification remain unknown. Thus, as neurogliaform cells (NGC) and Ivy cells (IvC) represent the main nNOS+interneurons, we investigated their developmental origins. Although considered distinct interneuron subtypes, NGCs and IvCs exhibited similar neurochemical and electrophysiological signatures, including NPY expression and late spiking. Moreover, lineage analyses, including loss-of-function experiments and inducible fate-mapping, indicated that nNOS+IvCs and NGCs are both derived from medial ganglionic eminence (MGE) progenitors under control of the transcription factor Nkx2-1. Surprisingly, a subset of NGCs lacking nNOS arises from caudal ganglionic eminence (CGE) progenitors. Thus, while nNOS+NGCs and IvCs arise from MGE progenitors, a CGE origin distinguishes a discrete population of nNOS−NGCs.
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Although all deep NGCs belong to the Lamp5 subclass, some are derived from the CGE and some from the MGE, as in the hippocampus.
“Our results suggest that although all deep NGCs belong to the Lamp5 subclass, some are derived from the CGE and some from the MGE, as in the hippocampus25–27.”
From Phenotypic variation of transcriptomic cell types in mouse motor cortex (2021) · cites this paper as [25]
AACs account for ~5% of MGE-derived hippocampal interneurons.
“AACs account for ~5% of MGE-derived hippocampal interneurons since AACs represent 15% of all PV interneurons (102, 1137).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1137]
Both hippocampal and neocortical AACs have origins in the medial ganglionic eminence (MGE) with specification driven by the homeodomain transcription factor Nkx2.1.
“Both hippocampal and neocortical AACs have origins in MGE with specification driven by the homeodomain transcription factor Nkx2.1 (1097, 1137, 1218).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1137]
Several primary dendrites extend from the soma then branch extensively in a stellate fashion yielding a compact somatodendritic profile reminiscent of glial cells that is typically fully contained within the NGFC's local axon cloud.
“Several primary dendrites extend from the soma then branch extensively in a stellate fashion yielding a compact somatodendritic profile reminiscent of glial cells that is typically fully contained within the NGFC’s local axon cloud (FIGURE 3D; Refs. 299, 367, 550, 578, 606, 926, 1137, 1172, 1280).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1137]
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 [1137]
In CA1 hippocampus differential expression of nNOS by NGFCs correlates to distinct embryonic origins.
“In CA1 hippocampus differential expression of nNOS by NGFCs correlates to distinct embryonic origins.”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1137]
In contrast to NGFCs, IvC somas avoid s.l.m. and are dominantly found in and around s.p. but also populate s.o. and s.r. to lesser extents.
“In contrast to NGFCs, IvC somas avoid s.l.m. and are dominantly found in and around s.p. but also populate s.o. and s.r. to lesser extents (366, 367, 1032, 1075, 1137).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1137]
IvCs are closely related to NGFCs and are estimated to be the largest cohort of hippocampal interneurons making up almost a quarter (23%, 8,800 cells) of the entire CA1 interneuron population (2.5% of all CA1 neurons).
“Ivy cells (IvCs) are closely related to NGFCs and are estimated to be the largest cohort of hippocampal interneurons making up almost a quarter (23%, 8,800 cells) of the entire CA1 interneuron population (2.5% of all CA1 neurons) (102, 366, 1137).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1137]
Hippocampal NGFCs exhibit dual MGE/CGE origins.
“hippocampal NGFCs exhibit dual MGE/CGE origins”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1137]
In the hippocampus, CGE-derived interneurons include CCK-expressing interneurons, ISIs, a subset of NGFCs, and approximately 40% of SST-expressing interneurons.
“In the hippocampus CGE-derived interneurons include CCK-expressing interneurons (CCKBCs, SCAs, ADIs, PPAs), ISIs (VIP and CR expressing), a subset of NGFCs, and ~40% of SST-expressing interneurons (e.g., O-LMs)”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1137]
In CA1 hippocampus, the vast majority of NGFCs are located within the s.l.m., where they appear to tile the entire extent of the region to cover the distal dendrites of principal cells.
“In the CA1 hippocampus, the vast majority of NGFCs are located within the s.l.m., where they appear to tile the entire extent of the region to cover the distal dendrites of principal cells (1137, 1138).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1137]
An interneuron type abundant in mouse hippocampus, the ivy cell with neurogliaform properties defined by Lamp5 and Lhx6 co-expression, expanded throughout primate neocortex.
“an interneuron type that is abundant in the mouse hippocampus–the ivy cell, which has properties similar to neurogliaform cells and is defined by co-expression of Lamp5 and Lhx636–has expanded throughout the neocortex in primates.”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [36]
Mouse hippocampal Lamp5+ Lhx6+ interneurons probably comprise the related MGE-derived ivy and neurogliaform subtypes.
“which probably comprise the closely related MGE-derived ivy and neurogliaform hippocampal subtypes36”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [36]
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- Authors
- Tricoire, L., Pelkey, K. A., Daw, M. I., Sousa, V. H., Miyoshi, G., Jeffries, B., Cauli, B., Fishell, G., & McBain, C. J.
- Affiliations
- National Institutes of Health (US)
- New York University (US)
- Centre National de la Recherche Scientifique (FR)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-02-10
- Volume
- 30
- Issue
- 6
- Pages
- 2165-2176
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2825142
- OpenAlex
- W2016662169
- Cited by
- 171
- References
- 75
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 9 · 2023: 6 · 2022: 11 · 2021: 15 · 2020: 12 · 2019: 8 · 2018: 12 · 2017: 7 · 2016: 6 · 2015: 9 · 2014: 12 · 2013: 13 · 2012: 10
- FWCI
- 5.37
- 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)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by-nc-sa)
- HAL (submittedVersion)
- Funders
- Simons Foundation
- New York State Stem Cell Science
- Centre National de la Recherche Scientifique
- National Institutes of Health
- Japan Society for the Promotion of Science
- National Institute of Mental Health (R01MH07679)
- National Institute of Neurological Disorders and Stroke (R01NS039007)
- National Institute of Child Health and Human Development
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (Z01HD001205)
- 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
- neurogliaform cells, nitric oxide synthase, hippocampal interneurons, GABAergic interneurons, medial ganglionic eminence, caudal ganglionic eminence, TTF-1, neuropeptide Y, interneuron specification
- MeSH terms
- Thyroid Nuclear Factor 1, Action Potentials, Animals, Hippocampus, Immunohistochemistry, Interneurons, Male, Mice, Transgenic, Neuropeptide Y, Nuclear Proteins, Stem Cells, Telencephalon, Transcription Factors, Vasoactive Intestinal Peptide, Cell Polarity, Patch-Clamp Techniques, Cell Lineage, Reverse Transcriptase Polymerase Chain Reaction, Mice, Nitric Oxide Synthase Type I
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