Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area
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We studied neurogliaform neurons in the stratum lacunosum moleculare of the CA1 hippocampal area. These interneurons have short stellate dendrites and an extensive axonal arbor mainly located in the stratum lacunosum moleculare. Single-cell reverse transcription-PCR showed that these neurons were GABAergic and that the majority expressed mRNA for neuropeptide Y. Most neurogliaform neurons tested were immunoreactive for alpha-actinin-2, and many stratum lacunosum moleculare interneurons coexpressed alpha-actinin-2 and neuropeptide Y. Neurogliaform neurons received monosynaptic, DNQX-sensitive excitatory input from the perforant path, and 40 Hz stimulation of this input evoked EPSCs displaying either depression or initial facilitation, followed by depression. Paired recordings performed between neurogliaform neurons showed that 85% of pairs were electrically connected and 70% were also connected via GABAergic synapses. Injection of sine waveforms into neurons during paired recordings resulted in transmission of the waveforms through the electrical synapse. Unitary IPSCs recorded from neurogliaform pairs readily fatigued, had a slow decay, and had a strong depression of the synaptic response at a 5 Hz stimulation frequency that was antagonized by the GABA(B) antagonist (2S)-3-[[(1S)-1-(3,4-dichlorophenyl)ethyl]amino-2-hydroxypropyl](phenylmethyl) phosphinic acid (CGP55845). The amplitude of the first IPSC during the 5 Hz stimulation was also increased by CGP55845, suggesting a tonic inhibition of synaptic transmission. A small unitary GABA(B)-mediated IPSC could also be detected, providing the first evidence for such a component between GABAergic interneurons. Electron microscopic localization of the GABA(B1) subunit at neurogliaform synapses revealed the protein in both presynaptic and postsynaptic membranes. Our data disclose a novel interneuronal network well suited for modulating the flow of information between the entorhinal cortex and CA1 hippocampus.
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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 [926]
NGFC dendrites and axons can also cross the hippocampal fissure into the molecular layer of the dentate gyrus and penetrate into superficial s.r., indicating that CA1 NGFC recruitment and distribution of inhibition extend beyond s.l.m.
“However, NGFC dendrites and axons can also cross the hippocampal fissure into the molecular layer of the dentate gyrus and penetrate into superficial s.r., indicating that CA1 NGFC recruitment and distribution of inhibition extend beyond s.l.m. (367, 550, 926, 927).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [926]
These features combined with the dense local ramification of NGFC axons are considered to underlie the ability of NGFCs to mediate volume transmission leading to slow dual component (GABAAR- and GABABR-mediated) inhibition at virtually any postsynaptic element within their dense axonal plexus.
“These features combined with the dense local ramification of NGFC axons are considered to underlie the ability of NGFCs to mediate volume transmission leading to slow dual component (GABAAR- and GABABR-mediated) inhibition at virtually any postsynaptic element within their dense axonal plexus (550, 926, 927, 1074, 1086).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [926]
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 [926]
The cloud of GABA generated from NGFC release can also activate presynaptic GABABR to mediate homosynaptic and heterosynaptic depression of GABAergic and glutamatergic release sometimes with remarkable target cell specificity.
“In addition, the cloud of GABA generated from NGFC release can also activate presynaptic GABABR to mediate homosynaptic and heterosynaptic depression of GABAergic and glutamatergic release (48, 858, 859, 926, 927) sometimes with remarkable target cell specificity (204).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [926]
NGFCs exhibit a remarkably high degree of chemical and electrical connectivity with each other and promiscuously with additional non-NGFC interneuron subtypes allowing individual NGFCs to extend their influence well beyond their local dense axonal cloud through disinhibition and coordination of inhibitory networks.
“Interestingly, NGFCs exhibit a remarkably high degree of chemical and electrical connectivity with each other and promiscuously with additional non-NGFC interneuron subtypes allowing individual NGFCs to extend their influence well beyond their local dense axonal cloud through disinhibition and coordination of inhibitory networks (926, 1017, 1280, 1281).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [926]
In CA1 and dentate gyrus, NGFCs/IvCs have been shown to mediate GABAA,slow on unidentified s.l.m. and molecular layer interneurons, respectively.
“although in CA1 and dentate gyrus they have been shown to mediate GABAA,slow on unidentified s.l.m. and molecular layer interneurons, respectively (48, 926).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [926]
Electrophysiological recordings from pairs of NGFCs demonstrate a marked functional connectivity with each other.
“Electrophysiological recordings from pairs of NGFCs demonstrate a marked functional connectivity with each other (48, 550, 926, 1074).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [926]
Neurogliaform cells evoked mixed GABAA,B postsynaptic events, whereas the model ivy cells only triggered GABAA IPSPs.
“These two model interneuron groups mainly differed in that the neurogliaform cells evoked mixed GABAA,B postsynaptic events (Price et al., 2005), whereas the model ivy cells only triggered GABAA IPSPs (in agreement with a lack of evidence for ivy cell-evoked GABAB IPSPs).”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Price et al., 2005
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“However, NGFCs are the only INs that have been shown so far to elicit robust unitary GABAB responses in response to a single AP (Tamás et al., 2003; Price et al., 2005, 2008; Wozny and Williams, 2011).”
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GABAB Receptor Modulation of Feedforward Inhibition through Hippocampal Neurogliaform Cells
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Neurogliaform and Ivy Cells: A Major Family of nNOS Expressing GABAergic Neurons
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Digital PCR to Determine the number of Transcripts from Single Neurons after Patch-Clamp Recording
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- Authors
- Price, C. J., Cauli, B., Kovacs, E. R., Kulik, A., Lambolez, B., Shigemoto, R., & Capogna, M.
- Affiliations
- University of Oxford (GB)
- Centre National de la Recherche Scientifique (FR)
- Japan Science and Technology Agency (JP)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2005-07-20
- Volume
- 25
- Issue
- 29
- Pages
- 6775-6786
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6725364
- OpenAlex
- W2001809841
- Cited by
- 255
- References
- 62
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 12 · 2023: 10 · 2022: 7 · 2021: 10 · 2020: 8 · 2019: 13 · 2018: 13 · 2017: 5 · 2016: 10 · 2015: 11 · 2014: 13 · 2013: 8 · 2012: 13
- FWCI
- 3.98
- 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)
- HAL (submittedVersion)
- FreiDok plus (Universitätsbibliothek Freiburg) (submittedVersion)
- Funders
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- hippocampal CA1, inhibitory interneurons, GABAergic synapses, GABAB receptors, ACTN2, neuropeptide Y, electrical synapses, perforant path, stratum lacunosum-moleculare, synaptic depression, entorhinal cortex
- MeSH terms
- Animals, Axons, Dendrites, Electric Stimulation, Hippocampus, Interneurons, Nerve Net, Neural Inhibition, Neuronal Plasticity, Organ Culture Techniques, Biomarkers, Polymerase Chain Reaction, Rats, Sprague-Dawley, Receptors, GABA-B, Patch-Clamp Techniques, Entorhinal Cortex, Perforant Pathway, Rats
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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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