Cited by 163Connexins and lens biologyNeural dynamics and brain functionNeuroscience and Neuropharmacology Research

Gap-Junctional Coupling between Neurogliaform Cells and Various Interneuron Types in the Neocortex

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Simon, Anna, Oláh, Szabolcs, Molnár, Gábor, Szabadics, János, Tamás, Gábor·2005·The Journal of Neuroscience

Abstract

Electrical synapses contribute to the generation of synchronous activity in neuronal networks. Several types of cortical GABAergic neurons acting via postsynaptic GABA(A) receptors also form electrical synapses with interneurons of the same class, suggesting that synchronization through gap junctions could be limited to homogenous interneuron populations. Neurogliaform cells elicit combined GABA(A) and GABA(B) receptor-mediated postsynaptic responses in cortical pyramidal cells, but it is not clear whether neurogliaform cells are involved in networks linked by electrical coupling. We recorded from pairs, triplets, and quadruplets of cortical neurons in layers 2 and 3 of rat somatosensory cortex (postnatal day 20-35). Neurogliaform cells eliciting slow IPSPs on pyramidal cells also triggered divergent electrical coupling potentials on interneurons. Neurogliaform cells were electrically coupled to other neurogliaform cells, basket cells, regular-spiking nonpyramidal cells, to an axoaxonic cell, and to various unclassified interneurons showing diverse firing patterns and morphology. Electrical interactions were mediated by one or two electron microscopically verified gap junctions linking the somatodendritic domain of the coupled cells. Our results suggest that neurogliaform cells have a unique position in the cortical circuit. Apart from eliciting combined GABA(A) and GABA(B) receptor-mediated inhibition on pyramidal cells, neurogliaform cells establish electrical synapses and link multiple networks formed by gap junctions restricted to a particular class of interneuron. Widespread electrical connections might enable neurogliaform cells to monitor the activity of different interneurons acting on GABA(A) receptors at various regions of target cells.

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Crossref · 10.1523/jneurosci.1431-05.2005

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  • While neocortical NGFCs can be found throughout all layers, they are particularly enriched in supragranular layers and form a major constituent cell population in L1.

    “While neocortical NGFCs can be found throughout all layers, they are particularly enriched in supragranular layers and form a major constituent cell population in L1 (564, 858, 1017, 1074, 1086, 1134).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1017]

  • 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 [1017]

  • NGFCs of layer 2/3 (but not layer 1) of rat somatosensory cortex are highly interconnected via electrical synapses and also make widespread electrical synapses with PVBCs, regular spiking nonpyramidal cells, AACs as well as many other unidentified interneuron cell types.

    “One interesting deviation from this canonical rule are NGFCs of layer 2/3 (but not layer 1) (206) of rat somatosensory cortex. Although these cells were highly interconnected via electrical synapses, they also made widespread electrical synapses with PVBCs, regular spiking nonpyramidal cells, AACs as well as many other unidentified interneuron cell types (1017).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1017]

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Authors
Simon, A., Oláh, S., Molnár, G., Szabadics, J., & Tamás, G.
Affiliations
University of Szeged (HU)
Venue
The Journal of Neuroscience
Published
2005-07-06
Volume
25
Issue
27
Pages
6278-6285
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2085107866
Cited by
163
References
51
Citations by year
2026: 3 · 2025: 4 · 2024: 4 · 2023: 5 · 2022: 1 · 2021: 5 · 2020: 6 · 2019: 3 · 2018: 4 · 2017: 12 · 2016: 8 · 2015: 7 · 2014: 9 · 2013: 7 · 2012: 8
FWCI
4.03
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Newcastle University ePrints (Newcastle Univesity)
Funders
  • Wellcome Trust
  • Boehringer Ingelheim Fonds
  • National Institutes of Health (NS35915)
  • National Institute of Neurological Disorders and Stroke (R29NS035915, R01NS035915, NS-35915, R37NS035915)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
neurogliaform cells, electrical coupling, electrical synapses, cortical interneurons, basket cells, GABAA receptor, GABAB receptors, somatosensory cortex, cortical pyramidal neurons, inhibitory interneurons, neuronal synchronization, interneuron networks
MeSH terms
Action Potentials, Animals, Cell Communication, Evoked Potentials, Interneurons, Neuroglia, Receptors, GABA-A, Somatosensory Cortex, Rats, Wistar, Gap Junctions, Pyramidal Cells, Receptors, GABA-B, Neocortex, Rats

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