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Cited by 110Neuroscience and Neuropharmacology ResearchIon channel regulation and functionNeural dynamics and brain function

Myelinating satellite oligodendrocytes are integrated in a glial syncytium constraining neuronal high-frequency activity

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Battefeld, Arne, Klooster, Jan, Kole, Maarten H. P.·2016·Nature Communications
DOI 10.1038/ncomms11298PMC PMC4866043
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Abstract

Satellite oligodendrocytes (s-OLs) are closely apposed to the soma of neocortical layer 5 pyramidal neurons but their properties and functional roles remain unresolved. Here we show that s-OLs form compact myelin and action potentials of the host neuron evoke precisely timed Ba 2+-sensitive K+ inward rectifying (Kir) currents in the s-OL. Unexpectedly, the glial K+ inward current does not require oligodendrocytic Kir4.1. Action potential-evoked Kir currents are in part mediated by gap–junction coupling with neighbouring OLs and astrocytes that form a syncytium around the pyramidal cell body. Computational modelling predicts that glial Kir constrains the perisomatic [K+]o increase most importantly during high-frequency action potentials. Consistent with these predictions neurons with s-OLs showed a reduced probability for action potential burst firing during [K+]o elevations. These data suggest that s-OLs are integrated into a glial syncytium for the millisecond rapid K+ uptake limiting activity-dependent [K+]o increase in the perisomatic neuron domain.

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  • Data from the cuprizone mouse model and in vivo imaging suggest that satellite oligodendrocytes can generate compact myelin around pyramidal neurons of mouse layer V.

    “data from the cuprizone mouse model and in vivo imaging suggests that these cells can generate compact myelin around pyramidal neurons of mouse layer V.54,55”

    From BCAS1-positive oligodendrocytes enable efficient cortical remyelination in multiple sclerosis (2025) · cites this paper as [54]

    The Results section (“Identified layer 5 s-OLs myelinate axons”; page not provided) reports that satellite oligodendrocytes beside layer 5 pyramidal neurons form compact myelin around axons. It does not report cuprizone-model data or in vivo imaging; its live imaging was performed during recordings in brain slices. The paper also says these cells did not myelinate the first internode of their host neuron. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Satellite oligodendrocytes are largely considered non-myelinating and may fulfil specific functions in neuronal support.

    “Satellite oligodendrocytes are largely considered non-myelinating and may fulfil specific functions in neuronal support.51-54”

    From BCAS1-positive oligodendrocytes enable efficient cortical remyelination in multiple sclerosis (2025) · cites this paper as [54]

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Cited by

Sorted by citations

Authors
Battefeld, A., Klooster, J., & Kole, M. H. P.
Affiliations
Netherlands Institute for Neuroscience (NL)
Corresponding author
Kole, Maarten H. P.
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2016-05-10
Volume
7
Issue
1
Pages
11298-11298
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/ncomms11298
PMC
PMC4866043
OpenAlex
W2414699956
Cited by
110
References
6
Citations by year
2026: 9 · 2025: 8 · 2024: 10 · 2023: 7 · 2022: 10 · 2021: 16 · 2020: 13 · 2019: 16 · 2018: 11 · 2017: 8 · 2016: 1
FWCI
6.75
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, other-oa)
  • KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
  • RePEc: Research Papers in Economics (submittedVersion, cc-by)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
Funders
  • Hersenstichting
  • FP7 Ideas: European Research Council (261114)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
inward rectifier potassium current, Kir4.1, electrical coupling, astrocytes, extracellular potassium, action potential bursts, layer 5 pyramidal neurons, myelination, neocortex, computational modelling
MeSH terms
Kcnj10 Channel, Action Potentials, Algorithms, Animals, Mice, Inbred C57BL, Mice, Transgenic, Microscopy, Electron, Models, Neurological, Myelin Sheath, Neurons, Oligodendroglia, Potassium, Giant Cells, Mice, Knockout, Patch-Clamp Techniques, Potassium Channels, Inwardly Rectifying

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