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

Arne Battefeld, Jan Klooster and Maarten H. P. Kole ()
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Arne Battefeld: Axonal Signalling Group, Netherlands Institute for Neuroscience, Royal Academy of Arts and Sciences
Jan Klooster: Axonal Signalling Group, Netherlands Institute for Neuroscience, Royal Academy of Arts and Sciences
Maarten H. P. Kole: Axonal Signalling Group, Netherlands Institute for Neuroscience, Royal Academy of Arts and Sciences

Nature Communications, 2016, vol. 7, issue 1, 1-13

Abstract: 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 Ba2+-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.

Date: 2016
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DOI: 10.1038/ncomms11298

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