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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.

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