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.
Highlights
Satellite oligodendrocytes (s-OLs) are closely apposed to the soma of neocortical layer 5 pyramidal neurons but their properties and functional roles remain unresolved
We find that satellite OLs (s-OLs) myelinate surrounding axons and exhibit time-locked Ba2 þ - and carbenoxolone-sensitive inward currents in response to action potential (AP) generated in the host neurons
These results suggest that s-OLs within a glial syncytium perform multiple functional and anatomical roles, spatially buffering K þ and myelinating axons within the perisomatic domain
Summary
Satellite oligodendrocytes (s-OLs) are closely apposed to the soma of neocortical layer 5 pyramidal neurons but their properties and functional roles remain unresolved. Computational modelling predicts that glial Kir constrains the perisomatic [K þ ]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 þ ]o elevations. These data suggest that s-OLs are integrated into a glial syncytium for the millisecond rapid K þ uptake limiting activity-dependent [K þ ]o increase in the perisomatic neuron domain. During repetitive high-frequency AP firing of pyramidal neurons, s-OL coupled syncytia constrain the neuronal AP generation during periods of fast accumulation of [K þ ]o These results suggest that s-OLs within a glial syncytium perform multiple functional and anatomical roles, spatially buffering K þ and myelinating axons within the perisomatic domain
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