The myelin sheath produced by oligodendrocytes ensures high velocity action potential conduction along CNS axons. Besides the white matter a great number of oligodendrocytes can be found in the neocortical grey matter where a population of oligodendrocytes is in close anatomical proximity to the soma of pyramidal neurons. These satellite oligodendrocytes are thought to be non-myelinating in nature and provide metabolic support for neurons, but their functional physiological properties remain unknown. In this study we examined the intrinsic properties of satellite oligodendrocytes and investigated to which extent there might be functional coupling with neurons. Adult male and female mice (22.8±0.5 g) were anaesthetised with isoflurane (3% v/v) and subsequently decapitated. Neocortical acute brain slices were prepared using standard methods and we subsequently performed simultaneous whole-cell recordings from neocortical layer 5 neurons and identified satellite oligodendrocytes. All results are mean ± SEM. Satellite oligodendrocytes were resting at −85.9±0.6 mV (n=101), had a low membrane resistance (13.4±1.9 MΩ, n=63) and were characterized by a linear current-voltage relationship in the steady state. Live confocal images revealed that satellite oligodendrocytes (n=31) had on average 32±2 myelinating internodal processes that were oriented in all angles. Action potentials generated in pyramidal neurons evoked in adjacent voltage-clamped oligodendrocytes temporally correlated inward currents (n=20). These currents were highly sensitive to 0.1 mM barium application (81±2.5% block, n=4, paired t-test, p=0.01) and were also reduced by carbenoxolone (58±4%, n=4). Subsequently, immunohistochemistry labelling indicated that the soma of satellite oligodendrocytes expressed Kir4.1 channels (n=3), a member of the barium-sensitive inward rectifying potassium channel family that is implicated in K+ buffering. Consistent with the presence of these channels, fast application of 1-30 mM [K+] revealed that the Kir4.1 mediated currents were highly sensitive to [K+]o and reversed at 3 mM [K+]o at a voltage of -85.4±1.1 mV (n=6). Furthermore, dual whole-cell recordings revealed that satellite oligodendrocytes are reciprocally gap junction coupled to astrocytes in a distance dependent manner (coupling ratio 2.3±0.7%, n=5). Lastly, Ca2+ imaging of satellite oligodendrocytes displayed no Ca2+ change in the cell body (p=0.7) in response to action potentials. In summary our data suggest that satellite oligodendrocytes in conjunction with neighbouring astrocytes co-regulate the [K+]o homeostasis near the somatic and proximal axon initial segment domains of pyramidal neurons via Kir4.1 channels and a gap-junction coupled microcircuit. [K+]o flux is thus efficiently siphoned at the temporal resolution of single action potentials.