Astroglial potassium clearance contributes to short‐term plasticity of synaptically evoked currents at the tripartite synapse

•  Astrocytes, active players in neurotransmission, display complex membrane ionic responses upon neuronal activity. •  However, the nature, plasticity and role of the activity‐dependent astroglial currents on synaptic plasticity remain unclear in the hippocampus. •  We here demonstrate, using simultaneous electrophysiological recordings of hippocampal neurons and astrocytes, that the complex astroglial current induced synaptically is dominated (80%) by potassium entry through Kir4.1 channels and also includes, in addition to the glutamate transporter current, a small residual current, partially mediated by GABA transporters and Kir4.1‐independent potassium channels. •  These synaptically evoked astroglial currents exhibit differential short‐term plasticity patterns, and astroglial potassium uptake mediated by Kir4.1 channels down‐regulates hippocampal short‐term plasticity. •  This study establishes astrocytes as integrators of excitatory and inhibitory synaptic activity, which may, through dynamic potassium handling, define the signal‐to‐noise ratio essential for specific strengthening of synaptic contacts and synchronization of neuronal ensembles, a prerequisite for learning and memory.

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