•  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. Abstract  Astroglial processes enclose ∼60% of CA1 hippocampal synapses to form the tripartite synapse. Although astrocytes express ionic channels, neurotransmitter receptors and transporters to detect neuronal activity, the nature, plasticity and impact of the currents induced by neuronal activity on short‐term synaptic plasticity remain elusive in hippocampal astrocytes. Using simultaneous electrophysiological recordings of astrocytes and neurons, we found that single stimulation of Schaffer collaterals in hippocampal slices evokes in stratum radiatum astrocytes a complex prolonged inward current synchronized to synaptic and spiking activity in CA1 pyramidal cells. The astroglial current is composed of three components sensitive to neuronal activity, i.e. a long‐lasting potassium current mediated by Kir4.1 channels, a transient glutamate transporter current and a slow residual current, partially mediated by GABA transporters and Kir4.1‐independent potassium channels. We show that all astroglial membrane currents exhibit activity‐dependent short‐term plasticity. However, only the astroglial glutamate transporter current displays neuronal‐like dynamics and plasticity. As Kir4.1 channel‐mediated potassium uptake contributes to 80% of the synaptically evoked astroglial current, we investigated in turn its impact on short‐term synaptic plasticity. Using glial conditional Kir4.1 knockout mice, we found that astroglial potassium uptake reduces synaptic responses to repetitive stimulation and post‐tetanic potentiation. These results show that astrocytes integrate synaptic activity via multiple ionic channels and transporters and contribute to short‐term plasticity in part via potassium clearance mediated by Kir4.1 channels.