Persistent enhancement of neuron-glia signaling mediated by increased extracellular K+ accompanying long-term synaptic potentiation.

Neuron-glia signaling is important for neural development and functions. This signaling may be regulated by neuronal activity and undergo modification similar to long-term potentiation (LTP) of neuronal synapses, a hallmark of neuronal plasticity. We found that tetanic stimulation of Schaffer collaterals (Sc) in the hippocampus that induced LTP in neurons also resulted in LTP-like persistent elevation of Sc-evoked slow depolarization in perisynaptic astrocytes. The elevated slow depolarization in astrocytes was abolished by NMDA receptor antagonist and K(+) channel inhibitors, but not by Ca(2+) chelator BAPTA loaded in the recorded astrocytes, suggesting involvement of an increased extracellular K(+) accumulation accompanying LTP of neuronal synapses. The increased K(+) accumulation and astrocyte depolarization after LTP induction may reduce the efficiency of glial glutamate transporters, which may contribute to the enhanced synaptic efficacy. The neuronal activity-induced persistent enhancement of neuron-glia signaling may thus have important physiological relevance.