Microglial surveillance is a key feature of brain physiology and disease. Here, we found that G_i-dependent microglial dynamics prevent neuronal network hyperexcitability. By generating Mg^PTX mice to genetically inhibit G_i in microglia, we show that sustained reduction of microglia brain surveillance and directed process motility induced spontaneous seizures and increased hypersynchrony after physiologically evoked neuronal activity in awake adult mice. Thus, G_i-dependent microglia dynamics may prevent hyperexcitability in neurological diseases.