In the dentate gyrus (DG), granule cells (GCs) and local interneurons transform dense cortical neuron ensemble theta/gamma band activity into sparse DG output to generate contextual representations. GABAB receptor-mediated inhibition contributes to sparse DG activity, but it is unclear how it contributes to frequency-dependent synaptic integration and spike output. We recorded perforant-path excitatory postsynaptic potentials from GCs in ventral horizontal slices from adult male and female mice and found GABAB-receptor dependent inhibition of action potential firing during gamma frequency trains. Consecutive trains generated a long-lasting inhibition that prevents repetitive action potential generation in GCs. We recently identified neuronal nitric oxide synthase-expressing (nNos) interneurons, a subpopulation of neurogliaform interneurons, as the primary source of GABAB-mediated inhibition. We thus compared frequency-dependent synaptic recruitment nNos interneurons with parvalbumin-expressing (PV) interneurons that generate exclusively GABAA mediated inhibition. Interestingly, whereas PV followed both theta and gamma frequencies throughout the entire train, nNos sparsely fired during theta stimulations and synchronized their firing at the onset of gamma trains while remaining silent at the end of the train. We used expression of channelrhodopsin-2 to mimic gamma-induced nNos interneuron synchronization. nNos interneuron population ensemble firing led to a long-lasting inhibition that was not evident during theta stimulation. In addition, we found that this long-lasting inhibition was shortened by mu-opioid receptor agonist, due to suppression of GABA release. These results suggest that gamma frequency synchronization can generate long-lasting GABAB-mediated inhibition that underlies network switching by neurogliaform interneurons and is under regulation by opioids.