ATP-sensitive potassium channels (K_ATP channels) are important sensors of cellular metabolic state that link metabolism and excitability in neuroendocrine cells, but their role in nonglucosensing central neurons is less well understood. To examine a possible role for K_ATP channels in modulating excitability in hippocampal circuits, we recorded the activity of single K_ATP channels in cell-attached patches of granule cells in the mouse dentate gyrus during bursts of action potentials generated by antidromic stimulation of the mossy fibers. Ensemble averages of the open probability (p_open) of single K_ATP channels over repeated trials of stimulated spike activity showed a transient increase in p_open in response to action potential firing. Channel currents were identified as K_ATP channels through blockade with glibenclamide and by comparison with recordings from Kir6.2 knock-out mice. The transient elevation in K_ATP p_open may arise from submembrane ATP depletion by the Na⁺-K⁺ ATPase, as the pump blocker strophanthidin reduced the magnitude of the elevation. Both the steady-state and stimulus-elevated p_open of the recorded channels were higher in the presence of the ketone body R-β-hydroxybutyrate, consistent with earlier findings that ketone bodies can affect K_ATP activity. Using perforated-patch recording, we also found that K_ATP channels contribute to the slow afterhyperpolarization following an evoked burst of action potentials. We propose that activity-dependent opening of K_ATP channels may help granule cells act as a seizure gate in the hippocampus and that ketone-body-mediated augmentation of the activity-dependent opening could in part explain the effect of the ketogenic diet in reducing epileptic seizures.