The olfactory bulb, a second-order sensory brain region, relays afferent input from olfactory receptor neurons to piriform cortex. While large inhibitory postsynaptic potentials (IPSPs) are evident in in vivo intracellular recordings, the functional significance of these synaptic responses has not been defined. In many brain regions, IPSPs can function to either inhibit spiking by transiently suppressing activity or can evoke spiking directly by triggering rebound discharges. We used whole cell patch clamp recordings from mitral cells in olfactory bulb slices to investigate the mechanisms by which IPSPs regulate mitral cell spike discharges. Mitral cells have unusual intrinsic membrane properties that support rebound spike generation in response to small amplitude (3-5 mV) but not large amplitude hyperpolarizing current injections or IPSPs. Rebound spiking occurred in mitral cells was dependent on recovery of subthreshold subthreshold Na currents, and could be blocked by tetrodotoxin (TTX, 1 µM) or the subthreshold Na channel blocker riluzole (10 µM). Surprisingly, larger amplitude hyperpolarizing stimuli impeded spike generation by recruiting a transient outward IA-like current that was sensitive to high concentrations of 4-aminopyridine (4-AP) and Ba. The interplay of voltage gated Na channels and transient outward current produces a narrow range of IPSP amplitudes that generate rebound spikes. We also found that subthreshold Na channels boost subthreshold excitatory stimuli to voltage ranges where granule cell mediated IPSPs can produce rebound spikes. These results demonstrate how the intrinsic membrane properties of mitral cells enables inhibitory inputs to bidirectionally control spike output from the olfactory bulb.