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Opposing Inward and Outward Conductances Regulate Rebound Discharges in Olfactory Mitral Cells

Department of Neurosciences, Case Western Reserve University, Cleveland, Ohio

Submitted 19 October 2006; accepted in final form 15 November 2006

The olfactory bulb, a second-order sensory brain region, relays afferent input from olfactory receptor neurons to piriform cortex and other higher brain centers. Although large inhibitory postsynaptic potentials (IPSPs) are evident in in vivo intracellular recordings from mitral cells, 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 occurring in mitral cells was dependent on recovery of 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 I_A-like current that was sensitive to high concentrations of 4-aminopyridine and Ba. The interplay of voltage-gated subthreshold Na channels and transient outward current produces a narrow range of IPSP amplitudes that generates rebound spikes. We also found that subthreshold Na channels boost subthreshold excitatory stimuli to produce membrane voltages where granule-cell-mediated IPSPs can produce rebound spikes. These results demonstrate how the intrinsic membrane properties of mitral cells enable inhibitory inputs to bidirectionally control spike output from the olfactory bulb.

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