Neural circuits are composed of diverse cell types, the firing properties of which reflect their intrinsic ionic currents. GABAergic and non-GABAergic neurons in the medial vestibular nuclei, identified in GIN and YFP-16 lines of transgenic mice, respectively, exhibit different firing properties in brain slices. The intrinsic ionic currents of these cell types were investigated in acutely dissociated neurons from 3- to 4-wk-old mice, where differences in spontaneous firing and action potential parameters observed in slice preparations are preserved. Both GIN and YFP-16 neurons express a combination of four major outward currents: Ca(2+)-dependent K(+) currents (I(KCa)), 1 mM TEA-sensitive delayed rectifier K(+) currents (I(1TEA)), 10 mM TEA-sensitive delayed rectifier K(+) currents (I(10TEA)), and A-type K(+) currents (I(A)). The balance of these currents varied across cells, with GIN neurons tending to express proportionately more I(KCa) and I(A), and YFP-16 neurons tending to express proportionately more I(1TEA) and I(10TEA). Correlations in charge densities suggested that several currents were coregulated. Variations in the kinetics and density of I(1TEA) could account for differences in repolarization rates observed both within and between cell types. These data indicate that diversity in the firing properties of GABAergic and non-GABAergic vestibular nucleus neurons arises from graded differences in the balance and kinetics of ionic currents.