Kv3 K+ channels enable burst output in rat cerebellar Purkinje cells

The ability of cells to generate an appropriate spike output depends on a balance between membrane depolarizations and the repolarizing actions of K+ currents. The high-voltage-activated Kv3 class of K+ channels repolarizes Na+ spikes to maintain high frequencies of discharge. However, little is known of the ability for these K+ channels to shape Ca2+ spike discharge or their ability to regulate Ca2+ spike-dependent burst output. Here we identify the role of Kv3 K+ channels in the regulation of Na+ and Ca2+ spike discharge, as well as burst output, using somatic and dendritic recordings in rat cerebellar Purkinje cells. Kv3 currents pharmacologically isolated in outside-out somatic membrane patches accounted for similar to 40% of the total K+ current, were very fast and high voltage activating, and required more than 1 s to fully inactivate. Kv3 currents were differentiated from other tetraethylammonium-sensitive currents to establish their role in Purkinje cells under physiological conditions with current-clamp recordings. Dual somatic-dendritic recordings indicated that Kv3 channels repolarize Na+ and Ca2+ spikes, enabling high-frequency discharge for both types of cell output. We further show that during burst output Kv3 channels act together with large-conductance Ca2+-activated K+ channels to ensure an effective coupling between Ca2+ and Na+ spike discharge by preventing Na+ spike inactivation. By contributing significantly to the repolarization of Na+ and especially Ca2+ spikes, our data reveal a novel function for Kv3 K+ channels in the maintenance of high-frequency burst output for cerebellar Purkinje cells.