Functional and ionic properties of a slow afterhyperpolarization in ferret perigeniculate neurons in vitro

Intracellular recordings from spontaneously spindling GABAergic neurons of the ferret perigeniculate nucleus in vitro revealed a fast afterhyperpolarization after each action potential, a medium-duration afterhyperpolarization after each low-threshold Ca2+ spike, and a slow afterhyperpolarization after the cessation of spindle waves. The slow afterhyperpolarization was associated with an increase in membrane conductance, and the reversal potential was sensitive to extracellular [K+]o, indicating that it is mediated at least in part by the activation of a K+ conductance. However, the block of Ca2+ channels did not block the slow afterhyperpolarization, whereas the block of Na+ channels did block this event, even after the generation of repetitive Ca2+ spikes, indicating that it is mediated by a Na+-activated K+ current. Application of apamin reduced the afterhyperpolarization and enhanced a plateau potential after each low-threshold Ca2+ spike. This plateau potential could result in a prolonged depolarization of perigeniculate neurons, even before the application of apamin, resulting in the generation of tonic discharge. The plateau potential was blocked by the local application of tetrodotoxin, indicating that it is mediated by a persistent Na+ current. The activation and interaction of these slowly developing and persistent currents contributes significantly to low-frequency components of spindle wave generation. In particular, we suggest that the activation of the slow afterhyperpolarization may contribute to the generation of the spindle wave refractory period in vitro.