Potassium currents and membrane excitability of neurons in the rat's dorsal nucleus of the lateral lemniscus

1. The contribution of voltage-activated outward potassium currents to membrane excitability of neurons in the rat's dorsal nucleus of the lateral lemniscus (DNLL) was studied in a brain slice preparation using whole cell patch-clamp and intracellular recordings. Voltage-clamp methods and pharmacological manipulations were used to examine the currents regulating membrane dynamics in DNLL. 2. A delayed sustained outward current was evoked by applying depolarizing voltage steps across the cell membrane from a holding potential of -50 mV. An additional transient outward current was evoked when the depolarizing steps were preceded by a hyperpolarizing prepulse of -110 or -120 mV. 3. The transient outward current peaked within 6.8 ms of the onset of a depolarizing pulse. It decayed with a time constant of 12.3 ms for a 60-mV depolarizing voltage shift. Half-inactivation of this current occurred at -81.3 mV. The time constant for removal of the inactivation was 17.4 ms. The transient current had a high sensitivity to 4-aminopyridine (4-AP). 4. The sustained current was activated more slowly and was more sensitive to tetraethylammonium (TEA) than the transient current. The sustained current had both Ca2+-dependent and Ca2+-independent components. The Ca2+-dependent portion emerged at potentials of about -35 mV and was activated fully at +10 mV. The Ca2+-independent component was activated at potentials more positive than -40 mV and increased in magnitude with further depolarization. Inactivation of the Ca2+-independent component was voltage dependent. 5. The transient current in DNLL neurons closely resembled the A current (I-A) described for hippocampal and other neurons in both kinetics and pharmacology. The Ca2+-independent component of the sustained current resembled the K current (I-K) described for other neurons in both its properties of activation and inactivation and its pharmacology. 6. The outward current of some DNLL neurons was found to contain a dendrotoxin-sensitive component. This component reached its peak at 6.8 ms and had voltage-sensitive time constants of decay of 25.5 and 8.5 ms with voltage steps of 40 and 60 mV, respectively. 7. Application of 4-AP and TEA markedly prolonged the spike width, abolished the fast component of the afterhyperpolarization and depolarized the cell membrane. Also, the number of action potentials produced by positive current injection increased under the influence of 4-AP and TEA. Membrane excitability and spike repolarization were dependent on both 4-AP-sensitive transient and TEA-sensitive sustained currents. 8. Neurons in DNLL typically exhibit a steady discharge of action potentials in response to sustained membrane depolarization. The rate and temporal pattern of production of action potentials in these cells are determined by the combination of transient and sustained potassium channels.