Single voltage-gated K+ channels and their functions in small dorsal root ganglion neurones of rat.

Abstract

1. Single voltage-activated K+ channels were investigated by means of the patch-clamp technique in small dorsal root ganglion (DRG) neurones in 150 microns thin slices of new-born rat DRG. It was found that K+ conductance in small DRG neurones is formed by one type of fast inactivating A-channel and four types of delayed rectifier K+ channels, which could be separated on the basis of their single-channel conductance, kinetics and sensitivity to external tetraethylammonium (TEA). 2. Potassium A-channels were observed at relatively moderate density. They were weakly sensitive to TEA and activated between -70 and +20 mV. The conductance of A-channels was about 40 pS for inward currents in symmetrical high-K+ solutions with external 5 mM TEA added to suppress other types of K+ channels. The time constant of channel inactivation (tau in) was 18.8 ms at -70 mV and 6 ms at potentials positive to -20 mV. 3. A fast delayed rectifier (DRF) channel with a conductance of 55 pS in symmetrical high-K+ solutions was the most frequent type of K+ channel. The channel activated in a broad potential range between -50 and +60 mV and demonstrated a fast deactivation within 1-3 ms after potential return to -80 mV in high-Ko+ solution. The tau in value was 90-150 ms at positive membrane potentials. The single-channel current amplitudes were blocked to 55% by 1 mM TEA. 4. Three further types of delayed rectifier K+ channels were called DR1-, DR2- and DR3- channels. Their single-channel conductances for inward currents in symmetrical high-K+ solutions were distributed between 30 and 44 pS. The channels activated in almost the same voltage range between -60 and -10 mV. Deactivation of the channels at -80 mV lasted tens of milliseconds. The channels were separated on the basis of their sensitivities to TEA. DR1-channel currents were reduced to 50% in the presence of 1 mM TEA, DR2-channel currents were reduced to about 50% by 5 mM TEA, whereas the amplitudes of currents through DR3-channels were almost unaffected by 5 mM TEA. 5. Addition of external 1 and 5 mM TEA to whole cells under current-clamp condition depolarized the cell membrane, lowered the threshold for action potential firing, prolonged action potential duration and reduced the amplitude of after-hyperpolarization. 6. It is concluded that potassium A-, DRF-, DR1-, DR2- and DR3-channels play multiple roles in the excitability of DRG neurones. Possible influences of these channels on the shape of the action potential, its firing threshold and the resting membrane potential of small DRG neurones are discussed.