Two calcium-activated potassium conductances in a subpopulation of coeliac neurones of guinea-pig and rabbit

Abstract

1. Some of the sympathetic neurones in coeliac ganglia isolated from young guinea-pigs and rabbits were found to generate action potentials followed by after-hyperpolarizations with durations of 3-8 s, much longer than those (congruent to 300-500 ms) observed in the majority of other mammalian sympathetic neurones. 2. This type of ganglion cell discharged only once at the onset of a depolarizing step unless a very high intensity current was applied. Passive and voltage-dependent membrane conductances studied in detail in guinea-pig ganglia differed from those in the two other classes of sympathetic ganglion cell described previously (Cassell, Clark & McLachlan, 1986). 3. By using a single microelectrode to voltage clamp the soma, it was possible to demonstrate that both fast and slow components of the tail current following initiation of an uncontrolled 'action current' in neurones with long after-hyperpolarizations (l.a.h.) were carried by K+ ions, as was the fast tail current (time constant, tau congruent to 130 ms) present in other coeliac neurones. 4. The amplitude of both components of the tail current in l.a.h. neurones was markedly reduced by the replacement of Ca2+ by Mn2+, Co2+ or Ba2+ ions. These manoeuvres had similar effects on the fast tail current in other coeliac neurones. 5. Both time course and amplitude of the fast tail current were increased when Ca2+ concentration was raised, or when several 'action currents' were initiated, whereas only the amplitude of the slow tail current was affected. 6. The time course of the slow tail current could be described by the sum of two exponentials with tau on = 285 ms and tau off = 1.3 s at 35 degrees C occurring after a delay of 60 ms. This current had a Q10 of about 4 between 35 and 25 degrees C. In contrast, the Q10 of the fast component was about 2. 7. Morphine (10(-6) M) and vasoactive intestinal polypeptide (10(-6) M) had no effect on the outward tail current in l.a.h. neurones, but 5-hydroxytryptamine (10(-6) M) was found to abolish the slow component without affecting the fast component. 8. The slow tail current was activated in the subthreshold range of membrane potentials, and its properties could account for the firing characteristics of this subpopulation of sympathetic neurones. 9. The two calcium-activated potassium conductances that are responsible for the prolonged after-hyperpolarization resemble those in a subpopulation of nodose ganglion cells with unmyelinated axons (Fowler, Greene & Weinreich, 1985).(ABSTRACT TRUNCATED AT 400 WORDS)