Multiple Serotonin-Activated Currents in Isolated, Neuronal Somata from Locust Thoracic Ganglia

Abstract

Three different responses were evoked by pressure micro-application of serotonin onto freshly dissociated, current- and voltage-clamped neuronal somata from the thoracic ganglia of the locust Locusta migratoria. In some neurones, an inward current, I(5HT)K, resulting from a decrease in potassium conductance, with slow kinetics and maximum activation at membrane potentials of –60 to –70 mV, was evoked by serotonin and by the 5-HT3 agonist 2-methyl serotonin. This current was completely abolished by either 10 mmol l-1 caesium or 5 mmol I-1 rubidium and partially blocked by 50mmoll-1 tetraethylammonium or 5 mmol l-1 4-aminopyridine. The response was antagonised by the 5-HT2-specific compounds, ketanserin and ritanserin. In other somata, serotonin, 2-methyl serotonin and the 5-HT3 antagonist ICS 205 930 evoked a second current, I(5HT)Na, which was due to an increase in sodium permeability and had slow kinetics similar to that of I(5HT)K. This current was inward over the membrane potential range –30 to –80 mV and increased with hyperpolarisation. The response was blocked by sodium-free saline and the 5-HT3 receptor antagonist MDL 72222. In other neurones, at membrane potentials more positive than –50 mV, serotonin pulses could activate a third current, I(5HT)X, which increased with depolarisation of the membrane potential and had comparatively fast kinetics. Activation of the current was accompanied by a decrease in membrane conductance. This response was completely blocked by 4-aminopyridine and weakly inhibited by both caesium and tetraethylammonium and is, therefore, probably a potassium current. The three currents described here differ in their pharmacology, their ionic mechanisms and their dependence on membrane potential from the serotonin-activated currents reported for vertebrates and they provide evidence for the mechanism of action of serotonin as a neurotransmitter in insects.