Resting membrane properties of locust muscle and their modulation II. Actions of the biogenic amine octopamine.

Abstract

Ionic currents in the resting membrane of locust jumping muscle and their modulation by the biogenic amine octopamine were investigated using the two-electrode voltage clamp. A Cl- conductance, GCl,H, which slowly activates on hyperpolarization, can be induced by raising the intracellular Cl- concentration via diffusion of Cl- ions from the recording electrode. The instantaneous I-V characteristic of the current, ICl,H, is linear and reverses at the same potential as the gamma-aminobutyric acid (GABA)-mediated Cl- current. Elevation of [Cl-]i increases the maximal steady state GCl,H (Gmax) and shifts the activation curve of GCl,H to more positive potentials. Octopamine enhances GCl,H, mainly by increasing Gmax. Octopamine also lowers the resting K+ conductance (GK,r). It reduces a hyperpolarization-activated component (GK,H) of GK,r, mainly by decreasing Gmax. Octopamine also transiently stimulates the Na+/K+ pump although this effect was not always seen. The effects of octopamine on the Cl- and K+ conductances are mimicked by membrane permeant cyclic nucleotides. The modulation of GK,r, but not that of GCl,H, seems to be mediated by protein kinase A (PKA). PKA seems to be constitutively activated as indicated by the pronounced increase in GK,r induced by a PKA inhibitor, H89. The properties of GCl,H and related Cl- conductances in invertebrate and vertebrate neurons are compared. GCl,H probably supports efflux of Cl- ions accumulating in the fibers during synaptic inhibition. Octopamine's multiple modulation at the level of the muscle cell membrane, in conjunction with previously established effects on synaptic transmission and excitation-contraction coupling, are suited to support strong and rapid muscle contractions.