Resting Membrane Properties of Locust Muscle and Their Modulation I. Actions of the Neuropeptides YGGFMRFamide and Proctolin

Walther, Christian, Klaus E. Zittlau, Harald Murck, and Karlheinz Voigt. Resting membrane properties of locust muscle and their modulation. I. Actions of the neuropeptides YGGFMRFamide and proctolin. J. Neurophysiol. 80: 771–784, 1998. The resting K+ conductance ( G K,r) of locust jumping muscle and its modulation by two neuropeptides, proctolin (Arg-Tyr-Leu-Pro-Thr) and YGGFMRFamide (Tyr-Gly-Gly-Phe-Met-Arg-Phe-NH2), were investigated using the two-electrode voltage clamp. At a physiological [K+]o of 10 mM, G K,r accounts for ∼90% of the membrane resting conductance, and the resting membrane potential differs by ≤1 mV from E K (mean: −74 mV). There is a K+ conductance that slowly activates on hyperpolarization ( G K,H) and that seems to be largely located in the transverse tubules. Steady-state activation of G K,H was analyzed by tail current measurements. G K,H is activated partially at E K but accounts for probably ≤50% of total resting K+ conductance. Raising [K+]o caused a large increase in G K,r and in maximal steady state G K,H without shifting the voltage sensitivity of G K,H. YGGFMRFamide and proctolin reduce G K,H, mainly affecting the maximal steady-state conductance. The voltage-insensitive component of the resting K+ conductance is also reduced. The conductance suppressed by the peptides exhibited an outwardly rectifying instantaneous current/voltage-characteristic that is quite similar to that of G K,H. The actions of the two peptides appeared to be identical, but proctolin was by some two orders of magnitude more potent than YGGFMRFamide. The effects of both peptides are mediated by G proteins. They are mimicked by phorbol esters but do not seem to be initiated by either branch of the phospholipase C-dependent intracellular pathways. The properties of the resting K+ conductance in locust muscle and other invertebrate muscles are compared. The biological significance of peptide-induced reduction in resting K+ conductance is discussed in view of the known property of proctolin to support tonic force as opposed to FMRFamide-peptides that support quick leg movements.

Resting Membrane Properties of Locust Muscle and Their Modulation II. Actions of the Biogenic Amine Octopamine

Walther, Christian and Klaus E. Zittlau. Resting membrane properties of locust muscle and their modulation. II. Actions of the biogenic amine octopamine. J. Neurophysiol. 80: 785–797, 1998. 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, G Cl,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, I Cl,H, is linear and reverses at the same potential as the γ-aminobutyric acid (GABA)-mediated Cl− current. Elevation of [Cl−]i increases the maximal steady state G Cl,H ( G max) and shifts the activation curve of G Cl,H to more positive potentials. Octopamine enhances G Cl,H, mainly by increasing G max. Octopamine also lowers the resting K+ conductance ( G K,r). It reduces a hyperpolarization-activated component ( G K,H) of G K,r, mainly by decreasing G max. 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 G K,r, but not that of G Cl,H, seems to be mediated by protein kinase A (PKA). PKA seems to be constitutively activated as indicated by the pronounced increase in G K,r induced by a PKA inhibitor, H89. The properties of G Cl,H and related Cl− conductances in invertebrate and vertebrate neurons are compared. G Cl,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.