Characterization of the membrane ion currents of a model molluscan muscle, the accessory radula closer muscle of Aplysia california. I. Hyperpolarization-activated currents.

Abstract

1. The simple neuromuscular circuit consisting of the accessory radula closer (ARC) muscle of the mollus Aplysia californica together with its innervating motor and modulatory neurons has been extensively studied as a model preparation in which it might be possible to reach an integrated understanding of the neural and cellular mechanisms of behavioral plasticity, in this case of a component of Aplysia feeding behavior. Previous work has suggested that much of the plasticity of this behavior is implemented by appropriate release of modulatory neurotransmitters and peptide cotransmitters that modulate several parameters of the contractions of the ARC muscle. However, little is as yet known about the underlying cellular mechanisms. 2. We have begun to study single, functionally intact fibers dissociated from the ARC muscle to assess to what extent the modulation of its contraction might be mediated by one candidate mechanism, modulation of its membrane ion currents. First, however, it was necessary to gain a thorough understanding of the unmodulated currents and their likely roles in normal contraction. Using voltage-clamp techniques, we have therefore identified and characterized the major currents present in the ARC muscle fibers. We describe these currents in this and the following two papers. These results constitute the first detailed description of ion currents in a molluscan muscle and lay the foundation for further study, to be presented in subsequent papers, of the roles of two currents that we have indeed found to be modulated in ways likely to contribute to the modulation of contraction. 3. In this paper we first describe the general electrophysiological characteristics of the dissociated fibers and present evidence that the fibers can be adequately space clamped. 4. The physiological operating voltage range of the nonspiking ARC muscle most likely extends from about -80 to about -25 mV. The steady-state current-voltage (I-V) relation of total membrane current rectifies inwardly in the negative and outwardly in the positive portion of this voltage range, with a plateau region of high or even negative slope resistance separating the two regions of rectification. 5. The current responsible for the inward rectification at negative voltages is a classical inwardly rectifying K current. It is activated by hyperpolarization with quasi-instantaneous kinetics; its whole I-V relation shifts along the voltage axis in a Nernstian manner with altered extracellular K+ concentration; it is blocked by low extracellular Ba2+ and Cs+, and the block is promoted by hyperpolarization.(ABSTRACT TRUNCATED AT 400 WORDS)