Activation of K current in the accessory radula closer muscle of Aplysia californica by neuromodulators that depress its contractions

V. Březina, C. G. Evans, K. R. Weiss

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The neural and cellular mechanisms of plasticity apparent in the feeding behavior of the mollusk Aplysia californica have been extensively studied in a simple neuromuscular circuit consisting of the accessory radula closer (ARC) muscle and its innervating motor and modulatory neurons. In this circuit, the plasticity is largely due to modulation of the amplitude and duration of the contractions of the muscle by a variety of modulatory neurotransmitters and peptide cotransmitters, among them the small cardioactive peptides (SCPs), myomodulins (MMs), and serotonin (5-HT). We have studied dissociated but functionally intact ARC muscle fibers to determine whether modulation of membrane ion currents in the muscle might underlie these effects. Using voltage-clamp techniques, we found that two currents were indeed modulated. In the preceding article, we proposed that enhancement of 'L'-type Ca current is the mechanism by which the modulators potentiate the amplitude of ARC-muscle contractions. Here, we report that the modulators also activate a distinctive K current. Large K currents were activated, in particular, by MM(A), while MM(B), the SCPs, and 5-HT activated much smaller currents most likely of the same kind. Buccalins, modulators that do not act directly on the ARC muscle, were ineffective. The modulator- induced K current was strongly enhanced by depolarization, but relatively slowly so that its amplitude continued to increase for several hundred milliseconds following a depolarizing voltage step. The current was Ca2+ independent, not readily blocked by extracellular Cs+ or Ba2+ and only by high concentrations of tetraethylammonium. However, it was almost completely blocked by as little as 10 μM 4-aminopyridine. In contrast to the modulator- induced enhancement of Ca current, activation of the K current was not significantly mimicked by elevation of cAMP. In the intact as well as the dissociated ARC muscle, although low levels of all of the modulators potentiate contractions, even moderate levels of MM(A) strongly depress them, whereas the other modulators depress them weakly only at high concentrations. The modulator-induced K current appears well suited to counteract depolarization of the muscle and thus limit activation of the 'L'-type Ca current that provides Ca2+ essential for contraction. We therefore propose that the modulators depress ARC-muscle contractions in large part by activating the K current. This occurs simultaneously with the enhancement of the Ca current; net potentiation or depression then depends on the balance between the relative strengths of the modulation of the two ion currents.

Original languageEnglish
Pages (from-to)4412-4432
Number of pages21
JournalJournal of Neuroscience
Issue number7
StatePublished - Jul 1994


  • Aplysia
  • cotransmitters
  • membrane ion channels
  • mollusk
  • neuromodulators
  • neuropeptides
  • potassium current
  • smooth muscle


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