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Journal of Neuroscience, Vol 14, 4412-4432, Copyright © 1994 by Society for Neuroscience
Activation of K current in the accessory radula closer muscle of Aplysia californica by neuromodulators that depress its contractions
V Brezina, CG Evans and KR Weiss
Department of Physiology and Biophysics, Mount Sinai School of Medicine, New York, New York 10029.
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 MMA, while MMB, 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 microM 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 MMA 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.
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