Ion Currents and Mechanisms of Modulation in the Radula Opener Muscles of Aplysia

Author:

Scott Marsha L.1,Brezina Vladimir1,Weiss Klaudiusz R.1

Affiliation:

1. Department of Physiology and Biophysics and The Fishberg Research Center in Neurobiology, Mount Sinai School of Medicine, New York, New York 10029

Abstract

Scott, Marsha L., Vladimir Brezina, and Klaudiusz R. Weiss. Ion currents and mechanisms of modulation in the radula opener muscles of Aplysia. J. Neurophysiol. 78: 2372–2387, 1997. Numerous studies of plasticity in the feeding behavior of Aplysia have shown that substantial plasticity is due to peripheral neuromodulation of the feeding musculature. Extensive previous work focusing on the accessory radula closer (ARC) muscle has led to the realization that a major function of the modulation in that muscle may be to ensure efficient coordination between its contractions and those of its antagonist muscles. For a more complete understanding, therefore, we must study these muscles also. Here we have studied the radula opener muscles I7–I10. Using single isolated muscle fibers under voltage clamp, we have characterized ion currents gated by voltage and by the physiological contraction-inducing neurotransmitter acetylcholine (ACh) and the effects of the physiological modulators serotonin, myomodulins A and B, and FMRFamide. Our results explain significant aspects of the electrophysiological behavior of the whole opener muscles, as well as why the opener and ARC muscles behave similarly in many ways yet differently in some key respects. Opener muscles express four types of K currents: inward rectifier, A-type [ I K(A)], delayed rectifier [ I K(V)], and Ca2+-activated [ I K(Ca)]. They also express an L-type Ca current [ I Ca] and a leakage current. ACh activates a positive-reversing cationic current [ I ACh(cat)] and a negative-reversing Cl current [ I ACh(Cl)]. The opener muscles differ from the ARC in that, in the openers, activation of I K(A) occurs ∼9 mV more positive and there is much less I ACh(Cl). In both muscles, I ACh(cat) most likely serves to depolarize the muscle until I Ca activates to supply Ca2+ for contraction, but further depolarization and spiking is opposed by coactivation of I K(A), I K(V), I K(Ca), and I ACh(Cl). Thus the differences in I K(A) and I ACh(Cl) may well be key factors that prevent spikes in the ARC but often allow them in the opener muscles. As in the ARC, the modulators enhance I Ca and so potentiate contractions. They also activate a modulator-specific K current, which causes hyperpolarization and depression of contractions. Finally, in the opener muscles but not in the ARC, the modulators activate a depolarizing cationic current that may help phase-advance the contractions. Each modulator exerts these effects to different degrees and thus has a distinct effect on voltage and contraction size and shape. The overall effect then will depend on the specific combinations of modulators released in different behaviors. By understanding the modulation in the opener muscles, as well as in the ARC, we are now in a position to understand how the behavior of the two muscles is coordinated under a variety of circumstances.

Publisher

American Physiological Society

Subject

Physiology,General Neuroscience

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