Isolated Giant Smooth Muscle Fibres in Beroe Ovata: Ionic Dependence of Action Potentials Reveals two Distinct Types of Fibre

Abstract

ABSTRACT The ionic dependence of action potentials evoked in giant smooth muscle fibres isolated by enzymatic digestion from the body wall of the marine invertebrate Beroe ovata (Ctenophora) has been investigated using conventional electrophysiological techniques. Differences were observed in the two fibre types studied. The resting membrane potential was –60 ± 1·35 mV (N = 25) in longitudinal muscle fibres and –66 ± 1·37 mV (N =32) in radial fibres. Action potentials had a short plateau in longitudinal fibres but not in radial fibres. The action potential overshoot of both fibre types was decreased in Ca2+-free artificial sea water (ASW). In Na+-deficient ASW, action potentials could not be generated in radial fibres and showed a reduced overshoot in longitudinal fibres. Tetrodotoxin (10−smoll−1) added to ASW or Ca2+-free ASW did not affect the action potentials of either type of fibre. Action potentials of both fibres were partially blocked by Co2+ (20-50 mmol 1−1) or Cd2+ (1-2 mmol 1−1). Action potentials of longitudinal fibres in Na+-deficient ASW were abolished by Co2+ (20 mmol 1−1). In Ca2+-free ASW, the action potential overshoots of both sets of fibres were restored following the addition of Sr2+ or Ba2+. In longitudinal fibres, Sr2+ increased the duration of the action potential plateau. In both longitudinal and radial muscle fibres, Ba2+ prolonged the action potential. In longitudinal fibres exposed to tetraethylammonium chloride (TEACI) or 4-aminopyridine (4AP), the action potential was slightly prolonged. In these fibres, TEA+ or 4AP added to Ca2+-free ASW induced only a long-lasting depolarizing plateau. In radial fibres, the action potential duration was slightly increased in the presence of TEA+; it was unaffected by 4AP. In Ca2+-free ASW, TEA+ and 4AP induced an oscillating membrane response which appeared to be dependent on the intensity of the injected current pulse. It is concluded that (a) there are significant differences between the action potentials of longitudinal and radial muscle fibres but that both are dependent on Na+ and Ca2+, (b) in longitudinal fibres, a Ca2+-activated K+ conductance and a TEA+-sensitive voltage-activated K+ conductance contribute to the repolarizing phase of the action potential, the former being predominant, (c) in radial fibres, the repolarizing phase of action potentials probably involves different membrane K+ conductances among which is a TEA+-sensitive K+ conductance.