Ionic Currents Underlying Fast Action Potentials in the Obliquely Striated Muscle Cells of the Octopus Arm

Abstract

The octopus arm provides a unique model for neuromuscular systems of flexible appendages. We previously reported the electrical compactness of the arm muscle cells and their rich excitable properties ranging from fast oscillations to overshooting action potentials. Here we characterize the voltage-activated ionic currents in the muscle cell membrane. We found three depolarization-activated ionic currents: 1) a high-voltage-activated L-type Ca2+current, which began activating at approximately −35 mV, was eliminated when Ca2+was substituted by Mg2+, was blocked by nifedipine, and showed Ca2+-dependent inactivation. This current had very rapid activation kinetics (peaked within milliseconds) and slow inactivation kinetics (τ in the order of 50 ms). 2) A delayed rectifier K+current that was totally blocked by 10 mM TEA and partially blocked by 10 mM 4-aminopyridine (4AP). This current exhibited relatively slow activation kinetics (τ in the order of 15 ms) and inactivated only partially with a time constant of ∼150 ms. And 3) a transient A-type K+current that was totally blocked by 10 mM 4AP and was partially blocked by 10 mM TEA. This current exhibited very fast activation kinetics (peaked within milliseconds) and inactivated with a time constant in the order of 60 ms. Inactivation of the A-type current was almost complete at −40 mV. No voltage-dependent Na+current was found in these cells. The octopus arm muscle cells generate fast (∼3 ms) overshooting spikes in physiological conditions that are carried by a slowly inactivating L-type Ca2+current.