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Original Article

Plastic Modulation of Action Potential

Tenpei Akita^a and Kenji Kuba^a

^a Department of Physiology, Nagoya University School of Medicine, Nagoya 466-8550, Japan
Department of Physiology, Nagoya University School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya 466-8550, Japan.81-52-744-2049

kubak{at}med.nagoya-u.ac.jp

Fluorescent ryanodine revealed the distribution of ryanodine receptors in the submembrane cytoplasm (less than a few micrometers) of cultured bullfrog sympathetic ganglion cells. Rises in cytosolic Ca²⁺ ([Ca²⁺]_i) elicited by single or repetitive action potentials (APs) propagated at a high speed (150 µm/s) in constant amplitude and rate of rise in the cytoplasm bearing ryanodine receptors, and then in the slower, waning manner in the deeper region. Ryanodine (10 µM), a ryanodine receptor blocker (and/or a half opener), or thapsigargin (1–2 µM), a Ca²⁺-pump blocker, or -conotoxin GVIA (-CgTx, 1 µM), a N-type Ca²⁺ channel blocker, blocked the fast propagation, but did not affect the slower spread. Ca²⁺ entry thus triggered the regenerative activation of Ca²⁺-induced Ca²⁺ release (CICR) in the submembrane region, followed by buffered Ca²⁺ diffusion in the deeper cytoplasm. Computer simulation assuming Ca²⁺ release in the submembrane region reproduced the Ca²⁺ dynamics. Ryanodine or thapsigargin decreased the rate of spike repolarization of an AP to 80%, but not in the presence of iberiotoxin (IbTx, 100 nM), a BK-type Ca²⁺-activated K⁺ channel blocker, or -CgTx, both of which decreased the rate to 50%. The spike repolarization rate and the amplitude of a single AP-induced rise in [Ca²⁺]_i gradually decreased to a plateau during repetition of APs at 50 Hz, but reduced less in the presence of ryanodine or thapsigargin. The amplitude of each of the [Ca²⁺]_i rise correlated well with the reduction in the IbTx-sensitive component of spike repolarization. The apamin-sensitive SK-type Ca²⁺-activated K⁺ current, underlying the afterhyperpolarization of APs, increased during repetitive APs, decayed faster than the accompanying rise in [Ca²⁺]_i, and was suppressed by CICR blockers. Thus, ryanodine receptors form a functional triad with N-type Ca²⁺ channels and BK channels, and a loose coupling with SK channels in bullfrog sympathetic neurons, plastically modulating AP.

Key Words: Ca²⁺-induced Ca²⁺ release • intracellular Ca²⁺ dynamics • spike broadening • afterhyperpolarization • plasticity of excitability

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