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Spatial characteristics of sarcoplasmic reticulum Ca²⁺ release events triggered by L-type Ca²⁺ current and Na⁺ current in guinea-pig cardiac myocytes

Peter Lipp*†, Marcel Egger* and Ernst Niggli*

Ca²⁺ signals in cardiac muscle cells are composed of spatially limited elementary events termed Ca²⁺ sparks. Several studies have also indicated that Ca²⁺ signals smaller than Ca²⁺ sparks can be elicited. These signals have been termed Ca²⁺ quarks and were proposed to result from the opening of a single Ca²⁺ release channel of the sarcoplasmic reticulum. We used laser-scanning confocal microscopy to examine the subcellular properties of Na⁺ current (I_Na)- and L-type Ca²⁺ current (I_Ca,L)-induced Ca²⁺ transients in voltage-clamped ventricular myocytes isolated from guinea-pigs. Both currents, I_Na and I_Ca,L, evoked substantial, global Ca²⁺ transients. To examine the spatiotemporal properties of such Ca²⁺ signals, we performed power spectral analysis of these Ca²⁺ transients and found that both lacked spatial frequency components characteristic for Ca²⁺ sparks. The application of 10 µM verapamil to partially block L-type Ca²⁺ current reduced the corresponding Ca²⁺ transients down to individual Ca²⁺ sparks. In contrast, I_Na-induced Ca²⁺ responses were still spatially homogeneous and lacked Ca²⁺ sparks even for small current amplitudes. By using high resistance patch pipettes (> 4 M) to exaggerate the loss of voltage control during I_Na, Ca²⁺ sparks appeared superimposed on a homogeneous Ca²⁺ release component and were exclusively triggered during the flow of I_Na. In the presence of 10 µM ryanodine both I_Ca,L and I_Na elicited small, residual Ca²⁺ transients that were spatially homogeneous but displayed distinctively different temporal profiles. We conclude that I_Na is indeed able to cause Ca²⁺ release in guinea-pig ventricular myocytes. In contrast to I_Ca,L-induced Ca²⁺ transients, which are built up from the recruitment of individual Ca²⁺ sparks, the I_Na-evoked cellular responses were always homogeneous, indicating that their underlying elementary Ca²⁺ release event is distinct from the Ca²⁺ spark. Thus, I_Na-induced Ca²⁺ transients are composed of smaller Ca²⁺ signals, most likely Ca²⁺ quarks.

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