Role of the sarcolemma in triggered propagated contractions in rat cardiac trabeculae.

Abstract

We have recently described that after contractions propagate through multicellular cardiac muscle preparations. These propagating contractions are triggered in damaged regions of rat right ventricular trabeculae during relaxation of electrically stimulated twitches. Propagation of triggered contractions has been attributed to calcium ions that diffuse along the preparation, causing calcium-induced calcium release from the sarcoplasmic reticulum in adjacent cells. In the present study we have investigated a possible role of the sarcolemma and delayed afterdepolarizations (DADs) in the initiation and propagation of triggered propagated contractions (TPCs) in multicellular preparations. We studied whether 1) TPCs are accompanied by delayed sarcolemmal depolarizations, 2) such depolarizations mediate local contraction, and 3) an intact sarcolemma is required for propagation of contractions. TPCs that remained stable for prolonged periods of time could be induced by trains of 15 stimuli (2 Hz, 15-second intervals) at lowered temperature (19-21 degrees C) of the superfusing Krebs-Henseleit medium and a [Ca(2+)]o of 1.0-1.5 mM. Although TPCs could be induced at 38 degrees C and a [Ca2+]o of 3.0-4.0 mM, they disappeared within 10 minutes. Force was measured with a silicon strain gauge; length and shortening of sarcomeres were measured at two sites of the muscle using laser diffraction techniques. Membrane potential was measured with flexible microelectrodes. Saponin was used to selectively render the sarcolemma permeable to small ions and molecules. Propagation velocity of TPCs in intact trabeculae varied from 1.7 to 13.4 mm/sec at 19-21 degrees C. TPCs were accompanied by DADs that could reach threshold and induce triggered arrhythmias. Changes in latency, duration, and force of TPCs, induced by changing [Ca(2+)]o or the number of conditioning stimuli, were closely matched by changes in latency, duration, and amplitude of DADs; DADs consistently preceded TPCs, on average by 60 msec. Local heating of the muscle, by applying a current through an insulated platinum wire (diameter 100 microns) that touched the muscle, interrupted propagation of TPCs reversibly. DADs were, in the absence of a local contraction, still recorded distal to the heated site. In muscles that were treated with saponin and exposed to solutions approximating the intracellular milieu, spontaneously occurring local contractions that propagated in both directions (at velocities of 70-200 microns/sec) were elicited at a bathing calcium concentration of approximately 0.6 microM. Below this threshold, propagated contractions could be triggered by pressure ejection of a calcium-containing solution from a microelectrode positioned close to the trabecula.(ABSTRACT TRUNCATED AT 400 WORDS)