Sarcomere dynamics in a spontaneous contraction wave and its effect on the following, electrically triggered twitch in rat myocyte: Comparison with the rested state twitch

Abstract

A spontaneous contraction (SC) wave propagates among sarcomeres in heart muscle by the mechanism of Ca++-induced release of Ca++ from sarcoplasmic reticulum (SR). In the present study, some characteristics of unloaded shortening during the SC and its effect on a subsequent, electrically triggered twitch (Tsc) were examined at a sarcomere level in isolated rat myocytes. The results were compared with those of a rested state twitch (RS), which was accompanied by an action potential. Average shortening velocity from onset to peak of shortening was 3.74 ± 1.25 (mean ± SD, n = 18) and 5.35 ± 2.30 μm/s per sarcomere (n = 54) in SC and RS, respectively. That the former was smaller than the latter (P < 0.01, t test) suggests that Ca++ are released from the SR more slowly in the SC than the RS. There were no differences in either the extent or area of shortening between SC and RS. The extent of shortening increased significantly as shortening velocity increased in all the SC (P < 0.05), RS, Tsc, and triggered twitch (Trs) after the RS (P < 0.001 in the last three). The slope of the line for the regression of the extent upon the velocity of shortening in the SC was ~ 1.5 times greater than the other three. This suggests that the SC has a different time course of change of myoplasmic [Ca++] and therefore a different mode of the causal SR Ca++ release from the electrically triggered twitches (RS, Trs, Tsc). There were positive correlations between the extent and the area of shortening in each of the RS (P < 0.01), the Trs (P < 0.05), and the Tsc (P < 0.001), but not in SC. The slope of the line for the regression of the extent upon the area of shortening in the Tsc was about three times greater than those in the RS and the Trs, suggesting characteristics of the Tsc from different those of the RS and the Trs. An SC inhibited a Tsc in an interval- dependent manner. The shortening velocity in the Tsc recovered fully at a test interval of ~0.6 s between the onsets of the two successive contractions. The velocity increased further with further increasing the test interval (up to 0.9 s). At a test interval of 0.8-0.9 s, the shortening velocity in the Tsc was greater than those in the preceding SC and the corresponding Trs by 1.17- and 1.80-fold, respectively, as compared in the same five sarcomeres. This may be taken to indicate that the SC accelerates the SR Ca++ release in the subsequent, Tsc. There was little difference in either the extent or area of shortening between the Tsc and the Trs, aside from the shortening area at a test interval of 0.3-0.4 s. At such short intervals, the shortening area was 17.6 ± 7.2 (n = 5) and 30.4 ± 9.1 μm · ms (n = 14) in the Tsc and the Trs, respectively. The difference was significant (P < 0.05). This result is in agreement with the idea that a part of Ca++ entering the myocyte during an action potential is sucked up by the SR and used for the next twitch. In conclusion, the SC has different effects from the RS on the subsequent, action potential-mediated twitch.