A New Method for Characterizing Muscle Shortening Deactivation

Abstract

A muscle undergoing a cyclical lengthening and shortening contraction pattern requires fast and efficient muscle activation and relaxation. To boost activation rate and increase force levels during shortening, some muscles have evolved stretch activation (SA), a delayed increased in force following rapid muscle lengthening. Equally important is a fast relaxation rate and low force during muscle lengthening. If a muscle incompletely relaxes, its antagonist muscle expends more energy lengthening it, causing decreased power generation and efficiency. Thus, increasing relaxation rate can increase work and power. However, increasing relaxation rate is costly because it typically occurs via ATPases pumping calcium out of the myoplasm. Some flying insect species have greatly reduced this cost in their indirect flight muscle (IFM) by evolving a property known as shortening deactivation (SD), which decreases force levels during a contraction cycle without having to change calcium concentration. SD is a delayed decrease in force following rapid shortening of an active muscle. In IFM, the timing of this force decrease allows the antagonist muscle (DVM) to be lengthened with much less resistance from the agonist muscle (DLM). While there is general appreciation for SD in IFM, there have been few investigations into whether SD is present in other muscle types and if so, how much it benefits these muscles. Even less is known about SD’s mechanism as there have been no investigations into the SD mechanism for any muscle type. To enable mechanistic investigations into SD and quantitatively compare it to SA, we developed a protocol to elicit SA and SD from Drosophila and Lethocerus indirect flight muscles (IFM) and Drosophila jump muscle. All three muscle types exhibited a 4‐phase tension transient in response to a 1% length decrease, with phase 3 defined as SD. Lethocerus IFM presented the greatest SD tension drop, 20 mN/mm2, which was ~1.5‐fold greater than Drosophila jump muscle and ~10‐fold greater than DrosophilaIFM. However, isometric tension in Drosophilajump muscle, 34.3 mN/mm2, was higher than Lethocerus, 18.4 mN/mm2, and DrosophilaIFM, 1.6 mN/mm2. Thus, when normalized to isometric tension, Drosophila IFM exhibited a 118% SD tension decrease. Similarly, SD tension in Lethocerus IFM dropped by 97%, while Drosophilajump muscle decreased by 37%. The same order occurred for normalized phase 3 SA tension: Drosophila IFM displayed the largest gain, 233%, Lethocerus IFM increased by 76%, and Drosophila jump muscle showed only a 11% increase. SD phase 3 occurred a bit earlier than SA phase 3, relative to the length change, for both IFMs; but SD was exceedingly earlier than SA for jump muscle. We suggest that SA and SD evolved together to enable fast and efficient IFM cyclical power generation and may be caused by the same molecular mechanism. However, the SA and SD molecular mechanisms in jump muscle are likely different and might have evolved for an alternate role besides increasing the power output of cyclical muscle contractions.