Shortening deactivation: quantifying a critical component of cyclical muscle contraction

Abstract

A muscle undergoing cyclical contractions requires fast and efficient muscle activation and relaxation to generate high power with relatively low energetic cost. To enhance activation and increase force levels during shortening, some muscle types have evolved stretch activation (SA), a delayed increased in force following rapid muscle lengthening. SA's complementary phenomenon is shortening deactivation (SD), a delayed decrease in force following muscle shortening. SD increases muscle relaxation, which decreases resistance to subsequent muscle lengthening. While it might be just as important to cyclical power output, SD has received less investigation than SA. 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. When normalized to isometric tension, Drosophila IFM exhibited a 118% SD tension decrease, Lethocerus IFM dropped by 97%, and Drosophila jump muscle decreased by 37%. The same order was found for normalized SA tension: Drosophila IFM increased by 233%, Lethocerus IFM by 76%, and Drosophila jump muscle by only 11%. SD occurred slightly earlier than SA, relative to the respective length change, for both IFMs; but SD was exceedingly earlier than SA for jump muscle. Our results suggest SA and SD evolved to enable highly efficient IFM cyclical power generation and may be caused by the same mechanism. However, jump muscle SA and SD mechanisms are likely different, and may have evolved for a role other than to increase the power output of cyclical contractions.

The self-oscillation paradox in the flight motor ofDrosophila melanogaster

“…Parameters in equation (3.5) can be fitted to ex vivo muscular testing data [42][43][44]. In this study, we use data from two independent sources: firstly, and principally, the complete wild-type D. melanogaster sinusoidal testing dataset reported by Viswanathan et al [46].…”

“…Figure 3 Secondly, we use the impulse-response characterization of the dual phenomenon of stretch-activation (SA) and shortening-deactivation (SD, i.e. SA upon contraction) in wild-type D. melanogaster flight muscle reported by Loya et al [42]. It is possible to fit equation (3.5) directly to this impulse-response data; cf.…”

“…For both model types, process parameters can be identified in ex vivo empirical results for both steady and transient response testing. Indeed, muscle behaviour as per equation ((3.5) can be seen as velocity feedback: a transfer function, Efalse(Ωfalse)/iΩ, between stress and strain rate, identifiable from strain-rate impulse response data [42,43]. In addition, we note that, while nonlinearity in stretch-activated muscles is known to occur [44,45], connecting nonlinear model formulations [2,14] with observed behaviour is difficult.…”

“…It is possible to fit equation (3.5) directly to this impulse-response data; cf . [5], but raw data and the full set of fitted rate constants ( b , c , …) are rarely reported [42]; and amplitude constants ( B , C , …) are typically unreported. For this reason, we develop our own time-independent impulse-response (TIIR) estimates of the peak r , based on only a few reported SA/SD measurements—accounting for the directionally nonlinear distinction between SA and SD.…”

“…Ex vivo muscular data, leading to estimates of muscular negative loss tangent, r. Sinusoidal testing dataset from Viswanathan et al[46], with associated fit and process-wise composition (Processes A, B, C): (a) storage modulus, (b) loss modulus, (c) negative loss tangent. (d ) Strain rate impulse response data for stretch-activation (SA) and shortening-deactivation (SD) from Loya et al[42], with associated time-independent impulse-response (TIIR) estimate of r overlaid on (c). This TIIR estimate is the largest among the impulse-response data for D. melanogaster surveyed in table 1.…”