Transient and Steady-State Force Enhancement in the Drosophila Jump Muscle

Author(s):  
Ryan A. Koppes ◽  
Douglas M. Swank ◽  
David T. Corr

The increase of isometric force after active lengthening, termed force enhancement (FE), is a well-accepted characteristic of skeletal muscle that has been demonstrated in both whole muscle [1,3] and single-fiber preparations [1,2]. The amount of FE increases with increasing amplitudes of stretch, yet no clear correlation between FE and the rate stretch has been demonstrated [2]. Although this behavior has been observed experimentally for over 70 years, its underlying mechanism(s) remain unknown. Furthermore, most studies of FE have been limited to steady-state (FESS) observations [1–3], whereas clues to the underlying mechanism(s) may very well exist in the transient force recovery period following an active stretch, as seen in another history-dependent phenomenon, force depression [4].

Author(s):  
Ryan A. Koppes ◽  
David T. Corr

The enhancement of isometric force after active stretching is a well-accepted and demonstrated characteristic of skeletal muscle in both whole muscle [1,2] and single-fiber preparations [1,3], but its mechanisms remain unknown. Although traditionally analyzed at steady-state, transient phenomena caused, at least in part, by cross-bridge kinetics may provide novel insight into the mechanisms associated with force enhancement (FE). In order to identify the transient aspects of FE and its relation to stretching speed, stretching amplitude, and muscle mechanical work, a post hoc analysis of in situ experiments in soleus muscle tendon units of anesthetized cats [2] was conducted. The period immediately following stretching, at which the force returns to steady-state, was fit using an exponential decay function. The aims of this study were to analyze and quantify the effects of stretching amplitude, stretching speed, and muscle mechanical work on steady-state force enhancement (FEss) and transient force relaxation rate after active stretching. The results of this study were interpreted with respect to prior force depression (FD) experiments [4], to identify if the two phenomena exhibited similar transient and steady-state behaviors, and thus could be described by the same underlying mechanism(s).


2015 ◽  
Vol 309 (8) ◽  
pp. C551-C557 ◽  
Author(s):  
Ryan A. Koppes ◽  
Douglas M. Swank ◽  
David T. Corr

The increase in steady-state force after active lengthening in skeletal muscle, termed force enhancement (FE), has been observed for nearly one century. Although demonstrated experimentally at various structural levels, the underlying mechanism(s) remain unknown. We recently showed that the Drosophila jump muscle is an ideal model for investigating mechanisms behind muscle physiological properties, because its mechanical characteristics, tested thus far, duplicate those of fast mammalian skeletal muscles, and Drosophila has the advantage that it can be more easily genetically modified. To determine if Drosophila would be appropriate to investigate FE, we performed classic FE experiments on this muscle. Steady-state FE (FESS), following active lengthening, increased by 3, 7, and 12% of maximum isometric force, with increasing stretch amplitudes of 5, 10, and 20% of optimal fiber length (FLOPT), yet was similar for stretches across increasing stretch velocities of 4, 20, and 200% FLOPT/s. These FESS characteristics of the Drosophila jump muscle closely mimic those observed previously. Jump muscles also displayed typical transient FE characteristics. The transient force relaxation following active stretch was fit with a double exponential, yielding two phases of force relaxation: a fast initial relaxation of force, followed by a slower recovery toward steady state. Our analyses identified a negative correlation between the slow relaxation rate and FESS, indicating that there is likely an active component contributing to FE, in addition to a passive component. Herein, we have established the Drosophila jump muscle as a new and genetically powerful experimental model to investigate the underlying mechanism(s) of FE.


2014 ◽  
Vol 116 (12) ◽  
pp. 1543-1550 ◽  
Author(s):  
Ryan A. Koppes ◽  
Douglas M. Swank ◽  
David T. Corr

Force depression (FD) is a decrease in isometric force following active muscle shortening. Despite being well characterized experimentally, its underlying mechanism remains unknown. To develop a new, genetically manipulatable experimental model that would greatly improve our ability to study the underlying mechanism(s) of FD, we tested the Drosophila jump muscle for classical FD behavior. Steady-state force generation following active shortening decreased by 2, 8, and 11% of maximum isometric force with increasing shortening amplitudes of 5, 10, and 20% of optimal fiber length, and decreased by 11, 8, and 5% with increasing shortening velocities of 4, 20, and 200% of optimal fiber length per second. These steady-state FD (FDSS) characteristics of Drosophila jump muscle mimic those observed in mammalian skeletal muscle. A double exponential fit of transient force recovery following shortening identified two separate phases of force recovery: a rapid initial force redevelopment, and a slower recovery toward steady state. This analysis showed the slower rate of force redevelopment to be inversely proportional to the amount of FDSS, while the faster rate did not correlate with FDSS. This suggests that the mechanism behind the slower, most likely cross-bridge cycling rate, influences the amount of FDSS. Thus the jump muscle, when coupled with the genetic mutability of its sarcomere proteins, offers a unique and powerful experimental model to explore the underlying mechanism behind FD.


2019 ◽  
Vol 126 (3) ◽  
pp. 647-657 ◽  
Author(s):  
Jackey Chen ◽  
Geoffrey A. Power

The increase and decrease in steady-state isometric force following active muscle lengthening and shortening are referred to as residual force enhancement (RFE) and force depression (FD), respectively. The RFE and FD states are associated with decreased (activation reduction; AR) and increased (activation increase; AI) neuromuscular activity, respectively. Although the mechanisms have been discussed over the last 60 years, no studies have systematically investigated the modifiability of RFE and FD with training. The purpose of the present study was to determine whether RFE and FD could be modulated through eccentric and concentric biased resistance training. Fifteen healthy young adult men (age: 24 ± 2 yr, weight: 77 ± 8 kg, height: 178 ± 5 cm) underwent 4 wk of isokinetic dorsiflexion training, in which one leg was trained eccentrically (−25°/s) and the other concentrically (+25°/s) over a 50° ankle excursion. Maximal and submaximal (40% maximum voluntary contraction) steady-state isometric torque and EMG values following active lengthening and shortening were compared to purely isometric values at the same joint angles and torque levels. Residual torque enhancement (rTE) decreased by ~36% after eccentric training ( P < 0.05) and increased by ~89% after concentric training ( P < 0.05), whereas residual torque depression (rTD), AR, AI, and optimal angles for torque production were not significantly altered by resistance training ( P ≥ 0.05). It appears that rTE, but not rTD, for the human ankle dorsiflexors is differentially modifiable through contraction type-dependent resistance training. NEW & NOTEWORTHY The history dependence of force production is a property of muscle unexplained by current cross bridge and sliding filament theories. Whether a muscle is actively lengthened (residual force enhancement; RFE) or shortened (force depression) to a given length, the isometric force should be equal to a purely isometric contraction—but it is not! In this study we show that eccentric training decreased RFE, whereas concentric training increased RFE and converted all nonresponders (i.e., not exhibiting RFE) into responders.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Ricarda M. Haeger ◽  
Dilson E. Rassier

AbstractWhen a muscle is stretched during a contraction, the resulting steady-state force is higher than the isometric force produced at a comparable sarcomere length. This phenomenon, also referred to as residual force enhancement, cannot be readily explained by the force-sarcomere length relation. One of the most accepted mechanisms for the residual force enhancement is the development of sarcomere length non-uniformities after an active stretch. The aim of this study was to directly investigate the effect of non-uniformities on the force-producing capabilities of isolated myofibrils after they are actively stretched. We evaluated the effect of depleting a single A-band on sarcomere length non-uniformity and residual force enhancement. We observed that sarcomere length non-uniformity was effectively increased following A-band depletion. Furthermore, isometric forces decreased, while the percent residual force enhancement increased compared to intact myofibrils (5% vs. 20%). We conclude that sarcomere length non-uniformities are partially responsible for the enhanced force production after stretch.


2020 ◽  
Vol 223 (15) ◽  
pp. jeb218776 ◽  
Author(s):  
Jackey Chen ◽  
Parastoo Mashouri ◽  
Stephanie Fontyn ◽  
Mikella Valvano ◽  
Shakeap Elliott-Mohamed ◽  
...  

ABSTRACTThe increase or decrease in isometric force following active muscle lengthening or shortening, relative to a reference isometric contraction at the same muscle length and level of activation, are referred to as residual force enhancement (rFE) and residual force depression (rFD), respectively. The purpose of these experiments was to investigate the trainability of rFE and rFD on the basis of serial sarcomere number (SSN) alterations to history-dependent force properties. Maximal rFE/rFD measures from the soleus and extensor digitorum longus (EDL) of rats were compared after 4 weeks of uphill or downhill running with a no-running control. SSN adapted to the training: soleus SSN was greater with downhill compared with uphill running, while EDL demonstrated a trend towards more SSN for downhill compared with no running. In contrast, rFE and rFD did not differ across training groups for either muscle. As such, it appears that training-induced SSN adaptations do not modify rFE or rFD at the whole-muscle level.


Author(s):  
Ryan A. Koppes ◽  
Douglas M. Swank ◽  
David T. Corr

The depression of isometric force after active shortening, termed force depression (FD), is a well-accepted characteristic of skeletal muscle that has been demonstrated in both whole muscle [1,3] and single-fiber preparations [1,2]. Although this history-dependent behavior has been observed experimentally for over 70 years, its underlying mechanism(s) remain unknown. Drosophila melangastor, commonly known as the fruit fly, is a well established, comprehensively understood, and genetically manipulable animal model. Furthermore, Drosophila have proved to be an accurate model species for studying muscle mechanics, and the Tergal Depressor of the Trochanter (TDT), or jump muscle, has most precisely resembled the mechanics of mammalian skeletal muscle [4]. Due to the structural and phenomenological similarities of the TDT muscle to skeletal muscle, in addition to the potential use of genetic mutations in fly models, it is extremely advantageous to investigate the presence of history dependent phenomenon in the TDT. If such phenomena are present, further investigation utilizing different myosin and actin isoforms to study the underlying mechanism(s) could produce new insight into this history-dependent phenomenon, otherwise impossible to elucidate using current experimental models. Thus, it is the goal of this study to determine the presence and degree of FD in the TDT muscle of wild type Drosophila.


2005 ◽  
Vol 99 (1) ◽  
pp. 252-260 ◽  
Author(s):  
David T. Corr ◽  
Walter Herzog

The depression of isometric force after active shortening is a well-accepted characteristic of skeletal muscle, yet its mechanisms remain unknown. Although traditionally analyzed at steady state, transient phenomena caused, at least in part, by cross-bridge kinetics may provide novel insight into the mechanisms associated with force depression (FD). To identify the transient aspects of FD and its relation to shortening speed, shortening amplitude, and muscle mechanical work, in situ experiments were conducted in soleus muscle-tendon units of anesthetized cats. The period immediately after shortening, in which force recovers toward steady state, was fit by using an exponential recovery function ( R2 > 0.99). Statistical analyses revealed that steady-state FD (FDss) increased with shortening amplitude and mechanical work. This FDss increase was always accompanied by a significant decrease in force recovery rate. Furthermore, a significant reduction in stiffness was observed after all activated shortenings, presumably because of a reduced proportion of attached cross bridges. These results were interpreted with respect to the two most prominent proposed mechanisms of force depression: sarcomere length nonuniformity theory ( 7 , 32 ) and a stress-induced inhibition of cross-bridge binding in the newly formed actin-myosin overlap zone ( 14 , 28 ). We hypothesized that the latter could describe both steady-state and transient aspects of FD using a single scalar variable, the mechanical work done during shortening. As either excursion (overlap) or force (stress) is increased, mechanical work increases, and cross-bridge attachment would become more inhibited, as supported by this study in which an increase in mechanical work resulted in a slower recovery to a more depressed steady-state force.


2020 ◽  
Author(s):  
Jackey Chen ◽  
Parastoo Mashouri ◽  
Stephanie Fontyn ◽  
Mikella Valvano ◽  
Shakeap Elliott-Mohamed ◽  
...  

AbstractThe increase or decrease in isometric force following active muscle lengthening or shortening, relative to a reference isometric contraction at the same muscle length and level of activation, are referred to as residual force enhancement (rFE) and residual force depression (rFD), respectively. The purpose of these experiments was to gain further mechanistic insight into the trainability of rFE and rFD, on the basis of serial sarcomere number (SSN) alterations to length-dependent properties. Maximal rFE/rFD measures from the soleus and extensor digitorum longus (EDL) of rats were compared after 4 weeks of uphill/downhill running and a no running control. Serial sarcomere numbers adapted to the training: soleus serial sarcomere number was greater with downhill compared to uphill running, while EDL demonstrated a trend towards more serial sarcomeres for downhill compared to no running. In contrast, absolute and normalized rFE/rFD did not differ across training groups for either muscle. As such, it appears that training-induced SSN adaptations do not modify rFE/rFD at the whole-muscle level.Summary StatementThe addition and subtraction of serial sarcomeres induced by downhill and uphill running, respectively, did not influence the magnitude of stretch-induced force enhancement and shortening-induced force depression.


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