scholarly journals Effect of Active Lengthening and Shortening on Small-Angle X-ray Reflections in Skinned Skeletal Muscle Fibres

2021 ◽  
Vol 22 (16) ◽  
pp. 8526
Author(s):  
Venus Joumaa ◽  
Ian C. Smith ◽  
Atsuki Fukutani ◽  
Timothy R. Leonard ◽  
Weikang Ma ◽  
...  

Our purpose was to use small-angle X-ray diffraction to investigate the structural changes within sarcomeres at steady-state isometric contraction following active lengthening and shortening, compared to purely isometric contractions performed at the same final lengths. We examined force, stiffness, and the 1,0 and 1,1 equatorial and M3 and M6 meridional reflections in skinned rabbit psoas bundles, at steady-state isometric contraction following active lengthening to a sarcomere length of 3.0 µm (15.4% initial bundle length at 7.7% bundle length/s), and active shortening to a sarcomere length of 2.6 µm (15.4% bundle length at 7.7% bundle length/s), and during purely isometric reference contractions at the corresponding sarcomere lengths. Compared to the reference contraction, the isometric contraction after active lengthening was associated with an increase in force (i.e., residual force enhancement) and M3 spacing, no change in stiffness and the intensity ratio I1,1/I1,0, and decreased lattice spacing and M3 intensity. Compared to the reference contraction, the isometric contraction after active shortening resulted in decreased force, stiffness, I1,1/I1,0, M3 and M6 spacings, and M3 intensity. This suggests that residual force enhancement is achieved without an increase in the proportion of attached cross-bridges, and that force depression is accompanied by a decrease in the proportion of attached cross-bridges. Furthermore, the steady-state isometric contraction following active lengthening and shortening is accompanied by an increase in cross-bridge dispersion and/or a change in the cross-bridge conformation compared to the reference contractions.

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.


2008 ◽  
Vol 105 (2) ◽  
pp. 457-462 ◽  
Author(s):  
Eun-Jeong Lee ◽  
Walter Herzog

Residual force enhancement (FE) following stretch of an activated muscle is a well accepted property of skeletal muscle contraction. However, the mechanism underlying FE remains unknown. A crucial assumption on which some proposed mechanisms are based is the idea that forces in the enhanced state cannot exceed the steady-state isometric force at a sarcomere length associated with optimal myofilament overlap. Although there are a number of studies in which forces in the enhanced state were compared with the corresponding isometric forces on the plateau of the force-length relationship, these studies either did not show enhanced forces above the plateau or, if they did, they lacked measurements of sarcomere lengths confirming the plateau region. Here, we revisited this question by optimizing stretch conditions and measuring the average sarcomere lengths in isolated fibers, and we found that FE exceeded the maximal isometric reference force obtained at the plateau of the force-length relationship consistently (mean ± SD: 4.8 ± 2.1%) and by up to 10%. When subtracting the passive component of FE from the total FE, the enhanced forces remained greater than the isometric plateau force (mean ± SD: 4.3 ± 2.0%). Calcium-induced increases in passive forces, known to be present in single fibers and myofibrils, are too small to account for the FE observed here. We conclude that FE cannot be explained exclusively with a stretch-induced development of sarcomere length nonuniformities, that FE in single fibers may be associated with the recruitment of additional contractile force, and that isometric steady-state forces in the enhanced state are not uniquely determined by sarcomere lengths.


PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e5421 ◽  
Author(s):  
Caleb T. Sypkes ◽  
Benjamin J. Kozlowski ◽  
Jordan Grant ◽  
Leah R. Bent ◽  
Chris J. McNeil ◽  
...  

Background Following active muscle lengthening, there is an increase in steady-state isometric force as compared with a purely isometric contraction at the same muscle length and level of activation. This fundamental property of skeletal muscle is known as residual force enhancement (RFE). While the basic mechanisms contributing to this increase in steady-state isometric force have been well documented, changes in central nervous system (CNS) excitability for submaximal contractions during RFE are unclear. The purpose of this study was to investigate spinal and supraspinal excitability in the RFE isometric steady-state following active lengthening of the ankle dorsiflexor muscles. Methods A total of 11 male participants (20–28 years) performed dorsiflexions at a constant level of electromyographic activity (40% of maximum). Half of the contractions were purely isometric (8 s at an ankle angle of 130°), and the other half were during the RFE isometric steady-state following active lengthening (2 s isometric at 90°, a 1 s lengthening phase at 40°/s, and 5 s at 130°). Motor evoked potentials (MEPs), cervicomedullary motor evoked potentials (CMEPs), and compound muscle action potentials (M-waves) were recorded from the tibialis anterior during the purely isometric contraction and RFE isometric steady-state. Results Compared to the purely isometric condition, following active lengthening, there was 10% RFE (p < 0.05), with a 17% decrease in normalized CMEP amplitude (CMEP/Mmax) (p < 0.05) and no change in normalized MEP amplitude (MEP/CMEP) (p > 0.05). Discussion These results indicate that spinal excitability is reduced during submaximal voluntary contractions in the RFE state with no change in supraspinal excitability. These findings may have further implications to everyday life offering insight into how the CNS optimizes control of skeletal muscle following submaximal active muscle lengthening.


2012 ◽  
Vol 302 (1) ◽  
pp. C240-C248 ◽  
Author(s):  
Dilson E. Rassier ◽  
Ivan Pavlov

When a stretch is imposed to activated muscles, there is a residual force enhancement that persists after the stretch; the force is higher than that produced during an isometric contraction in the corresponding length. The mechanisms behind the force enhancement remain elusive, and there is disagreement if it represents a sarcomeric property, or if it is associated with length nonuniformities among sarcomeres and half-sarcomeres. The purpose of this study was to investigate the effects of stretch on single sarcomeres and myofibrils with predetermined numbers of sarcomeres ( n = 2, 3. . . , 8) isolated from the rabbit psoas muscle. Sarcomeres were attached between two precalibrated microneedles for force measurements, and images of the preparations were projected onto a linear photodiode array for measurements of half-sarcomere length (SL). Fully activated sarcomeres were subjected to a stretch (5–10% of initial SL, at a speed of 0.3 μm·s−1·SL−1) after which they were maintained isometric for at least 5 s before deactivation. Single sarcomeres showed two patterns: 31 sarcomeres showed a small level of force enhancement after stretch (10.46 ± 0.78%), and 28 sarcomeres did not show force enhancement (−0.54 ± 0.17%). In these preparations, there was not a strong correlation between the force enhancement and half-sarcomere length nonuniformities. When three or more sarcomeres arranged in series were stretched, force enhancement was always observed, and it increased linearly with the degree of half-sarcomere length nonuniformities. The results show that the residual force enhancement has two mechanisms: 1) stretch-induced changes in sarcomeric structure(s); we suggest that titin is responsible for this component, and 2) stretch-induced nonuniformities of half-sarcomere lengths, which significantly increases the level of force enhancement.


2010 ◽  
Vol 299 (6) ◽  
pp. C1398-C1401 ◽  
Author(s):  
T. R. Leonard ◽  
M. DuVall ◽  
W. Herzog

It has been accepted for half a century that, for a given level of activation, the steady-state isometric force of a muscle sarcomere depends exclusively on the amount of overlap between the contractile filaments actin and myosin, or equivalently sarcomere length (Gordon AM et al., J Physiol 184: 170–192, 1966). Moreover, according to the generally accepted paradigm of muscle contraction, the cross-bridge theory (Huxley AF, Prog Biophys Biophys Chem 7: 255–318, 1957), this steady-state isometric sarcomere force is independent of the muscle's contractile history (Huxley AF, Prog Biophys Biophys Chem 7: 255–318, 1957; Walcott S and Herzog W, Math Biosci 216: 172–186, 2008); i.e., it is independent of whether a muscle is held at a constant length before and during the contraction or whether the muscle is shortened or lengthened to the same constant length. This, however, is not the case, as muscles and single fibers that are stretched show greatly increased steady-state isometric forces compared with preparations that are held at a constant length (Abbott BC and Aubert XM, J Physiol 117: 77–86, 1952; De Ruiter CJ et al., J Physiol 526.3: 671–681, 2000; Edman KAP et al., J Physiol 281: 139–155, 1978; Edman KAP et al., J Gen Physiol 80: 769–784, 1982; Edman KAP and Tsuchiya T, J Physiol 490.1: 191–205, 1996). This so-called “residual force enhancement” (Edman KAP et al., J Gen Physiol 80: 769–784, 1982) offers a perplexing puzzle for muscle physiologists. Many theories have been advanced to address the discrepancy between prediction and observation with the most popular and accepted being the sarcomere length nonuniformity theory (Morgan DL, Biophys J 57: 209–221, 1990), which explains the residual force enhancement with the development of large nonuniformities in sarcomere lengths during muscle stretching. Here, we performed experiments in mechanically isolated sarcomeres and observed that the residual force enhancement following active stretching is preserved. Since our preparation utilizes a single sarcomere, a redistribution of the length of neighboring sarcomeres to produce the higher force following stretch is, by design, precluded. Furthermore, the enhanced forces in the single sarcomeres always exceed the isometric forces on the plateau of the force-length relationship, thereby eliminating the possibility that our result might have been obtained because of a redistribution of half-sarcomere lengths. Since force enhancement in single myofibrils has been associated with actin-titin interactions (Kulke M et al., Circ Res 89: 874–881, 2001; Li Q et al., Biophys J 69: 1508–1518, 1995) and calcium binding to titin (Joumaa V et al., Am J Physiol Cell Physiol 294: C74–C78, 2008; Labeit D et al., Proc Natl Acad Sci USA 100: 13716–13721, 2003), titin may regulate the sarcomeric force enhancement observed here.


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.


1982 ◽  
Vol 80 (5) ◽  
pp. 769-784 ◽  
Author(s):  
K A Edman ◽  
G Elzinga ◽  
M I Noble

Single fibers from the tibialis anterior muscle of Rana temporaria at 0.8-3.8 degrees C were subjected to long tetani lasting up to 8 s. Stretch of the fiber early in the tetanus caused an enhancement of force above the isometric control level which decayed only slowly and stayed higher throughout the contraction. This residual enhancement was uninfluenced by velocity of stretch and occurred only on the descending limb of the length-tension curve. The absolute magnitude of the effect increased with sarcomere length to a maximum at approximately 2.9 micrometers and then declined. The phenomenon was further characterized by its dependence on the amplitude of stretch. The final force level reached after stretch was usually higher than the isometric force level corresponding to the starting length of the stretch. The possibility that the phenomenon was caused by nonuniformity of sarcomere length along the fiber was examined by (a) laser diffraction studies that showed sarcomere stretch at all locations and (b) studies of 9-10 segments of approximately 0.6-0.7 mm along the entire fiber, which all elongated during stretch. Length-clamped segments showed residual force enhancement after stretch when compared with the tetanus produced by the same segment held at the short length as well as at the long length. It is concluded that residual force enhancement after stretch is a property shown by all individual segments along the fiber.


2016 ◽  
Vol 3 (3) ◽  
pp. 150657 ◽  
Author(s):  
Kaleena Johnston ◽  
Azim Jinha ◽  
Walter Herzog

The sarcomere length non-uniformity theory (SLNT) is a widely accepted explanation for residual force enhancement (RFE). RFE is the increase in steady-state isometric force following active muscle stretching. The SLNT predicts that active stretching of a muscle causes sarcomere lengths (SL) to become non-uniform, with some sarcomeres stretched beyond actin–myosin filament overlap (popping), causing RFE. Despite being widely known, this theory has never been directly tested. We performed experiments on isolated rabbit muscle myofibrils ( n  = 12) comparing SL non-uniformities for purely isometric reference contractions (I-state) and contractions following active stretch producing RFE (FE-state). Myofibrils were activated isometrically along the descending limb of the force–length relationship (mean ± 1 standard deviation (SD) = 2.8 ± 0.3 µm sarcomere −1 ). Once the I-state was reached, myofibrils were shortened to an SL on the plateau of the force–length relationship (2.4 µm sarcomere −1 ), and then were actively stretched to the reference length (2.9 ± 0.3 µm sarcomere −1 ). We observed RFE in all myofibrils (39 ± 15%), and saw varying amounts of non-uniformity (1 SD = 0.9 ± 0.5 µm) that was not significantly correlated with the amount of RFE, but through pairwise comparisons was found to be significantly greater than the non-uniformity measured for the I-state (0.7 ± 0.4 µm). Three myofibrils exhibited no increase in non-uniformity. Active stretching was accompanied by sarcomere popping in four myofibrils, and seven had popped sarcomeres in the I-state. These results suggest that, while non-uniformities are present with RFE, they are also present in the I-state. Furthermore, non-uniformity is not associated with the magnitude of RFE, and myofibrils that had no increase in non-uniformity with stretch still showed normal RFE. Therefore, it appears that SL non-uniformity is a normal associate of muscle contraction, but does not contribute to RFE following active stretching of isolated skeletal muscle myofibrils.


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