The steady-state isometric force attained after active stretch is greater than that attained in a purely isometric contraction at the corresponding muscle length and activation level. This property is referred to as residual force enhancement (RFE) (1–3). Although RFE is observed across all structural levels, from entire muscles to single sarcomeres (4–8), the molecular mechanisms of RFE remain a matter of debate. The primary mechanisms associated with RFE are (i) sarcomere length instability and associated development of sarcomere length non-uniformities during eccentric contractions (9–11), and (ii) the recruitment of a passive filamentous structures in the sarcomere, with titin often implicated as serving in this role (6,12,13).
Since RFE is induced by active stretch (i.e., eccentric contraction) and is long-lasting (7,14), one might surmise that RFE contributes to the increased work in the shortening phase of stretch-shortening cycles (SSCs), and the increased steady-state force after SSCs (15–17). For example, Cavagna et al. (15) reported that mechanical work performed during muscle shortening was increased in SSCs compared with pure shortening contractions, despite standardization of the force preceding muscle shortening for the two conditions. This result was taken as evidence that RFE may contribute to the increased force in the shortening phase of SSCs (16). However, others reported that the steady-state, isometric force after SSCs was smaller than the corresponding force for corresponding isometric reference forces (18,19). These latter results suggest that the long lasting RFE typically observed for pure eccentric contractions, may be eliminated “instantaneously” by the shortening phase in SSCs. In fact, Herzog et al. (20) reported that the passive force enhancement was eliminated instantaneously by a quick shortening step of sufficient magnitude. The passive force enhancement is the increase in passive force after active stretching of muscle (14). It has been shown to be a major contributor to the RFE for some experimental conditions. Therefore, if the passive force enhancement is indeed abolished by a quick shortening of sufficient magnitude, then one might expect a significant reduction in RFE in SSCs with a quick shortening of sufficient magnitude.
After SSCs, RFE might be reduced compared to pure stretch conditions for at least two reasons: (i) shortening produces a well-known force depression which might offset some of the RFE obtained in the stretch phase of SSCs (1,21,22), and (ii) shortening under certain conditions has been shown to abolish the passive component of the RFE (20). To identify the pure effects of shortening on RFE, without interference of shortening-induced force depression, shortening must occur at speeds exceeding the maximal speed of shortening of the muscle (23–25).
The purpose of this study was to examine the effect of shortening on stretch-induced RFE. To this end, three tests were conducted. The first test was aimed at confirming that quick shortening did not induce residual force depression (RFD). The second and third tests were conducted to examine the effect of shortening on RFE by using quick shortening steps of 1% and 12.5% of fiber length after RFE had been induced by active stretching. Herzog et al. (20) reported that passive force enhancement was eliminated instantaneously by a large but not a small shortening of the muscle. Therefore, we adopted a big strain (12.5%) and a small strain (1%) hypothesizing that the big strain would attenuate stretch-induced RFE, whereas the small strain would not.
MATERIALS AND METHODS
Muscle sample preparation and experimental setup
New Zealand white rabbits were euthanized according to a protocol approved by the University of Calgary’s Life Sciences animal ethics committee. Strips of soleus muscles were harvested and tied to wooden sticks to preserve the in situ sarcomere length. These strips were then placed in a 50% rigor and 50% glycerol solution with protease inhibitors (Complete; Roche Diagnostics, Montreal, Quebec, Canada) to remove the cell membranes. Subsequently, the strips were stored in a freezer at −20°C for 2 to 4 wk. On the day of the experiments, a single fiber of the soleus muscle was isolated under a dissecting microscope using fine forceps (SMZ1500; Nikon, Tokyo, Japan). The isolated fiber was transferred to an experimental chamber (Model 802B; Aurora Scientific, Ontario, Canada) containing a relaxing solution with protease inhibitors. One end of the fiber was attached to a force transducer (Model 400A; Aurora Scientific), the other end to a length controller (Model 308B; Aurora Scientific). Sarcomere length was measured using a He-Ne laser-based diffraction system (1508P-1; JDSU, Milpitas, CA). Fiber length was measured using a microscope (Stemi 2000; Zeiss, Oberkochen, Germany). All experiments were conducted at room temperature (20.5°C ± 0.8°C).
Skinned fibers from rabbit soleus (N = 43) were used for all tests. Three tests were performed with different fibers for each test. Test 1 (N = 13) was conducted to confirm that our quick shortening protocol did not induce RFD. Tests 2 and 3 were conducted to examine if a 1% or 12.5% fiber shortening eliminates the stretch-induced RFE. All tests were performed with active and passive fibers. Because the average fiber length of this experiment was 1.2 ± 0.3 mm (N = 43), the 1% length change corresponded to about 12 μm per fiber or 0.024 μm per sarcomere. Average sarcomere lengths were obtained by measuring sarcomere lengths at a reference length and then linearly extrapolating to a new sarcomere length based on the imposed changes in fiber lengths.
In test 1, the pure shortening trials and the reference isometric trial were conducted as shown in Figure 1. For the pure shortening trial (Fig. 1, blue line), fibers were kept at an average sarcomere length of 2.4 μm, passively stretched to an average sarcomere length of 3.3 μm, and then activated using an activating solution (see solutions). Basically, it takes about 10 s to obtain stable force. Thus, 15 s after the onset of activation, fibers were shortened to an average sarcomere length of 3.0 μm (12.5% of the initial muscle length) in 0.5 ms. Sixteen seconds after the end of shortening, fibers were deactivated using a relaxing solution (see solutions). For the reference isometric trial (Fig. 1, red line), fibers were passively stretched from an average sarcomere length of 2.4 to 3.0 μm, then activated. The duration of the pure shortening contraction and the isometric reference contractions was kept constant.
For test 2 (N = 15), the magnitude of RFE was compared between normal RFE trials (stretch-only trials) and RFE after small shortening trials (SSC with 1% shortening trials). The reference isometric trials were conducted, and the protocol for these trials was the same as that of experiment 1 (Fig. 2, red line). In the stretch-only trial (Fig. 2, blue line, left panel), fibers were initially kept at an average sarcomere length of 2.4 μm, then passively stretched to an average sarcomere length of 2.7 μm, and subsequently activated. Fifteen seconds after the onset of activation, fibers were actively stretched to an average sarcomere length of 3.0 μm (12.5% of the initial muscle length) in 2 s. Sixteen seconds after the end of elongation, fibers were deactivated. In the SSC with 1% shortening trial (Fig. 2, blue line, right panel), fibers were kept at an average sarcomere length of 2.4 μm, then passively stretched to an average sarcomere length of 2.724 μm and activated. Fifteen seconds after the onset of activation, fibers were actively stretched to an average sarcomere length of 3.024 μm (12.5% of the initial muscle length) in 2 s. Immediately after stretching, fibers were shortened to an average sarcomere length of 3.0 μm in 0.5 ms. Sixteen seconds after the end of elongation, fibers were deactivated.
For test 3 (N = 15), the magnitude of RFE was compared between normal RFE trials (stretch-only trials) and RFE after large shortening trials (SSC with 12.5% shortening trials). The reference isometric trials were conducted with respect to the above conditions (Fig. 3). The protocol of reference isometric trial and stretch-only trial were the same with those of test 2. For the SSC with 12.5% shortening trial (Fig. 3, blue line, right panel), fibers were initially held at an average sarcomere length of 2.4 μm, then passively stretched to an average sarcomere length of 3.0 μm and activated. Fifteen seconds after the onset of activation, fibers were actively stretched to an average sarcomere length of 3.3 μm (12.5% of the initial muscle length) in 2 s. Immediately after the end of active stretching, fibers were shortened to an average sarcomere length of 3.0 μm in 0.5 ms. Sixteen seconds after the end of active stretch, muscle fibers were deactivated. A minimum of 2 min of rest was allowed between trials.
All data were collected at a sampling rate of 10,000 Hz. In test 1, active and passive forces attained 15 s after the end of shortening were compared between the pure shortening and the reference isometric tests. In tests 2 and 3, active forces at 15 s after the end of active stretch were compared between the stretch-only/SSC trials and the corresponding reference isometric trials. After active stretching or shortening, there is a time of transient force decline or recovery which in the current preparations and the current protocol took about 10 s. After 10 s, an approximate steady state force was reached, and so we waited for 15 s to make sure a steady-state was reached for all conditions and tests. In addition, the magnitude of RFE was also compared between the stretch-only conditions and the SSC conditions (1% and 12.5% shortening). Finally, the active isometric forces attained before and after the SSC with 12.5% shortening were compared.
The relaxing solution contained (in mM) 170 potassium propionate, 2.5 magnesium acetate, 20 3-(N-morpholino)propanesulfonic acid (MOPS), 5 K2 ethylene glycol-bis(2-aminoethylether)-N,N,N′,N′-tetraacetic acid (EGTA), and 2.5 adenosine triphosphate (ATP), pH 7.0. One tablet of protease inhibitors was added to each 100 mL of relaxing solution. The washing solution contained (in mM) 185 potassium propionate, 2.5 magnesium acetate, 20 MOPS, and 2.5 ATP, pH 7.0. The activating solution contained (in mME) 170 potassium propionate, 2.5 magnesium acetate, 10 MOPS, 2.5 ATP and free Ca2+ buffered with EGTA (CaEGTA and K2EGTA mixed to obtain a pCa value of 4.2), pH 7.0. In addition, the cross-bridge inhibitor, 2,3-butanedione monoxime (BDM) (26) was added (10.0 mM) in the activating solution.
Paired t-tests were used for all statistical analyses using SPSS version 20 (IBM, Tokyo, Japan). The level of significance was set at P < 0.05. All values are presented as means ± SD.
Test 1 (pure shortening trial vs reference isometric trial)
In the passive trials, the passive force at 15 s after the end of shortening in the pure shortening trial (0.043 ± 0.018 mN) was smaller than that measured at the corresponding time point in the reference isometric test (0.066 ± 0.026 mN) (P < 0.001). Because there were small but significant differences in passive force, active force (i.e., total force minus passive force) was used for following all analyses. Active forces at 15 s after the end of the quick shortening in the pure shortening trial (0.526 ± 0.227 mN) were the same as the corresponding forces in the reference isometric trials (0.516 ± 0.216 mN) (P = 0.179) (Fig. 4, left panel). This result was consistent even when the pure shortening test was conducted after the reference isometric test (P = 0.602) (Fig. 4, right panel).
Tests 2 and 3 (stretch-only condition vs SSC condition)
The active forces at 15 s after the end of active stretch in the stretch only and SSC with 1% shortening tests were greater than the corresponding forces attained in the reference isometric tests, for both, the stretch-only condition (P < 0.001) and the SSC with 1% shortening condition (P < 0.001). The magnitude of RFE was the same for the stretch only (7.9% ± 2.7%) and the SSC with 1% shortening (7.1 ± 2.9) conditions (P = 0.316) (Fig. 5, left panel).
In test 3, active forces at 15 s after the end of active stretch in the stretch only and SSC with 12.5% shortening tests were greater than the corresponding forces attained in the reference isometric conditions for both, the stretch only (P < 0.001) and the SSC with 12.5% shortening conditions (P < 0.001). However, in contrast to the results in test 2, RFE was significantly greater for the stretch only (8.4% ± 2.5%) than the SSC with 12.5% shortening (3.5% ± 2.4%) condition (P < 0.001) (Fig. 5, right panel). The isometric forces after the SSC (0.437 ± 0.103 mN) were greater than those measured before the SSC (0.422 ± 0.104 mN) (P = 0.016) (Fig. 6).
The purpose of this study was to examine whether active muscle shortening eliminates the stretch-induced RFE. A quick shortening step was used to eliminate the confounding effect of RFD in a slow shortening step. We confirmed that quick shortening did not induce RFD (Fig. 4), as had been observed before (27). Therefore, if stretch-induced RFE is decreased or even eliminated by quick shortening, the mechanisms underlying this loss of force are not caused by shortening-induced RFD. For quick shortening of 1% of fiber length, RFE was not decreased. However, for the 12.5% shortening steps, the stretch-induced RFE was significantly decreased. Based on these observations, we suggest that the magnitude of RFE decreases in SSCs when the magnitude of shortening is substantial.
Is RFD induced by quick shortening?
The quick shortening steps did not produce RFD, as expected from the relationship between RFD and mechanical work (stress imposed on the actin filament) (24,25). RFD is thought to be associated with a decrease in the proportion of attached cross-bridges, possibly due to a decrease in the cross-bridge attachment rates after active shortening, which in turn, has been speculated to be caused by a stress-induced deformation of actin filaments (21). This deformation is thought to inhibit the interaction between actin and myosin, which leads to the decreased isometric force after shortening, that is, RFD (1,28). Since the duration of our quick shortening (0.5 ms) should be shorter on average than the duration of the strongly bound cross-bridge state (29), the attached cross-bridges become slack during the quick shortening step (and then, they are forcibly detached from the actin filament when the shortening magnitude becomes larger than the working range of myosin head). Therefore, we would expect that the attached cross-bridges do not produce force or work (or at best a negligible amount) during shortening, thus minimizing any potential RFD (28). This expectation was supported in this study, which is also consistent with results found by Herzog and Leonard (27) in isolated cat soleus muscle. Therefore, we concluded that our experimental protocol did not induce RFD, and consequently, we could examine the influence of shortening amplitude on RFE separately from the influence of RFD on RFE.
Influence of shortening on the RFE
In experiments 2 and 3, we examined the influence of different magnitudes of shortening in SSCs on RFE. When the magnitude of shortening was small, RFE was not decreased (Fig. 5, left panel). This result is consistent with a previous study in which a small, quick shortening step did not reduce the stretch-induced RFE (2). However, using a large shortening step, RFE was decreased compared to the RFE obtained when muscle stretching was not followed by shortening (Fig. 5, right panel), suggesting that RFE is partly eliminated by muscle shortening if the shortening magnitude is sufficiently large. However, before reaching a firm conclusion, we must consider the difference in the stretching protocols between the stretch-only and the SSC trials. In experiment 2, fibers were stretched from an average sarcomere length of 2.7 to 3.0 μm in the stretch-only condition, but were stretched from 2.724 to 3.024 μm in the SSC condition to standardize the final isometric fiber length (i.e., 3.0 μm) following the 1% (0.024 μm per sarcomere) shortening step. However, this difference between the two trials is negligibly small, and thus, would likely not have affected the magnitude of the RFE. In experiment 3, fibers were stretched from an average sarcomere length of 3.0 to 3.3 μm. The absolute amount of RFE is related to the magnitude of active stretching (30–32) and the final length after active stretching (33,34). The magnitude of stretching was identical (i.e., 0.3 μm) between the stretch-only and the SSC trials, but the final length was different (3.0 μm vs 3.3 μm). This protocol was required as we wanted to compare the isometric steady-state forces after pure stretch contractions and the SSCs at the same sarcomere length (i.e., 3.0 μm). However, we assumed that the RFE obtained when stretching fibers from 2.7 to 3.0 μm would be similar to stretching them from 3.0 to 3.3 μm because the final muscle length where RFE was calculated (i.e., 15 s after the end of length changes) was the same (3.0 μm). Likely, the RFE was slightly greater when stretching fibers to 3.3 rather than 3.0 μm, but even if this was the case, the final conclusions would remain unchanged. Our conclusion is consistent with that of Herzog and Leonard (20) who reported that passive force enhancement, which is considered be caused by the similar mechanism, titin, was decreased by muscle shortening in a magnitude-dependent manner (20). Here we have tacitly assumed that shortening or stretch of the skinned fibers is associated with a corresponding shortening and stretch of the mean sarcomere length. Because there is compliance in the system, it is possible that shortening and stretching of the fibers are associated with (likely smaller) different changes in mean sarcomere length. Furthermore, single fibers are known to have nonuniform sarcomere lengths (35), and it is impossible at this time to know the changes in sarcomere length non-uniformities associated with the SSC protocol used in this study. This remains a limitation but should not detract from the general results of this study that larger shortening magnitudes attenuate RFE independent of non-uniformities in sarcomere length.
Contribution of RFE to increased SSC performance
Because RFE was eliminated to some extent by shortening (Fig. 5), its effect in SSC needs to be carefully reconsidered. In the RFE after 12.5% shortening trials, the isometric active forces attained after SSCs were slightly (3.6%) but significantly (P = 0.016) greater than the isometric forces attained before SSCs at the corresponding sarcomere length (i.e., 3.0 μm) (Fig. 6). This result indicates that RFE still existed after shortening, suggesting that RFE can contribute to the increased force and work in the shortening phase of SSCs compared to the force and work of purely concentric contractions as suggested by Seiberl et al. (16).
Results from previous studies on the steady-state forces after SSCs are contradictory. For example, Herzog and Leonard (18), Brown and Loeb (19), and Lee et al. (36) reported that the isometric forces after SSCs were smaller than the corresponding (same length and same activation) isometric reference forces, and were similar to the depressed forces after pure shortening experiments. These results suggested that the RFE was completely abolished by shortening in these whole muscle experiments. Fukutani et al (37) also reported that RFE was completely eliminated after shortening in human ankle plantar flexor muscles. However, Seiberl et al. (16) and Fortuna et al. (38) found that joint torques attained after SSCs were larger than the torques obtained for pure shortening contractions, indicating that RFE was not fully abolished by shortening. One reason for the inconsistency among studies may be associated with differences in the shortening magnitude. Here, we demonstrated that RFE decreases when the magnitude of shortening was large. In addition, Fortuna et al. (38) suggests that the timing of shortening should be considered. Another reason might be the region of the force–length relationship where testing is performed, since the magnitude of RFE is known to depend on the final muscle length (2,33,34). For example, no RFE was observed after SSCs when the final muscle length was on the ascending limb (18,37) or plateau region of the force–length relationship (19,36). In agreement with this speculation are findings by Ettema et al. (39) who reported that isometric forces after SSCs were greater than those found after pure shortening when the final muscle length was greater than optimal, but this enhancement of force was not present when the final muscle length was on the ascending limb of the force–length relationship.
We found that some fibers did not show RFE after SSCs. One of the reasons for this variation would be the natural variation. In addition to the natural variation, there is a possibility that this variation might be caused by damage induced during the eccentric phase of the SSCs that may have masked the effects of the RFE.
Many human movements include SSCs. However, stretching of the muscle tendon unit may not be associated with stretching of the muscle fascicles, and thus the contractile elements (40). Since fascicle elongation is likely needed to induce RFE, fascicle lengths during SSCs should be measured carefully to clarify if RFE can contribute to the SSCs in human. Thus, studies will need to be conducted that examine RFE and force depression in entire muscle tendon units while simultaneously measuring and manipulating fascicle dynamics. Such studies might provide some insight into the role of SSCs on RFE in everyday human movements. In addition, RFE during SSCs may differ among muscles because the magnitude of history-dependent effects is related to the fiber type (41). For example, fast twitch fibers that are shortened at the same absolute speed as a corresponding (same length) slow twitch fiber, will produce more work during shortening (due to its slower relative speed of shortening), and thus show more force depression (41). Considering the fact that fiber type distribution varies within all major human limb muscles, this point should be considered when analyzing human movements.
We conclude from the findings of this study that when the magnitude of shortening is small (1% of fiber length), RFE is fully preserved, while when the magnitude of shortening is large (12.5% of fiber length), RFE is attenuated and these observations are not caused by shortening-induced RFD. The molecular mechanisms at play in the elimination of RFE by shortening need explanation.
This study was supported by a Grant-in-Aid for Challenging Exploratory Research (16K13009) and a Postdoctoral Fellowship for Research Abroad (183), Nakatomi Foundation, CIHR, NSERC of Canada, The Canada Research Chair Programme, and the Killam Foundation. The results of the present study do not constitute an endorsement by the American College of Sports Medicine. The authors declare that the results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation.
Conflicts of interest: None.
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