Impact of lengthening velocity on the generation of eccentric force by slow-twitch muscle fibers in long stretches

Abstract

After an initial increase, isovelocity elongation of a muscle fiber can lead to diminishing (referred to as Give in the literature) and subsequently increasing force. How the stretch velocity affects this behavior in slow-twitch fibers remains largely unexplored. Here, we stretched fully activated individual rat soleus muscle fibers from 0.85 to 1.3 optimal fiber length at stretch velocities of 0.01, 0.1, and 1 maximum shortening velocity, v_max, and compared the results with those of rat EDL fast-twitch fibers obtained in similar experimental conditions. In soleus muscle fibers, Give was 7%, 18%, and 44% of maximum isometric force for 0.01, 0.1, and 1 v_max, respectively. As in EDL fibers, the force increased nearly linearly in the second half of the stretch, although the number of crossbridges decreased, and its slope increased with stretch velocity. Our findings are consistent with the concept of a forceful detachment and subsequent crossbridge reattachment in the stretch's first phase and a strong viscoelastic titin contribution to fiber force in the second phase of the stretch. Interestingly, we found interaction effects of stretch velocity and fiber type on force parameters in both stretch phases, hinting at fiber type-specific differences in crossbridge and titin contributions to eccentric force. Whether fiber type-specific combined XB and non-XB models can explain these effects or if they hint at some not fully understood properties of muscle contraction remains to be shown. These results may stimulate new optimization perspectives in sports training and provide a better understanding of structure-function relations of muscle proteins.

Keywords: Contractile behavior; Give; Skeletal muscle; Soleus; Stretch.

Fig. 1

Exemplary force–length trace obtained in a long isovelocity stretch. Fiber forces are normalized to maximum isometric force, F₀, and fiber length is normalized to optimal fiber length, l_opt. Experiments start with an isometric phase until force achieves a plateau (not shown). Here, the fully activated skinned soleus fiber is then stretched from 0.85 to 1.3 l_opt at 1 maximum fiber contraction velocity. s₂ is the first local force maximum during the stretch. s_g is the local force minimum during the stretch, and Give is the difference between s₂ and s_g. The force at the end of the stretch is s_e. slope₁ and slope₂ are the force slopes resulting from linear regression analysis of the force–length data between the initial isometric force and s₂ and the second half of the stretch, respectively. l_s2 and l_sg are the lengths, where s₂ and s_g occurred. A raw data set for three experiments with different stretch velocities is shown in Figure S1

Fig. 2

Force–length traces of fully activated slow- and fast-twitch fibers during long isovelocity stretches. Total fiber forces (active + passive force), F, are normalized to maximum isometric fiber force, F₀; fiber lengths, l, are normalized to optimal fiber length, l_opt. Ensemble averages (solid lines) and variances (shadowed areas) of active stretch forces and corresponding ensemble averages of passive stretch forces (dashed lines) are shown for stretch velocities of 0.01 (black), 0.1 (blue), and 1 v_max (red). Soleus data (slow-twitch, a) from this study and EDL data (fast-twitch, b) from [85] were obtained under similar experimental conditions. For orientation, figures include a schematic active isometric force–length relationship (gray dashed line). An enlarged section of the region of slope₁ can be found in Figure S2

Fig. 3

Interaction stretch velocity × fiber type on force parameters. Subgroup means (points) and 95% confidence intervals (error bars) are shown. Stretch velocity and fiber type exhibit ordinal interaction on the initial force rise, slope₁ (a); the force slope in the last half of the stretch, slope₂ (d); hybrid interaction (only stretch velocity is interpretable) on the peak force s₂ (b); and disordinal interaction (no main effect is interpretable) on the local force minimum s_g (c). Stretch velocity has a main effect on slope₁, s₂, and slope₂ (a, b, d right). fiber type has a main effect on slope₁ and slope₂ (a, d left). Maximum isometric fiber force, F₀