Significant mechanical interactions at physiological lengths and relative positions of rat plantar flexors

Abstract

In situ studies involving supraphysiological muscle lengths and relative positions have shown that connective tissue linkages connecting adjacent muscles can transmit substantial forces, but the physiological significance is still subject to debate. The present study investigates effects of such epimuscular myofascial force transmission in the rat calf muscles. Unlike previous approaches, we quantified the mechanical interaction between the soleus (SO) and the lateral gastrocnemius and plantaris complex (LG+PL) applying a set of muscle lengths and relative positions corresponding to the range of knee and ankle angles occurring during normal movements. In nine deeply anesthetized Wistar rats, the superficial posterior crural compartment was exposed, and distal and proximal tendons of LG+PL and the distal SO tendon were severed and connected to force transducers. The target muscles were excited simultaneously. We found that SO active and passive tendon force was substantially affected by proximally lengthening of LG+PL mimicking knee extension (10% and 0.8% of maximal active SO force, respectively; P < 0.05). Moreover, SO relative position significantly changed the LG+PL length-force relationship, resulting in nonunique values for passive slack-length and optimum-length estimates. We conclude that also, for physiological muscle conditions, isometric force of rat triceps surae muscles is determined by its muscle-tendon unit length as well as by the length and relative position of its synergists. This has implications for understanding the neuromechanics of skeletal muscle in normal and pathological conditions, as well as for studies relying on the assumption that muscles act as independent force actuators.

Longitudinal and transversal displacements between triceps surae muscles during locomotion of the rat

“…The second pathway contains branches of the popliteal artery and tibial nerve running from the popliteal fossa to the proximal-dorsal surface of LG and MG muscle bellies. In situ, mechanical interaction between SO and LG of the rat has been reported (Bernabei et al, 2015) for a range of MTU length changes (6 mm), which were consistent with the ones estimated in this study (7.2 and 6.4 mm for LG and SO, respectively; Fig. 6A).…”

“…6A). However, in the study by Bernabei et al (2015), both muscles were maximally activated, while the extent of mechanical interaction has been shown to decrease with submaximal activation and passive muscle conditions (Tijs et al, 2015a(Tijs et al, , 2016a. Moreover, the maximal MTU relative displacement imposed in the study by Bernabei et al LG proximal tendon is detached from its origin on the lateral epicondyle of the femur to show the intermuscular connective tissues and SO muscle belly lying more anterior in the triceps surae compartment.…”

“…Such anatomical and morphological organization can have consequences for muscle mechanics. When manipulating the relative position of muscle-tendon units (MTUs) within a physiological range in situ, mechanical interaction between the SO and LG was found (Bernabei et al, 2015). Previous studies have investigated the activation and length changes of the triceps surae muscles in vivo Wakeling, 2007, 2008), yet muscle relative displacements have not been measured.…”

Limited mechanical effects of intermuscular myofascial connections within the intact rat anterior crural compartment

“…This may be advantageous for accurate control of ankle joint stability. This seems to be in contrast to a recent study showing that lengthening gastrocnemius and plantaris muscles proximally, simulating knee extension, increased the force exerted at the distal tendon of soleus muscle significantly (Bernabei et al, 2015). However, because ankle plantar-flexors have largely comparable lines of action (Tijs et al, 2014), the presence of myofascial force transmission will not affect the functional output at the joint.…”

“…Although tissue deformations indicate effects of myofascial force transmission, the applied imaging techniques cannot provide a direct measure of the mechanical effects at the tendon or joint. A study that did assess the mechanical effect at the tendon reported sizable epimuscular myofascial force transmission between active rat ankle plantarflexor muscles for a physiological range of muscle lengths and relative muscle positions (Bernabei et al, 2015). In contrast, ankle moments exerted by soleus muscle in rats (Tijs et al, 2015a) and cats (Maas and Sandercock, 2008) were not affected by length changes of passive synergists, as imposed by changes in knee angle.…”