Altered mechanical interaction between rat plantar flexors due to changes in intermuscular connectivity

Abstract

Connective tissue formation following muscle injury and remedial surgery may involve changes in the stiffness and configuration of the connective tissues linking adjacent muscles. We investigated changes in mechanical interaction of muscles by implanting either a tissue-integrating mesh (n = 8) or an adhesion barrier (n = 8) to respectively increase or decrease the intermuscular connectivity between soleus muscle (SO) and the lateral gastrocnemius and plantaris complex (LG+PL) of the rat. As a measure of mechanical interaction, changes in SO tendon forces and proximal-distal LG+PL force differences in response to lengthening LG+PL proximally were assessed 1 and 2 weeks post-surgery. The extent of mechanical interaction was doubled 1 week post-implantation of the tissue-integrating mesh compared to an unaffected compartment (n = 8), and was more than four times higher 2 weeks post-surgery. This was found only for maximally activated muscles, but not when passive. Implanting the adhesion barrier did not result in a reduction of the mechanical interaction between these muscles. Our findings indicate that the ratio of force transmitted via myofascial, rather than myotendinous pathways, can increase substantially when the connectivity between muscles is enhanced. This improves our understanding of the consequences of connective tissue formation at the muscle boundary on skeletal muscle function.

A lumped stiffness model of intermuscular and extramuscular myofascial pathways of force transmission

“…Surgical procedures for the implantation have been previously reported in detail (Bernabei et al. 2016). Briefly, following preparation for aseptic surgery and inhalation anesthesia (2–3 % isoflurane), the lateral side of the posterior crural compartment was accessed by a partial fasciotomy of the surrounding crural fascia, limiting the exposure of the posterior crural muscles to the proximal two-thirds of the SO and LG muscle-tendon units (MTUs).…”

“…This pathway was divided into a proximal and a distal part with respect to the neurovascular tract, which runs centrally between SO and LG muscle bellies (see Bernabei et al. 2016 for a detailed description). Bundles of connective tissues surrounding blood vessels and nerves reaching the posterior crural muscles can be divided in two main pathways for extramuscular force transmission (Fig.…”

“…2016), here referred as the testing dataset . The experimental protocol used for measuring forces in the testing dataset differed from that used for the calibration dataset .…”

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

“…This could partially explain the limited or no mechanical interaction between muscles when intact muscle compartments and physiological joint excursions in rats and cats hindlimb muscles were tested (Sandercock and Maas, 2009;Tijs et al, 2015b). According to previous studies relating the amount of intermuscularly transmitted force with the active and passive state of muscles (Bernabei et al, 2016a;Tijs et al, 2016b), the largest effects of intermuscular force transmission are expected during the pre-stance and stance phases, when both the LG and SO are active. When the relative position changes between passive muscles, compliant intramuscular structures will likely fully absorb the resulting shear strain and, hence, the strain on intermuscular connections will be minimal.…”

“…Our observed relative displacements and the previously reported minimal mechanical interaction between submaximally activated muscles suggest that during level and upslope trotting, the extent of epimuscular force transmission between ankle plantar-flexors is not significant in healthy rats. This may change in pathological conditions of the musculoskeletal system, such as those caused by muscle injury and surgical interventions, for which enhanced mechanical interactions between muscles have been reported (Bernabei et al, 2016a;Maas and Huijing, 2012).…”