Michel Bernabei

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

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.

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

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

Mechanical behavior of skeletal muscles is commonly modeled under the assumption of mechanical independence between individual muscles within a muscle group. Epimuscular myofascial force transmission via the connective tissue network surrounding a muscle challenges this assumption as it alters the force distributed to the tendons of individual muscles. This study aimed to derive a lumped estimate of stiffness of the intermuscular and extramuscular connective tissues and to assess changes in such stiffness in response to a manipulation of the interface between adjacent muscles. Based on in situ measurements of force transmission in the rat plantar flexors, before and after resection of their connective tissue network, a nonlinear estimate of epimuscular myofascial stiffness was quantified and included in a multi-muscle model with lumped parameters which allows for force transmission depending on the relative position between the muscles in the group. Such stiffness estimate was assessed for a group with normal intermuscular connective tissues and for a group with increased connectivity, mimicking scar tissue development. The model was able to successfully predict the amount of epimuscular force transmission for different experimental conditions than those used to obtain the model parameters. The proposed nonlinear stiffness estimates of epimuscular pathways could be integrated in larger musculoskeletal models, to provide more accurate predictions of force when effects of mechanical interaction or altered epimuscular connections, e.g. after surgery or injury, are substantial.

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

ABSTRACT The functional consequences of differential muscle activation and contractile behavior between mechanically coupled synergists are still poorly understood. Even though synergistic muscles exert similar mechanical effects at the joint they span, differences in the anatomy, morphology and neural drive may lead to non-uniform contractile conditions. This study aimed to investigate the patterns of activation and contractile behavior of triceps surae muscles, to understand how these contribute to the relative displacement between the one-joint soleus (SO) and two-joint lateral gastrocnemius (LG) muscle bellies and their distal tendons during locomotion in the rat. In seven rats, muscle belly lengths and muscle activation during level and upslope trotting were measured by sonomicrometry crystals and electromyographic electrodes chronically implanted in the SO and LG. Length changes of muscle–tendon units (MTUs) and tendon fascicles were estimated based on joint kinematics and muscle belly lengths. Distances between implanted crystals were further used to assess longitudinal and transversal deformations of the intermuscular volume between the SO and LG. For both slope conditions, we observed differential timing of muscle activation as well as substantial differences in contraction speeds between muscle bellies (maximal relative speed 55.9 mm s−1). Muscle lengths and velocities did not differ significantly between level and upslope locomotion, only EMG amplitude of the LG was affected by slope. Relative displacements between SO and LG MTUs were found in both longitudinal and transversal directions, yielding an estimated maximal length change difference of 2.0 mm between their distal tendons. Such relative displacements may have implications for the force exchanged via intermuscular and intertendinous pathways. Summary: Differences in anatomy, morphology and neural drive between rat ankle plantar-flexors cause substantial intermuscular displacement during locomotion, which may affect mechanical interactions between muscle bellies and tendons.

Non-uniform displacement and strain between the soleus and gastrocnemius subtendons of rat Achilles tendon

Achilles tendon (AT) comprises of 3 subtendons arising from the soleus (SOL) and the lateral (LG) and medial (MG) heads of the gastrocnemius muscle. While recent human studies show differential displacement within AT, these displacements have not been attributed to specific subtendons. We tested the hypothesis that the SOL and LG subtendons show differential displacement and strain during various combinations of SOL, LG, and MG excitations. Movement of knots, sutured onto SOL and LG subtendons of 12 Wistar rats, was videotaped, while the muscles were stimulated intramuscularly and ankle torque was assessed. When SOL only was stimulated, the plantar flexion torque was the smallest among the different conditions (P < .001). In this condition, from passive to active state, the displacement (0.57 vs 0.47 mm, P = .002) and strain (8.4% vs 2.4%, P < .001) in the SOL subtendon were greater than in LG subtendon. When LG only was stimulated, a higher ankle torque was measured as compared to SOL stimulation (P < .001); the displacement was similar in both subtendons (~0.6 mm), while the strain was greater in LG than in SOL (4.7% vs 1.7%, P < .001). When all 3 muscles were stimulated simultaneously, ankle torque was highest and the displacement (0.79 vs 0.74 mm, P = .002) and strain (7.7% vs 4.4%, P = .003) were greater in SOL than in LG. These data show that the different subtendons of AT can experience relative displacement and differential strains. Together with anatomical dissections, the results revealed that such uniformities may be due to a lower stiffness of SOL subtendon compared to LG.

Myofascial Loads Can Occur without Fascicle Length Changes

Many studies have shown that connective tissue linkages can transmit force between synergistic muscles and that such force transmission depends on the position of these muscles relative to each other and on properties of their intermuscular connective tissues. Moving neighboring muscles has been reported to cause longitudinal deformations within passive muscles held at a constant muscle-tendon unit (MTU) length (e.g., soleus [SO]), but muscle forces were not directly measured. Deformations do not provide a direct measure of the force transmitted between muscles. We combined two different muscle preparations to assess whether myofascial loads exerted by neighboring muscles result in length changes of SO fascicles. We investigated the effects of proximal MTU length changes of two-joint gastrocnemius (GA) and plantaris (PL) muscles on the fascicle length of the one-joint SO muscle within (1) an intact muscle compartment and (2) a disrupted compartment that allowed measurements of fascicle length and distal tendon force of SO simultaneously. SO muscle bellies of Wistar rats (n = 5) were implanted with sonomicrometry crystals. In three animals, connectivity between SO and GA+PL was enhanced. Measurements were performed before and during maximal excitation of all plantar flexor muscles. In both setups, MTU length of GA+PL did not affect the length of SO fascicles, neither during passive nor active conditions. However, lengthening the MTU of GA+PL increased distal tendon force of SO by 43.3-97.8% (P < 0.001) and 27.5-182.6% (P < 0.001), respectively. This indicates that substantial myofascial force transmission between SO and synergistic muscle can occur via a connective tissue network running parallel to the series of SO sarcomeres without substantial length changes of SO fascicles.