Adaptation of muscle size and myofascial force transmission: a review and some new experimental results

This paper considers the literature and some new experimental results important for adaptation of muscle fiber cross-sectional area and serial sarcomere number. Two major points emerge: (1) general rules for the regulation of adaptation (for in vivo immobilization, low gravity conditions, synergist ablation, tenotomy and retinaculum trans-section experiments) cannot be derived. As a consequence, paradoxes are reported in the literature. Some paradoxes are resolved by considering the interaction between different levels of organization (e.g. muscle geometrical effects), but others cannot. (2) An inventory of signal transduction pathways affecting rates of muscle protein synthesis and/or degradation reveals controversy concerning the pathways and their relative contributions. A major explanation for the above is not only the inherently limited control of the experimental conditions in vivo, but also of in situ experiments. Culturing of mature single Xenopus muscle fibers at high and low lengths (allowing longitudinal study of adaptation for periods up to 3 months) did not yield major changes in the fiber cross-sectional area or the serial sarcomere number. This is very different from substantial effects (within days) of immobilization in vivo. It is concluded that overall strain does not uniquely regulate muscle fiber size. Force transmission, via pathways other than the myotendinous junctions, may contribute to the discrepancies reported: because of substantial serial heterogeneity of sarcomere lengths within muscle fibers creating local variations in the mechanical stimuli for adaptation. For the single muscle fiber, mechanical signalling is quite different from the in vivo or in vitro condition. Removal of tensile and shear effects of neighboring tissues (even of antagonistic muscle) modifies or removes mechanical stimuli for adaptation. It is concluded that the study of adaptation of muscle size requires an integrative approach taking into account fundamental mechanisms of adaptation, as well as effects of higher levels of organization. More attention should be paid to adaptation of connective tissues within and surrounding the muscle and their effects on muscular properties. Copyright © Blackwell Munksgaard 2005

Myofascial force transmission causes interaction between adjacent muscles and connective tissue: Effects of blunt dissection and compartmental fasciotomy on length force characteristics of rat extensor digitorum longus muscle

Muscles within the anterior tibial compartment (extensor digitorum longus: EDL. tibialis anterior: TA, and extensor hallucis longus muscles: EHL) and within the peroneal compartment were excited simultaneously and maximally. The ankle joint was fixed kept at 90°. For EDL length force characteristics were determined. This was performed first with the anterior tibial compartment intact (1), and subsequently after: (2) blunt dissection of the anterior and lateral interface of EDL and TA. (3) Full longitudinal lateral fasciotomy of the anterior tibial compartment. (4) Full removal of TA and EHL muscles. Length-force characteristics were changed significantly by these interventions. Blunt dissection caused a force decrease of approximately 10% at all lengths, i.e., without changing EDL optimum or active slack lengths. This indicates that intermuscular connective tissue mediates significant interactions between adjacent muscles. Indications of its relatively stiff mechanical properties were found both in the physiological part of the present study, as well as the anatomical survey of connective tissue. Full lateral compartmental fasciotomy increased optimum length and decreased active slack length, leading to an increase of length range (by ≈47%). while decreasing optimal force. As a consequence an increase in force for the lower length range was found. Such changes of length force characteristics are compatible with an increased distribution of fiber mean sarcomere length. On the basis of these results, it is concluded that extramuscular connective tissue has a sufficiently stiff connection to intramuscular connective tissue to be able to play a role in force transmission. Therefore, in addition to intramuscular myofascial force transmission, extramuscular force transmission has to be considered within intact compartments of limbs. A survey of connective tissue structures within the compartment indicated sheet-like neuro-vascular tracts to be major components of extramuscular connective tissue with connections to intramuscular connective tissue stroma. Removal of TA and EHL yielded yet another decrease of force (mean for optimal force ≈10%). No significant changes of optimum and active slack lengths could be shown in this case. It is concluded that myofascial force transmission should be taken into account when considering muscular function and its coordination, and in clinical decisions regarding fasciotomy and repetitive strain injury

Finite element modeling of aponeurotomy: altered intramuscular myofascial force transmission yields complex sarcomere length distributions determining acute effects

Finite element modeling of aponeurotomized rat extensor digitorium longus muscle was performed to investigate the acute effects of proximal aponeurotomy. The specific goal was to assess the changes in lengths of sarcomeres within aponeurotomized muscle and to explain how the intervention leads to alterations in muscle length–force characteristics. Major changes in muscle length–active force characteristics were shown for the aponeurotomized muscle modeled with (1) only a discontinuity in the proximal aponeurosis and (2) with additional discontinuities of the muscles’ extracellular matrix (i.e., when both myotendinous and myofascial force transmission mechanisms are interfered with). After muscle lengthening, two cut ends of the aponeurosis were separated by a gap. After intervention (1), only active slack length increased (by approximately 0.9 mm) and limited reductions in muscle active force were found (e.g., muscle optimum force decreased by only 1%) After intervention (2) active slack increased further (by 1.2 mm) and optimum length as well (by 2.0 mm) shifted and the range between these lengths increased. In addition, muscle active force was reduced substantially (e.g., muscle optimum force decreased by 21%). The modeled tearing of the intramuscular connective tissue divides the muscle into a proximal and a distal population of muscle fibers. The altered force transmission was shown to lead to major sarcomere length distributions [not encountered in the intact muscle and after intervention (1)], with contrasting effects for the two muscle fiber populations: (a) Within the distal population (i.e. fibers with no myotendinous connection to the muscles’ origin), sarcomeres were much shorter than within the proximal population (fibers with intact myotendinous junction at both ends). (b) Within the distal population, from proximal ends of muscle fibers to distal ends, the serial distribution of sarcomere lengths ranged from the lowest length to high lengths. In contrast within the proximal population, the direction of the distribution was reversed. Such differences in distribution of sarcomere lengths between the proximal and distal fiber populations explain the shifts in muscle active slack and optimal lengths. Muscle force reduction after intervention (2) is explained primarily by the short sarcomeres within the distal population. However, fiber stress distributions showed contribution of the majority of the sarcomeres to muscle force: myofascial force transmission prevents the sarcomeres from shortening to nonphysiological lengths. It is concluded that interfering with the intramuscular myofascial force transmission due to rupturing of the intramuscular connective tissue leads to a complex distribution of sarcomere lengths within the aponeurotomized muscle and this determines the acute effects of the intervention on muscle length–force characteristics rather than the intervention with the myotendinous force transmission after which the intervention was named. These results suggest that during surgery, but also postoperatively, major attention should be focused on the length and activity of aponeurotomized muscle, as changes in connective tissue tear depth will affect the acute effects of the intervention

Twitch and tetanic tension during culture of mature Xenopus laevis single muscle fibres

Investigation of the mechanisms of muscle adaptation requires independent control of the regulating factors. The aim of the present study was to develop a serum-free medium to culture mature single muscle fibres of Xenopus laevis. As an example, we used the culture system to study adaptation of twitch and tetanic force characteristics, number of sarcomeres in series and fibre cross-section. Fibres dissected from m. iliofibularis (n = 10) were kept in culture at a fibre mean sarcomere length of 2.3 µm in a culture medium without serum. Twitch and tetanic tension were determined daily. Before and after culture the number of sarcomeres was determined by laser diffraction and fibre cross-sectional area (CSA) was determined by microscopy. For five fibres twitch tension increased during culture and tetanic tension was stable for periods varying from 8 to 14 days (‘stable fibres’), after which fibres were removed from culture for analysis. Fibre CSA and the number of sarcomeres in series remained constant during culture. Five other fibres showed a substantial reduction in twitch and tetanic tension within the first five days of culture (‘unstable fibres’). After 7–9 days of culture, three of these fibres died. For two of the unstable fibres, after the substantial force reduction, twitch and tetanic tension increased again. Finally at day 14 and 18 of culture, respectively, the tensions attained values higher than their original values. For stable fibres, twitch contraction time, twitch half-relaxation time and tetanus 10%-relaxation time increased during culture. For unstable fibres these parameters fluctuated. For all fibres the stimulus threshold fluctuated during the first two days, and then remained constant, even for the fibres that were cultured for at least two weeks. It is concluded that the present culture system for mature muscle fibres allows long-term studies within a well-defined medium. Unfortunately, initial tetanic and twitch force are poor predictors of the long-term behaviour of the fibres