Guus C. Baan

Intermuscular interaction via myofascial force transmission: effects of tibialis anterior and extensor hallucis longus length on force transmission from rat extensor digitorum longus muscle

Force transmission in rat anterior crural compartment, containing tibialis anterior (TA), extensor hallucis longus (EHL) and extensor digitorum longus (EDL) muscles, was investigated. These muscles together with the muscles of the peroneal compartment were excited maximally. Force was measured at both proximal and distal tendons of EDL muscle as well as at the tied distal tendons of TA and EHL muscles (the TA + EHL complex). Effects of TA + EHL complex length and force on proximally and distally measured forces of EDL muscle kept at constant muscle-tendon complex length were assessed. Length changes of EDL muscle were imposed by movement of the proximal force transducer to different positions.Proximal EDL force was unequal to distal EDL force (active as well as passive) over a wide range of EDL muscle-tendon complex lengths. This is an indication that force is also transmitted out of EDL muscle via pathways other than the tendons (i.e. inter- and/or extramuscular myofascial force transmission). At constant low EDL length, distal lengthening of the TA + EHL complex increased proximal EDL force and decreased distal EDL force. At optimum EDL length, TA+EHL active force was linearly related to the difference between proximal and distal EDL active force. These results indicate intermuscular myofascial force transmission between EDL muscle and the TA + EHL complex. The most likely pathway for this transmission is via connections of the intact intermuscular connective tissue network. The length effects of the TA + EHL complex can be understood on the basis of changes in the configuration, and consequently the stiffness, of these connections. Damage to connective tissue of the compartment decreased the proximo-distal EDL force difference, which indicates the importance of an intact connective tissue network for force transmission from muscle fibers to bone.

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.

Muscle force is determined also by muscle relative position: isolated effects.

Effects on force of changes of the position of extensor digitorum longus muscle (EDL) relative to surrounding tissues were investigated in rat. Connective tissue at the muscle bellies of tibialis anterior (TA), extensor hallucis longus (EHL) and EDL was left intact, to allow myofascial force transmission. The position of EDL muscle was altered, without changing EDL muscle-tendon complex length, and force exerted at proximal and distal tendons of EDL as well as summed force exerted at the distal tendons of TA and EHL muscles (TA+EHL) were measured. Proximal and distal EDL forces as well as distal TA+EHL force changed significantly on repositioning EDL muscle. These muscle position-force characteristics were assessed at two EDL lengths and two TA+EHL lengths. It was shown that changes of muscle force with length changes of a muscle is the result of the length changes per se, as well as of changes of relative position of parts of the muscle. It is concluded that in addition to length, muscle position relative to its surroundings co-determines isometric muscle force.

The relative position of EDL muscle affects the length of sarcomeres within muscle fibers: experimental results and finite-element modeling.

BACKGROUND Effects of extramuscular connective tissues on muscle force (experimentally measured) and lengths of sarcomeres (modeled) were investigated in rat. It was hypothesized that changes of muscle-relative position affect the distribution of lengths of sarcomeres within muscle fibers. METHOD OF APPROACH The position of extensor digitorum longus muscle (EDL) relative to intact extramuscular connective tissues of the anterior crural compartment was manipulated without changing its muscle-tendon complex length. RESULTS Significant effects of EDL muscle relative position on proximal and distal EDL forces were found, indicating changes of extramuscular myofascial force transmission. EDL isometric force exerted at its proximal and distal tendons differed significantly. Finite-element modeling showed that the distribution of lengths of sarcomeres is altered by changes of muscle-relative position. CONCLUSIONS It is concluded that forces exerted on a muscle via extramuscular myofascial pathways augment distributions of lengths of sarcomeres within that muscle.

From Twitch to tetanus: Performance of excitation dynamics optimized for a twitch in predicting tetanic muscle forces

Abstract. In models of the excitation of muscles it is often assumed that excitation during a tetanic contraction can be obtained by the linear summation of responses to individual stimuli from which the active state of the muscle is calculated. The purpose of this study was to investigate whether such a model adequately describes the process of excitation of muscle. Parameters describing the contraction dynamics of the muscle model used were derived from physiological and morphological measurements made on the gastrocnemius medialis muscle of three adult Wistar rats. Parameters pertaining to the excitation dynamics were optimized such that the muscle model correctly predicted force histories recorded during an isometric twitch. When a relationship between intracellular calcium and active state from literature on rat muscle was used, the muscle model was capable of generating force histories at stimulation frequencies of 20, 40, 60 and 80 Hz and other muscle-tendon complex lengths which closely matched those measured experimentally – albeit forces were underestimated slightly in all cases. Differences in responses to higher stimulation frequencies between animals could be traced back to differences in twitch dynamics between the animals and adequate predictions of muscle forces were obtained for all animals. These results suggest that the linear summation of responses to individual stimuli indeed gives an adequate description of the excitation of muscle.

IMPLICATIONS OF MUSCLE RELATIVE POSITION AS A CO-DETERMINANT OF ISOMETRIC MUSCLE FORCE: A REVIEW AND SOME EXPERIMENTAL RESULTS

Force is transmitted from muscle fiber to bone via several pathways: (1) via the tendons (i.e. myotendinous force transmission), (2) via intermuscular connective tissue to adjacent muscles (i.e. intermuscular myofascial force transmission), (3) via structures other than muscles (i.e. extramuscular myofascial force transmission). In vivo, the position of a muscle relative to adjacent muscles changes due to differences in moment arm between synergists as well as due to the fact that some muscles span only one joint and other muscles more than one joint. The position of a muscle relative to non-muscular structures within a compartment is altered with each change of the length of the muscle. The aim of this article is to describe recent experimental results, as well as some new experimental data, that have elucidated the role of muscle relative position on force transmission from muscle. Furthermore, relevant literature is discussed, taking into consideration these new insights of muscle functioning. It is concluded that the position of a muscle relative to surrounding tissues is a major co-determinant of isometric muscle force. For muscles operating within their in vivo context of connective tissue, such position effects should be taken into account.

Pre-Strained Epimuscular Connections Cause Muscular Myofascial Force Transmission to Affect Properties of Synergistic EHL and EDL Muscles of the Rat

BACKGROUND Myofascial force transmission occurs between muscles (intermuscular myofascial force transmission) and from muscles to surrounding nonmuscular structures such as neurovascular tracts and bone (extramuscular myofascial force transmission). The purpose was to investigate the mechanical role of the epimuscular connections (the integral system of inter- and extramuscular connections) as well as the isolated role of extramuscular connections on myofascial force transmission and to test the hypothesis, if such connections are prestrained. METHOD OF APPROACH Length-force characteristics of extensor hallucis longus (EHL) muscle of the rat were measured in two conditions: (I) with the neighboring EDL muscle and epimuscular connections of the muscles intact: EDL was kept at a constant muscle tendon complex length. (II) After removing EDL, leaving EHL with intact extramuscular connections exclusively. RESULTS (I) Epimuscular connections of the tested muscles proved to be prestrained significantly. (1) Passive EHL force was nonzero for all isometric EHL lengths including very low lengths, increasing with length to approximately 13% of optimum force at high length. (2) Significant proximodistal EDL force differences were found at all EHL lengths: Initially, proximal EDL force = 1.18 +/- 0.11 N, where as distal EDL force = 1.50 +/- 0.08 N (mean +/- SE). EHL lengthening decreased the proximo-distal EDL force difference significantly (by 18.4%) but the dominance of EDL distal force remained. This shows that EHL lengthening reduces the prestrain on epimuscular connections via intermuscular connections; however; the prestrain on the extramuscular connections of EDL remains effective. (II) Removing EDL muscle affected EHL forces significantly. (1) Passive EHL forces decreased at all muscle lengths by approximately 17%. However, EHL passive force was still non-zero for the entire isometric EHL length range, indicating pre-strain of extramuscular connections of EHL. This indicates that a substantial part of the effects originates solely from the extramuscular connections of EHL. However, a role for intermuscular connections between EHL and EDL, when present, cannot be excluded. (2) Total EHL forces included significant shape changes in the length-force curve (e.g., optimal EHL force decreased significantly by 6%) showing that due to myofascial force transmission muscle length-force characteristics are not specific properties of individual muscles. CONCLUSIONS The pre-strain in the epimuscular connections of EDL and EHL indicate that these myofascial pathways are sufficiently stiff to transmit force even after small changes in relative position of a muscle with respect to its neighboring muscular and nonmuscular tissues. This suggests the likelihood of such effects also in vivo.

Extramuscular myofascial force transmission for in situ rat medial gastrocnemius and plantaris muscles in progressive stages of dissection

SUMMARY The aim of this study was to establish the extent of extramuscular myofascial force transmission for dissected rat medial gastrocnemius (GM) and plantaris (PL) muscles. Initially, this was done with GM still connected to extramuscular connective tissue (general fascia, neuro-vascular tract and compartmental fascia). Neighbouring muscles were also connected to these tissues. In a later stage, it was dissected progressively until finally a fully dissected in situ GM was obtained, for which the neuro-vascular tract (i.e. the nerves, bloodvessels and the surrounding connective tissue) was the only extramuscular tissue left intact. Force of GM was measured not only at its distal tendon in progressive stages of dissection, but also at its dissected proximal tendon. In the stage where GM was still connected to extramuscular tissues, the experiments showed that up to 40.5±5.9% (mean ± s.e.m.) of the force exerted by the neighbouring PL muscle was transmitted onto the calcaneal bone, even when the PL tendon was not connected to this bone. After distal PL-tenotomy, a difference between proximally and distally measured forces of GM constituted evidence for myofascial force transmission. In the fully dissected in situ GM muscle, no relevant myofascial force transmission occurred in the reference position (the position of the GM origin corresponding to a knee angle of 120°). However, some myofascial force transmission occurred when the relative position of the origin of the fully dissected GM muscle was changed with respect to the neuro-vascular tract.

Progressive surgical dissection for tendon transposition affects length-force characteristics of rat flexor carpi ulnaris muscle.

Extramuscular connective tissue and muscular fascia have been suggested to form a myo‐fascial pathway for transmission of forces over a joint that is additional to the generally accepted myo‐tendinous pathway. The consequences of myo‐fascial force transmission for the outcome of conventional muscle tendon transfer surgery has not been studied as yet. To test the hypothesis that surgical dissection of a muscle will affect its length‐force characteristics, a study was undertaken in adult male Wistar rats. During progressive dissection of the flexor carpi ulnaris muscle, isometric length‐force characteristics were measured using maximal electrical stimulation of the ulnar nerve. After fasciotomy, muscle active force decreased by approximately 20%. Further dissection resulted in additional decline of muscle active force by another 40% at maximal dissection. The muscle length at which the muscle produced maximum active force increased by approximately 0.7 mm (i.e. 14% of the measured length range) after dissection. It is concluded that, in rats, the fascia surrounding the flexor carpi ulnaris muscle is a major determinant of muscle length‐force characteristics.

Epimuscular myofascial force transmission occurs in the rat between the deep flexor muscles and their antagonistic muscles

The goal of the present study was to test the hypothesis that epimuscular myofascial force transmission occurs between deep flexor muscles of the rat and their antagonists: previously unstudied mechanical effects of length changes of deep flexors on the anterior crural muscles (i.e., extensor digitorum longus (EDL), as well as tibialis anterior and extensor hallucis longus muscle complex (TA+EHL) and peroneal (PER) muscles were assessed experimentally. These muscles or muscle groups were kept at constant length, whereas, distal length changes were imposed on deep flexor (DF) muscles before performing isometric contractions. Distal forces of all muscle-tendon complexes were measured simultaneously, in addition to EDL proximal force. Distal lengthening of DF caused substantial significant effects on its antagonistic muscles: (1) increase in proximal EDL total force (maximally 19.2%), (2) decrease in distal EDL total (maximally 8.4%) and passive (maximally 49%) forces, (3) variable proximo-distal total force differences indicating net proximally directed epimuscular myofascial loads acting on EDL at lower DF lengths and net distally directed loads at higher DF lengths, (4) decrease in TA+EHL total (maximally 50%) and passive (maximally 66.5%) forces and (5) decrease in PER total force (maximally 51.3%). It is concluded that substantial inter-antagonistic epimuscular myofascial force transmission occurs between deep flexor, anterior crural and peroneal muscles. In the light of our present results and recently reported evidence on inter-antagonistic interaction between anterior crural, peroneal and triceps surae muscles, we concluded that epimuscular myofascial force transmission is capable of causing major effects within the entire lower leg of the rat. Implications of such large scale myofascial force transmission are discussed and expected to be crucial to muscle function in healthy, as well as pathological conditions.