Substantial effects of epimuscular myofascial force transmission on muscular mechanics have major implications on spastic muscle and remedial surgery

The specific aim of this paper is to review the effects of epimuscular myofascial force transmission on muscular mechanics and present some new results on finite element modeling of non-isolated aponeurotomized muscle in order to discuss the dependency of mechanics of spastic muscle, as well as surgery for restoration of function on such force transmission.

The etiology of the effects of spasticity on muscular mechanics is not fully understood. Clinically, such effects feature typically a limited joint range of motion, which at the muscle level must originate from altered muscle length–force characteristics, in particular a limited muscle length range of force exertion. In studies performed to understand what is different in spastic muscle and what the effects of remedial surgery are, muscle is considered as being independent of its surroundings. Conceivably, this is because the classical approach in muscle mechanics is built on experimenting with dissected muscles. Certainly, such approach allowed improving our understanding of fundamental muscle physiology yet it yielded implicitly a narrow point of view of considering muscle length–force characteristics as a fixed property of the muscle itself.

However, within its context of its intact connective tissue surroundings (the in vivo condition) muscle is not an isolated and independent entity. Instead, collagenous linkages between epimysia of adjacent muscles provide direct intermuscular connections, and structures such as the neurovascular tracts provide indirect intermuscular connections. Moreover, compartmental boundaries (e.g., intermuscular septa, interosseal membranes, periost and compartmental fascia) are continuous with neurovascular tracts and connect muscular and non-muscular tissues at several locations additional to the tendon origins and insertions. Epimuscular myofascial force transmission occurring via this integral system of connections has major effects on muscular mechanics including substantial proximo-distal force differences, sizable changes in the determinants of muscle length–force characteristics (e.g. a condition dependent shift in muscle optimum length to a different length or variable muscle optimal force) explained by major serial and parallel distributions of sarcomere lengths. Therefore, due to epimuscular myofascial force transmission, muscle length–force characteristics are variable and muscle length range of force exertion cannot be considered as a fixed property of the muscle.

The findings reviewed presently show that acutely, the mechanical mechanisms manipulated in remedial surgery are dominated by epimuscular myofascial force transmission. Conceivably, this is also true for the mechanism of adaptation during and after recovery from surgery. Moreover, stiffened epimuscular connections and therefore a stiffened integral system of intra- and epimuscular myofascial force transmission are indicated to affect the properties of spastic muscle. We suggest that important advancements in our present understanding of such properties, variability in the outcome of surgery and considerable recurrence of the impeded function after recovery cannot be made without taking into account the effects of epimuscular myofascial force transmission.     

Extramuscular myofascial force transmission alters substantially the acute effects of surgical aponeurotomy: assessment by finite element modeling

Effects of extramuscular myofascial force transmission on the acute effects of aponeurotomy were studied using finite element modeling and implications of such effects on surgery were discussed. Aponeurotomized EDL muscle of the rat was modeled in two conditions: (1) fully isolated (2) with intact extramuscular connections. The specific goal was to assess the alterations in muscle length-force characteristics in relation to sarcomere length distributions and to investigate how the mechanical mechanism of the intervention is affected if the muscle is not isolated. Major effects of extramuscular myofascial force transmission were shown on muscle length-force characteristics. In contrast to the identical proximal and distal forces of the aponeurotomized isolated muscle, substantial proximo-distal force differences were shown for aponeurotomized muscle with extramuscular connections (for all muscle lengths F (dist) > F (prox) after distal muscle lengthening). Proximal optimal length did not change whereas distal optimal length was lower (by 0.5 mm). The optimal forces of the aponeurotomized muscle with extramuscular connections exerted at both proximal and distal tendons were lower than that of isolated muscle (by 15 and 7%, respectively). The length of the gap separating the two cut ends of the intervened aponeurosis decreases substantially due to extramuscular myofascial force transmission. The amplitude of the difference in gap length was muscle length dependent (maximally 11.6% of the gap length of the extramuscularly connected muscle). Extramuscular myofascial force transmission has substantial effects on distributions of lengths of sarcomeres within the muscle fiber populations distal and proximal to the location of intervention: (a) Within the distal population, the substantial sarcomere shortening at the proximal ends of muscle fibers due to the intervention remained unaffected however, extramuscular myofascial force transmission caused a more pronounced serial distribution towards the distal ends of muscle fibers. (b) In contrast, extramuscular myofascial force transmission limits the serial distribution of sarcomere lengths shown for the aponeurotomized isolated muscle in the proximal population. Fiber stress distributions showed that extramuscular myofascial force transmission causes most sarcomeres within the aponeurotomized muscle to attain lengths favorable for higher force exertion. It is concluded that acute effects of aponeurotomy on muscular mechanics are affected greatly by extramuscular myofascial force transmission. Such effects have important implications for the outcome of surgery performed to improve impeded function since muscle in vivo is not isolated both anatomically and mechanically.     

Extramuscular myofascial force transmission: experiments and finite element modeling

The specific purpose of the present study was to show that extramuscular myofascial force transmission exclusively has substantial effects on muscular mechanics. Muscle forces exerted at proximal and distal tendons of the rat extensor digitorium longus (EDL) were measured simultaneously, in two conditions (1) with intact extramuscular connections (2) after dissecting the muscles' extramuscular connections to a maximum extent without endangering circulation and innervation (as in most in situ muscle experiments). A finite element model of EDL including the muscles' extramuscular connections was used to assess the effects of extramuscular myofascial force transmission on muscular mechanics, primarily to test if such effects lead to distribution of length of sarcomeres within muscle fibers. In condition (1), EDL isometric forces measured at the distal and proximal tendons were significantly different (F(dist) > F(prox), DeltaF approximates maximally 40% of the proximal force). The model results show that extramuscular myofascial force transmission causes distributions of strain in the fiber direction (shortening in the proximal, lengthening in the distal ends of fibers) at higher lengths. This indicates significant length distributions of sarcomeres arranged in series within muscle fibers. Stress distributions found are in agreement with the higher distal force measured, meaning that the muscle fiber is no longer the unit exerting equal forces at both ends. Experimental results obtained in condition (2) showed no significant changes in the length-force characteristics (i.e., proximo-distal force differences were maintained). This shows that a muscle in situ has to be distinguished from a muscle that is truly isolated in which case the force difference has to be zero. We conclude that extramuscular myofascial force transmission has major effects on muscle functioning.     

Epimuscular myofascial force transmission between antagonistic and synergistic muscles can explain movement limitation in spastic paresis

Details and concepts of intramuscular, extramuscular and intermuscular myofascial force transmission are reviewed. Some new experimental data are added regarding myofascial force transmission between antagonistic muscles across the interosseal membrane of the lower hind limb of the rat. Combined with other result presented in this issue, it can be concluded that myofascial force transmission occurs between all muscles within a limb segment. This means that force generated within sarcomeres of an antagonistic muscle may be exerted at the tendon of target muscle or its synergists.

Some, in vivo, but initial indications for intersegmental myofascial force transmission are discussed. The concept of myofascial force transmission as an additional load on the muscle proved to be fruitful in the analysis of its muscular effects. In spastic paresis and for healthy muscles distal myofascial loads are often encountered, but cannot fully explain the movement limitations in spastic paresis. Therefore, the concept of simultaneous and opposing myofascial loads is analyzed and used to formulate a hypothesis for explaining the movement limitation: Myofascially transmitted antagonistic force is borne by the spastic muscle, but subsequently transmitted again to distal tendons of synergistic muscles.     

Three-dimensional finite element modeling of skeletal muscle using a two-domain approach: linked fiber-matrix mesh model

In previous applications of the finite element method in modeling mechanical behavior of skeletal muscle, the passive and active properties of muscle tissue were lumped in one finite element. Although this approach yields increased understanding of effects of force transmission, it does not support an assessment of the interaction between the intracellular structures and extracellular matrix. In the present study, skeletal muscle is considered in two domains: (1) the intracellular domain and (2) extracellular matrix domain. The two domains are represented by two separate meshes that are linked elastically to account for the trans-sarcolemmal attachments of the muscle fibers' cytoskeleton and extracellular matrix. With this approach a finite element skeletal muscle model is developed, which allows force transmission between these domains with the possibility of investigating their interaction as well as the role of the trans-sarcolemmal systems. The model is applied to show the significance of myofascial force transmission by investigating possible mechanical consequences due to any missing link within the trans-sarcolemmal connections such as found in muscular dystrophies. This is realized by making the links between the two meshes highly compliant at selected intramuscular locations. The results indicate the role of extracellular matrix for a muscle in sustaining its physiological condition. It is shown that if there is an inadequate linking to the extracellular matrix, the myofibers become deformed beyond physiological limits due to the lacking of mechanical support and impairment of a pathway of force transmission by the extracellular matrix. This leads to calculation of a drop of muscle force and if the impairment is located more towards the center of the muscle model, its effects are more pronounced. These results indicate the significance of non-myotendinous force transmission pathways.     

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.     

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.     

Mechanical interaction between neighboring muscles in human upper limb: Evidence for epimuscular myofascial force transmission in humans

To confirm the existence of epimuscular myofascial force transmission in humans, this study examined if manipulating joint angle to stretch the muscle can alter the shear modulus of a resting adjacent muscle, and whether there are regional differences in this response. The biceps brachii (BB: manipulated muscle) and the brachialis (BRA: resting adjacent muscle) were deemed suitable for this study because they are neighboring, yet have independent tendons that insert onto different bones. In order to manipulate the muscle length of BB only, the forearm was passively set at supination, neutral, and pronation positions. For thirteen healthy young adult men, the shear modulus of BB and BRA was measured with shear-wave elastography at proximal and distal muscle regions for each forearm position and with the elbow joint angle at either 100° or 160°. At both muscle regions and both elbow positions, BB shear modulus increased as the forearm was rotated from a supinated to pronated position. Conversely, BRA shear modulus decreased as function of forearm position. The effect of forearm position on shear modulus was most pronounced in the distal muscle region when the elbow was at 160°. The observed alteration of shear modulus of the resting adjacent muscle indicates that epimuscular myofascial force transmission is present in the human upper limb. Consistent with this assertion, we found that the effect of muscle length on shear modulus in both muscles was region-dependent. Our results also suggest that epimuscular myofascial force transmission may be facilitated at stretched muscle lengths.     

Magnetic resonance and diffusion tensor imaging analyses indicate heterogeneous strains along human medial gastrocnemius fascicles caused by submaximal plantar-flexion activity

Sarcomere length changes are central to force production and excursion of skeletal muscle. Previous modeling indicates non-uniformity of that if mechanical interaction of muscle with its surrounding muscular and connective tissues is taken into account. Hence, quantifying length changes along the fascicles of activated human muscle in vivo is crucial, but this is lacking due to technical complexities. Combining magnetic resonance imaging deformation analyses and diffusion tensor imaging tractography, the aim was to test the hypothesis that submaximal plantar flexion activity at 15% MVC causes heterogeneous length changes along the fascicles of human medial gastrocnemius (GM) muscle. A general fascicle strain distribution pattern shown for all subjects indicates that proximal track segments are shortened, whereas distal ones are lengthened (e.g., by 13% and 29%, respectively). Mean fiber direction strains of different tracts also shows heterogeneity (for up to 57.5% of the fascicles). Inter-subject variability of amplitude and distribution of fascicle strains is notable. These findings confirm the hypothesis and are solid indicators for the functionally dependent mechanics of human muscle, in vivo. Heterogeneity of fascicle strains can be explained by epimuscular myofascial force transmission. To the best of our knowledge, this is the first study, which quantified local deformations along human skeletal muscle fascicles caused by sustained submaximal activation. The present approach and indicated fascicle strain heterogeneity has numerous implications for muscle function in health and disease to estimate the muscle’s contribution to the joint moment and excursion and to evaluate mechanisms of muscle injury and several treatment techniques.     

Effects of inter- and extramuscular myofascial force transmission on adjacent synergistic muscles: assessment by experiments and finite-element modeling

The effects of inter- and extramuscular myofascial force transmission on muscle length force characteristics were studied in rat. Connective tissues at the bellies of the experimental synergistic muscles of the anterior crural compartment were left intact. Extensor digitorium longus (EDL) muscle was lengthened distally whereas tibialis anterior (TA) and extensor hallucis longus (EHL) were kept at constant muscle–tendon complex length. Substantial differences were found in EDL force measured at the proximal and distal tendons (maximally 46% of the proximal force). EDL with intact inter- as well as extramuscular connections had an increased length range between active slack and optimum length compared to EDL with extramuscular connections exclusively: optimum muscle length was shifted by more than 2 mm. Distal EDL lengthening caused the distal force exerted by TA+EHL complex to decrease (approximately 17% of the initial force). This indicates increased intermuscular myofascial force transmission from TA+EHL muscle complex to EDL muscle.

Finite-element modeling showed that: (1) Inter- and extramuscular myofascial force transmission leads to a substantial distribution of the lengths of the sarcomeres arranged in series within muscle fibers. Distribution of stress within the muscle fibers showed that the muscle fiber cannot be considered as a unit exerting equal forces at both ends. (2) Increased heterogeneity of mean fiber sarcomere lengths (i.e., a “parallel” distribution of length of sarcomeres among different muscle fibers) is found, particularly at high muscle lengths. This also explains the shift in muscle optimum length to higher lengths.

It is concluded that inter- and extramuscular myofascial force transmission has substantial effects on muscle length–force characteristics.     

Extramuscular myofascial force transmission also occurs between synergistic muscles and antagonistic muscles

The purpose of the present study was to test the hypothesis that myofascial force transmission may not be limited by compartmental boundaries of a muscle group to synergists. Muscles of the anterior tibial compartment in rat hindlimb as well as of the neighbouring peroneal compartment (antagonistic muscles) were excited maximally. Length–force data, based on proximal lengthening, of EDL, as well as distal lengthening of the tibial muscles (TA + EHL) and the peroneal muscle group (PER) were collected independently, while keeping the other two muscle groups at a constant muscle–tendon complex length. Simultaneously measured, distal and proximal EDL active forces were found to differ significantly throughout the experiment. The magnitude of this difference and its sign was affected after proximal lengthening of EDL itself, but also of the tibial muscle complex and of the peroneal muscle complex. Proximal lengthening of EDL predominantly affected its synergistic muscles within the anterior crural compartment (force decrease <4%). Lengthening of either TA or PER caused a decrease in distal EDL isometric force (by 5–6% of initial force). It is concluded also that mechanisms for mechanical intermuscular interaction extend beyond the limits of muscle compartments in the rat hindlimb. Even antagonistic muscles should not be considered fully independent units of muscular function.

Particular, strong mechanical interaction was found between antagonistic tibial anterior muscle and peroneal muscle complexes: Lengthening of the peroneal complex caused tibial complex force to decrease by approximately 25%, whereas for the reverse a 30% force decrease was found.     

Acute effects of intramuscular aponeurotomy on rat gastrocnemius medialis: force transmission, muscle force and sarcomere length

Acute effects of intramuscular aponeurotomy on muscle force and geometry as a function to muscle length were studied in rat m. gastrocnemius medialis (GM). Acutely after aponeurotomy, activation of the muscle at increasing lengths (acute trajectory) showed a spontaneous and progressive but patial tearing of the connective tissue interface between the fibres inserting directly proximally and distally to the location of the section. After this the muscle consisted morphologically of a stable proximal and a distal part (post-aponeurotomy). Post-aponeurotomy mean active sarcomere length within fibres of the proximal part was shown to be unaffected. In contrast, mean sarcomere length within the distal part was reduced substantially after aponeurotomy. However active sarcomeres in the distal part were still attaining higher lengths with increasing muscle lengths (p<0.005), indicating myofascial force transmission through the intact part of the connective tissue interface of the muscle parts. Post-aponeurotomy optimum muscle force was reduced substantially to less than 45% of pre-aponeurotomy values. During the acute trajectory the muscle yielded approximately 20% higher forces than post-aponeurotomy, indicating that myofascial force transmission was related to the area of connective tissue interface. It is concluded that after aponeurotomy of the proximal aponeurosis of rat GM, fibres without direct myotendinous connection to the origin of the muscle are still able to contribute to muscle force. As the magnitude of reduction in muscle force can only be explained partially by the spontaneous rupture of the connective tissue interface between proximal and distal muscle part, other factors causing a decrease of muscle force are present. Clinical implication of acute effects of intramuscular aponeurotomy are discussed.     

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.     

Myofascial force transmission between a single muscle head and adjacent tissues: length effects of head III of rat EDL.

Force transmission from muscle fibers via the connective tissue network (i.e., myofascial force transmission) is an important determinant of muscle function. This study investigates the role of myofascial pathways for force transmission from multitendoned extensor digitorum longus (EDL) muscle within an intact anterior crural compartment. Effects of length changes exclusively of head III of rat EDL muscle (EDL III) on myofascial force transmission were assessed. EDL III was lengthened at the distal tendon. For different lengths of EDL III, isometric forces were measured at the distal tendon of EDL III, as well as at the proximal tendon of whole EDL and at the distal tendons of tibialis anterior and extensor hallucis longus (TA+EHL) muscles. Lengthening of EDL III caused high changes in force exerted at the distal tendon of EDL III (from 0 to 1.03 +/- 0.07 N). In contrast, only minor changes were found in force exerted at the proximal EDL tendon (from 2.37 +/- 0.09 to 2.53 +/- 0.10 N). Increasing the length of EDL III decreased TA+EHL force significantly (by 7%, i.e., from 5.62 +/- 0.27 to 5.22 +/- 0.32 N). These results show that force is transmitted between EDL III and adjacent tissues via myofascial pathways. Optimal force exerted at the distal tendon of EDL III (1.03 +/- 0.07 N) was more than twice the force expected on the basis of the physiological cross-sectional area of EDL III muscle fibers (0.42 N). Therefore, a substantial fraction of this force must originate from sources other than EDL III. It is concluded that myofascial pathways play an important role in force transmission from multitendoned muscles.     

Myofascial force transmission between antagonistic rat lower limb muscles: Effects of single muscle or muscle group lengthening

Effects of lengthening of the whole group of anterior crural muscles (tibialis anterior and extensor hallucis longus muscles (TA + EHL) and extensor digitorum longus (EDL)) on myofascial interaction between synergistic EDL and TA + EHL muscles, and on myofascial force transmission between anterior crural and antagonistic peroneal muscles, were investigated. All muscles were either passive or maximally active. Peroneal muscles were kept at a constant muscle tendon complex length. Either EDL or all anterior crural muscles were lengthened so that effects of lengthening of TA + EHL could be analyzed. For both lengthening conditions, a significant difference in proximally and distally measured EDL passive and active forces, indicative of epimuscular myofascial force transmission, was present. However, added lengthening of TA + EHL significantly affected the magnitude of the active and passive load exerted on EDL. For the active condition, the direction of the epimuscular load on EDL was affected; at all muscle lengths a proximally directed load was exerted on EDL, which decreased at higher muscle lengths. Lengthening of anterior crural muscles caused a 26% decrease in peroneal active force.

Extramuscular myofascial connections are thought to be the major contributor to the EDL proximo-distal active force difference. For antagonistic peroneal complex, the added distal lengthening of a synergistic muscle increases the effects of extramuscular myofascial force transmission.     

Compartmental fasciotomy and isolating a muscle from neighboring muscles interfere with myofascial force transmission within the rat anterior crural compartment

Muscles within the anterior crural compartment (extensor digitorum longus, EDL; tibialis anterior, TA; and extensor hallucis longus, EHL) and within the peroneal compartment were excited simultaneously and maximally. All muscles were kept at constant length with the exception of EDL, for which muscle length was changed by moving its proximal tendon. Active and passive force was measured at proximal as well as distal EDL tendons and at the combined distal tendons of TA and EHL (TA+EHL). In the initial experimental condition, a difference (F(proximal) > F(distal)) in EDL force, amounting to 0-14% of proximal force, was confirmed for most EDL lengths. This is interpreted as a clear proof of extramuscular myofascial force transmission, as no significant EDL length effects could be shown on TA+EHL force. Repeated measurements were confirmed to cause marked changes of both proximal and distal length-force characteristics, such as a shift of the whole ascending limb of the active curve, including optimum length, to higher lengths without decreasing optimum force, and decreasing active force at low lengths (by approximately 57%). Repeated measurements also lowered proximal and distal EDL passive force (by up to 35%). The proximo-distal difference in passive as well as active EDL force was decreased, but persisted. At most lengths, this difference for active force amounted to a constant fraction (14%) of proximal force. TA+EHL force was not affected significantly. Subsequently, acute effects of experimental surgical alterations were studied: The first manipulation was full lateral fasciotomy of the anterior crural compartment that caused a further decrease in active force at the proximal EDL but not at the distal EDL tendon. Passive forces showed no further significant changes. The proximo-distal EDL active force difference decreased to 0-5% of proximal force. After fasciotomy, TA+EHL force increased by 30%. This was interpreted as evidence of increased intramuscular and decreased extramuscular myofascial force transmission. The second manipulation was full isolation of EDL from TA+EHL, but not from extramuscular connective tissues, which caused a further decrease of the EDL proximo-distal force differences, indicating a stiffening effect of the presence of TA+EHL on the extramuscular matrix. For EDL active force the difference was no longer significantly different from zero. In contrast, for EDL passive force the proximo-distal force difference persisted. It is concluded that extramuscular myofascial force transmission is an important feature of the anterior crural compartment. The magnitude of this force transmission requires that it be considered in analysis of muscular function.     

Myofascial force transmission also occurs between antagonistic muscles located within opposite compartments of the rat lower hind limb

Force transmission via pathways other than myotendinous ones, is referred to as myofascial force transmission. The present study shows that myofascial force transmission occurs not only between adjacent synergistic muscles or antagonistic muscles in adjacent compartments, but also between most distant antagonistic muscles within a segment. Tibialis anterior (TA), extensor hallucis longus (EHL), extensor digitorum longus (EDL), peroneal muscles (PER) and triceps surae muscles of 7 male anaesthetised Wistar rats were attached to force transducers, while connective tissues at the muscle bellies were left fully intact. The TA + EHL-complex was made to exerted force at different lengths, but the other muscles were held at a constant muscle–tendon complex length. With increasing TA + EHL-complex length, active force of maximally activated EDL, PER and triceps surae decreased by maximally 5%, 32% and 16%, respectively. These decreases are for the largest part explained by myofascial force transmission. Particularly the force decrease in triceps surae muscles is remarkable, because these muscles are located furthest away from the TA + EHL-complex. It is concluded that substantial extramuscular myofascial force transmission occurs between antagonistic muscles even if the length of the path between them is considerable.     

Muscular force transmission: a unified, dual or multiple system? A review and some explorative experimental results

Structures contributing to force transmission in muscle are reviewed combining some historical and relatively recently published experimental data. Also, effects of aponeurotomy and tenotomy are reviewed shortly as well as some new experimental results regarding these interventions that reinforce the concept of myofascial force transmission. The review is also illustrated by some new images of single muscle fibres from Xenopus Laevis indicative of such transmission and some data about locations of insertion of human gluteus maximus muscle. From this review and the new material, emerges a line of thought indicating that mechanical connections between muscle fibres and intramuscular connective tissue play an important role in force transmission. New experimental observations are presented for non-spanning muscle (i.c., rat biceps femoris muscle), regarding the great variety of types of intramuscular connections that exist i n addition to myo-tendinous junctions at the perimuscular ends of muscle fibres. Such connections are classified as (1) tapered end connections, (2) Myo-myonal junctions, (3) myo-epimysial junctions and (3) Myo-endomysial junctions. This line of thought is followed up by consideration of a possible role of connections of intra- and extramuscular connective tissue in force transmission out of the muscle. Experimental results of an explorative nature, regarding the interactions of extensor digitorum longus (EDL), tibialis anterior (TA) and hallucis longus (HAL) muscles within a relatively intact dorsal flexor compartment of the rat hind leg, indicate that: (1) length force properties of EDL are influenced by TA activity in a length dependent fashion. Depending on TA length, force exerted by EDL, kept at constant origin insertion distance, is variable and the effect is influenced by EDL length itself as well; (2) Force is transmitted from muscle to extramuscular connective tissue and vice versa. As a consequence force exerted at proximal and distal tendons of a muscle are not always equal. The difference being transmitted by extramuscular connective tissue and may appear at the tendons of other muscles or may be transmitted via connective tissue directly to bone. It is concluded that the system of force transmission from skeletal muscle should be considered as a multiple system.     

Mechanical principles of effects of botulinum toxin on muscle length–force characteristics: An assessment by finite element modeling

Recent experiments involving muscle force measurements over a range of muscle lengths show that effects of botulinum toxin (BTX) are complex e.g., force reduction varies as a function of muscle length. We hypothesized that altered conditions of sarcomeres within active parts of partially paralyzed muscle is responsible for this effect. Using finite element modeling, the aim was to test this hypothesis and to study principles of how partial activation as a consequence of BTX affects muscle mechanics. In order to model the paralyzing effect of BTX, only 50% of the fascicles (most proximal, or middle, or most distal) of the modeled muscle were activated. For all muscle lengths, a vast majority of sarcomeres of these BTX-cases were at higher lengths than identical sarcomeres of the BTX-free muscle. Due to such “longer sarcomere effect”, activated muscle parts show an enhanced potential of active force exertion (up to 14.5%). Therefore, a muscle force reduction originating exclusively from the paralyzed muscle fiber populations, is compromised by the changes of active sarcomeres leading to a smaller net force reduction. Moreover, such “compromise to force reduction” varies as a function of muscle length and is a key determinant of muscle length dependence of force reduction caused by BTX. Due to longer sarcomere effect, muscle optimum length tends to shift to a lower muscle length. Muscle fiber–extracellular matrix interactions occurring via their mutual connections along full peripheral fiber lengths (i.e., myofascial force transmission) are central to these effects. Our results may help improving our understanding of mechanisms of how the toxin secondarily affects the muscle mechanically.     

Muscular dystrophies, dilated cardiomyopathy, lipodystrophy and neuropathy: the nuclear connection

An understanding of muscle structure and function is central to improving our knowledge of the group of muscle diseases referred to as muscular dystrophies. These diseases involve a progressive weakening and wasting of skeletal muscle, which can be associated with life-threatening cardiac arrhythmias. The vast majority of these diseases arise from defects in either cytoskeletal or structural proteins, resulting in a breakdown of muscle cell integrity. However, mutations in two nuclear proteins--emerin and lamin A/C--have also been demonstrated to give rise to a muscular dystrophy phenotype. In addition, mutations in lamin A/C can give rise to a dilated cardiomyopathy, a lipodystrophy or a neuropathy. It is far from clear how mutations in nuclear proteins can result in a dystrophy, or cause more than one clinically distinct disease. Understanding the functional role of nuclear proteins in causing these diseases will therefore provide novel insights into muscle function, and should hopefully provide new directions for treatment.