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.     

Inferences on force transmission from muscle fiber architecture of the canine diaphragm

Functional properties of the diaphragm are mediated by muscle structure. Modeling of force transmission necessitates a precise knowledge of muscle fiber architecture. Because the diaphragm experiences loads both along and transverse to the long axes of its muscle fibers in vivo, the mechanism of force transmission may be more complex than in other skeletal muscles that are loaded uniaxially along the muscle fibers. Using a combination of fiber microdissections and histological and morphological methods, we determined regional muscle fiber architecture and measured the shape of the cell membrane of single fibers isolated from diaphragm muscles from 11 mongrel dogs. We found that muscle fibers were either spanning fibers (SPF), running uninterrupted between central tendon (CT) and chest wall (CW), or were non-spanning fibers (NSF) that ended within the muscle fascicle. NSF accounted for the majority of fibers in the midcostal, dorsal costal, and lateral crural regions but were only 25-41% of fibers in the sternal region. In the midcostal and dorsal costal regions, only approximately 1% of the NSF terminated within the fascicle at both ends; the lateral crural region contained no such fibers. We measured fiber length, tapered length, fiber diameters along fiber length, and the taper angle for 271 fibers. The lateral crural region had the longest mean length of SPF, which is equivalent to the mean muscle length, followed by the costal and sternal regions. For the midcostal and crural regions, the percentage of tapered length of NSF was 45.9 +/- 5.3 and 40.6 +/- 7.5, respectively. The taper angle was approximately 0.15 degrees for both, and, therefore, the shear component of force was approximately 380 times greater than the tensile component. When the diaphragm is submaximally activated, as during normal breathing and maximal inspiratory efforts, muscle forces could be transmitted to the cell membrane and to the extracellular intramuscular connective tissue by shear linkage, presumably via structural transmembrane proteins.     

Finite element analysis of mechanics of lateral transmission of force in single muscle fiber

Most of the myofibers in long muscles of vertebrates terminate within fascicles without reaching either end of the tendon, thus force generated in myofibers has to be transmitted laterally through the extracellular matrix (ECM) to adjacent fibers; which is defined as the lateral transmission of force in skeletal muscles. The goal of this study was to determine the mechanisms of lateral transmission of force between the myofiber and ECM. In this study, a 2D finite element model of single muscle fiber was developed to study the effects of mechanical properties of the endomysium and the tapered ends of myofiber on lateral transmission of force. Results showed that most of the force generated is transmitted near the end of the myofiber through shear to the endomysium, and the force transmitted to the end of the model increases with increased stiffness of ECM. This study also demonstrated that the tapered angle of the myofiber ends can reduce the stress concentration near the myofiber end while laterally transmitting force efficiently.     

Myofascial force transmission: muscle relative position and length determine agonist and synergist muscle force.

Equal proximal and distal lengthening of rat extensor digitorum longus (EDL) were studied. Tibialis anterior, extensor hallucis longus, and EDL were active maximally. The connective tissues around these muscle bellies were left intact. Proximal EDL forces differed from distal forces, indicating myofascial force transmission to structures other than the tendons. Higher EDL distal force was exerted (ratio approximately 118%) after distal than after equal proximal lengthening. For proximal force, the reverse occurred (ratio approximately 157%). Passive EDL force exerted at the lengthened end was 7-10 times the force exerted at the nonlengthened end. While kept at constant length, synergists (tibialis anterior + extensor hallucis longus: active muscle force difference approximately -10%) significantly decreased in force by distal EDL lengthening, but not by proximal EDL lengthening. We conclude that force exerted at the tendon at the lengthened end of a muscle is higher because of the extra load imposed by myofascial force transmission on parts of the muscle belly. This is mediated by changes of the relative position of most parts of the lengthened muscle with respect to neighboring muscles and to compartment connective tissues. As a consequence, muscle relative position is a major codeterminant of muscle force for muscle with connectivity of its belly close to in vivo conditions.     

Muscle development in squid: Ultrastructural differentiation of a specialized muscle fiber type

The ultrastructural differentiation of two muscle fiber types of the squid Sepioteuthis lessoniana was correlated with development of prey-capture behavior. Transmission electron microscopy was used to document the differentiation of the fast-contracting cross-striated muscle cells of the tentacles and the obliquely striated muscle cells of the arms of specimens sampled at one week intervals from hatching to 5 weeks. By using high-speed video recordings, the ultrastructural differentiation was correlated with changes in prey-capture behavior that occur during development and growth. The ultrastructural analysis focused on the muscle cells of the transverse muscle of the tentacles and the transverse muscle of the arms. For the first 2 weeks after hatching, the tentacle transverse muscle fibers do not show the adult ultrastructure and are indistinguishable from the obliquely striated fibers of the transverse muscle of the arms. Transverse striation of the tentacle muscle cells appears at approximately three weeks and adult ultrastructure is present by 4–5 weeks after hatching. The high-speed video recordings show correlated behavioral changes. During the first 2–3 weeks after hatching, the animals use a different prey-capture mode from the adults; they jet forward and capture the prey with splayed arms and tentacles rather than employing the rapid tentacular strike. © 1996 Wiley-Liss, Inc.     

Myofascial force transmission in the lower limb: An in vivo experiment

Anatomical studies have shown structural continuity between the lumbopelvic region and the lower limb. The present study aimed to verify how simultaneous changes on knee/hip positions modify the ankle’s resting position and passive torque. Thirty-seven subjects underwent an isokinetic assessment of ankle passive torque. The relationship between the absolute values of ankle passive resistance torque and the ankle angular position was used to calculate the dependent variables: ankle resting position (position in which the passive resistance torque is zero); and ankle passive torque at 0° (torque at the neutral position of the ankle in the sagittal plane). These measures were carried out under three test conditions: 0° at knee and 0° at hip (0°/0°); 90° at knee and 90° at hip (90°/90°); and, 135° at knee and 120° at hip (135°/120°). The results demonstrated that the ankle resting position shifted towards dorsiflexion when knee/hip position changed from 0°/0° to 90°/90° and shifted towards plantar flexion when knee/hip position changed from 90°/90° to 135°/120°, achieving values close to the ones at the position 0°/0°. Similarly, passive torque reduced when knee/hip position changed from 0°/0° to 90°/90°, but it increased when knee/hip position changed from 90°/90° to 135°/120°. The unexpected changes observed in ankle passive torque and resting position due to changes in knee and hip from 90°/90° to 135°/120°, cannot be explained exclusively by forces related to tissues crossing the knee and ankle. This result supports the existence of myofascial force transmission among lower limb joints.     

Muscle fiber characteristics of pectoralis major muscle as related to muscle mass in different Japanese quail lines

The objectives of this study were to investigate the muscle fiber characteristics of the pectoralis major muscle, and its relation to growth performance in the random bred control (RBC) and heavy weight (HW) Japanese quail lines at 42 days of age. The HW line had greater body (232.0 v. 100.2 g, P < 0.001) and pectoralis major muscle (19.0 v. 6.2 g, P < 0.001) weights than the RBC line. Color differences were observed between the superficial and deep regions of the pectoralis major muscle, with the superficial region showing a higher value of lightness than the deep region of the RBC or HW lines (P < 0.001). The percentage of the superficial region in the pectoralis major muscle was higher in the HW line compared with the RBC line (46.2% v. 38.0%, P = 0.017). There were no significant differences in the total fiber number in the superficial and deep regions between the two quail lines (P = 0.718). The HW quail line showed a larger mean fiber cross-sectional area (CSA; 375.5 v. 176.6 μm², P < 0.001) and type IIA fiber CSA (243.7 v. 131.9 μm², P < 0.001) than the RBC quail line. The HW line also had greater CSA percentage (60.2% v. 34.2%, P < 0.001) and number percentage (41.6% v. 14.2%, P < 0.001) of type IIB fibers, although there were no significant differences in type IIB fiber CSA between the RBC and HW lines (P = 0.219). Therefore, greater body and muscle weights of the HW line are caused by differences in muscle fiber characteristics, especially the proportion of type IIB fiber and the CSA of type IIA fiber, compared with the RBC line. The results of this study suggest that muscle fiber hypertrophy has more impact on body and muscle weights of the different quail lines than muscle fiber hyperplasia.     

A micromechanical muscle model for determining the impact of motor unit fiber clustering on force transmission in aging skeletal muscle

This study used a micromechanical finite element muscle model to investigate the effects of the redistribution of spatial activation patterns in young and old muscle. The geometry consisted of a bundle of 19 active muscle fibers encased in endomysium sheets, surrounded by passive tissue to model a fascicle. Force was induced by activating combinations of the 19 active muscle fibers. The spacial clustering of muscle fibers modeled in this study showed unbalanced strains suggesting tissue damage at higher strain levels may occur during higher levels of activation and/or during dynamic conditions. These patterns of motor unit remodeling are one of the consequences of motor unit loss and reinnervation associated with aging. The results did not reveal evident quantitative changes in force transmission between old and young adults, but the patterns of stress and strain distribution were affected, suggesting an uneven distribution of the forces may occur within the fascicle that could provide a mechanism for muscle injury in older muscle.

     

From single muscle fiber to whole muscle mechanics: a finite element model of a muscle bundle with fast and slow fibers

Muscles exhibit highly complex, multi-scale architecture with thousands of muscle fibers, each with different properties, interacting with each other and surrounding connective structures. Consequently, the results of single-fiber experiments are scarcely linked to the macroscopic or whole muscle behavior. This is especially true for human muscles where it would be important to understand of how skeletal muscles disorders affect patients’ life. In this work, we developed a mathematical model to study how fast and slow muscle fibers, well characterized in single-fiber experiments, work and generate together force and displacement in muscle bundles. We characterized the parameters of a Hill-type model, using experimental data on fast and slow single human muscle fibers, and comparing experimental data with numerical simulations obtained from finite element (FE) models of single fibers. Then, we developed a FE model of a bundle of 19 fibers, based on an immunohistochemically stained cross section of human diaphragm and including the corresponding properties of each slow or fast fiber. Simulations of isotonic contractions of the bundle model allowed the generation of its apparent force–velocity relationship. Although close to the average of the force–velocity curves of fast and slow fibers, the bundle curve deviates substantially toward the fast fibers at low loads. We believe that the present model and the characterization of the force–velocity curve of a fiber bundle represents the starting point to link the single-fiber properties to those of whole muscle with FE application in phenomenological models of human muscles.     

Optimal design of flax fiber reinforced polymer composite as a lightweight component for automobiles from a life cycle assessment perspective

The present study combines the generalized rule‐of‐mixture (ROM) model and the Ashby material selection method for the life cycle assessment (LCA) of flax fiber reinforced polymers (FRPs) and glass FRPs (GFRPs). The ROM model allows life cycle environmental impact predictions according to specific parameters of flax FRPs such as fiber format, volume fraction, manufacturing technique, and load‐bearing capacity. The comparisons applied in this study are constructed on two common composite structures: mat panels and injection molded struts with equal stiffness and strength as the design criteria. On the one hand, the parametric LCA predicts that the equal strength design criterion for flax FRPs contributes to consistent mass increases, subsequently resulting in higher life cycle environmental impacts compared to the reference GFRPs; on the other hand, under the equal stiffness criterion the flax mat polypropylene (flax mat‐PP) film helps with mass reduction in reference to the glass mat‐PP composite, leading to the 20–50% life cycle environmental impact reductions for most impact categories. The subsequent evaluation of the influences of the fiber volume fraction on flax FRPs shows different patterns. For the short flax fiber‐PP composite, a steady decrease of the life cycle CO₂ emissions can be observed with the increasing fiber volume fraction. However, for the flax mat‐PP composite, depending on the tensile modulus of the flax fiber, the optimal volume fractions of the fiber change from 28 to 32% v/v, whereby the lowest life cycle greenhouse gas (GHG) emissions can be achieved.     

Skeletal muscle fiber atrophy: altered thin filament density changes slow fiber force and shortening velocity

Single skinned fibers from soleus and adductor longus (AL) muscles of weight-bearing control rats and rats after 14-day hindlimb suspension unloading (HSU) were studied physiologically and ultrastructurally to investigate how slow fibers increase shortening velocity (V₀) without fast myosin. We hypothesized that unloading and shortening of soleus during HSU reduces densities of thin filaments, generating wider myofilament separations that increase V₀ and decrease specific tension (kN/m²). During HSU, plantarflexion shortened soleus working length 23%. AL length was unchanged. Both muscles atrophied as shown by reductions in fiber cross-sectional area. For AL, the 60% atrophy accounted fully for the 58% decrease in absolute tension (mN). In the soleus, the 67% decline in absolute tension resulted from 58% atrophy plus a 17% reduction in specific tension. Soleus fibers exhibited a 25% reduction in thin filaments, whereas there was no change in AL thin filament density. Loss of thin filaments is consistent with reduced cross bridge formation, explaining the fall in specific tension. V₀ increased 27% in soleus but was unchanged in AL. The V₀ of control and HSU fibers was inversely correlated (R = –0.83) with thin filament density and directly correlated (R = 0.78) with thick-to-thin filament spacing distance in a nonlinear fashion. These data indicate that reduction in thin filament density contributes to an increased V₀ in slow fibers. Osmotically compacting myofilaments with 5% dextran returned density, spacing, and specific tension and slowed V₀ to near-control levels and provided evidence for myofilament spacing modulating tension and V₀. rat; soleus; adductor longus; fiber length; electron microscopy; hindlimb suspension unloading     

Hormones and the barnacle muscle fiber as a preparation

This minireview discusses the use of single barnacle muscle fibers as a model system for studying hormonal actions. The response of barnacle muscle fibers to serotonin, proctolin, octopamine, aldosterone and insulin is described. Recent data relating to the actions of these hormones on other invertebrate and vertebrate preparations is touched upon. The use of the barnacle muscle fiber as a preparation to investigate hormone-stimulated protein phosphorylation is emphasized.     

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.     

The role of transmembrane proteins on force transmission in skeletal muscle

Lateral transmission of force from myofibers laterally to the surrounding extracellular matrix (ECM) via the transmembrane proteins between them is impaired in old muscles. Changes in geometrical and mechanical properties of ECM of skeletal muscle do not fully explain the impaired lateral transmission with aging. The objective of this study was to determine the role of transmembrane proteins on force transmission in skeletal muscle. In this study, a 2D finite element model of single muscle fiber composed of myofiber, ECM, and the transmembrane proteins between them was developed to determine how changes in spatial density and mechanical properties of transmembrane proteins affect the force transmission in skeletal muscle. We found that force transmission and stress distribution are not affected by mechanical stiffness of the transmembrane proteins due to its non-linear stress–strain relationship. Results also showed that the muscle fiber with insufficient transmembrane proteins near the end of muscle fiber transmitted less force than that with more proteins does. Higher stress was observed in myofiber, ECM, and proteins in the muscle fiber with fewer proteins.     

Force recovery after activated shortening in whole skeletal muscle: transient and steady-state aspects of force depression.

The depression of isometric force after active shortening is a well-accepted characteristic of skeletal muscle, yet its mechanisms remain unknown. Although traditionally analyzed at steady state, transient phenomena caused, at least in part, by cross-bridge kinetics may provide novel insight into the mechanisms associated with force depression (FD). To identify the transient aspects of FD and its relation to shortening speed, shortening amplitude, and muscle mechanical work, in situ experiments were conducted in soleus muscle-tendon units of anesthetized cats. The period immediately after shortening, in which force recovers toward steady state, was fit by using an exponential recovery function (R2 > 0.99). Statistical analyses revealed that steady-state FD (FD(ss)) increased with shortening amplitude and mechanical work. This FD(ss) increase was always accompanied by a significant decrease in force recovery rate. Furthermore, a significant reduction in stiffness was observed after all activated shortenings, presumably because of a reduced proportion of attached cross bridges. These results were interpreted with respect to the two most prominent proposed mechanisms of force depression: sarcomere length nonuniformity theory (7, 32) and a stress-induced inhibition of cross-bridge binding in the newly formed actin-myosin overlap zone (14, 28). We hypothesized that the latter could describe both steady-state and transient aspects of FD using a single scalar variable, the mechanical work done during shortening. As either excursion (overlap) or force (stress) is increased, mechanical work increases, and cross-bridge attachment would become more inhibited, as supported by this study in which an increase in mechanical work resulted in a slower recovery to a more depressed steady-state force.