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.     

Myofascial force transmission between the human soleus and gastrocnemius muscles during passive knee motion

The plantarflexors of the lower limb are often assumed to act as independent actuators, but the validity of this assumption is the subject of considerable debate. This study aims to determine the degree to which passive changes in gastrocnemius muscle length, induced by knee motion, affect the tension in the adjacent soleus muscle. A second aim is to quantify the magnitude of myofascial passive force transmission between gastrocnemius and adjacent soleus. Fifteen healthy volunteers participated. Simultaneous ultrasound images of the gastrocnemius and soleus muscles were obtained during passive knee flexion (0-90°), while keeping the ankle angle fixed at either 70° or 115°. Image correlation analysis was used to quantify muscle fascicle lengths in both muscles. The data show that the soleus muscle fascicles elongate significantly during gastrocnemius shortening. The approximate change in passive soleus force as a result of the observed change in fascicle length was estimated and appears to be <5 N, but this estimate is sensitive to the assumed slack length of soleus.     

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.     

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.     

Lateral force transmission between human tendon fascicles.

Whether adjacent collagen fascicles transmit force in parallel is unknown. The purpose of the present study was to examine the magnitude of lateral force transmission between adjacent collagen fascicles from the human patellar and Achilles tendon. From each sample two adjacent strands of fascicles (phi 300-530 mum) enclosed in a fascicular membrane were dissected. The specimen was deformed to approximately 3% strain in three independent load-displacement cycles in a small-scale tensile testing device. Cycle 1: the fascicles and the fascicular membrane were intact. Cycle 2: one fascicle was transversally cut while the other fascicle and the fascicular membrane were kept intact. Cycle 3: both fascicles were cut in opposite ends while the fascicular membrane was left intact. A decline in peak force of 45% and 55% from cycle 1 to cycle 2, and 93% and 92% from cycle 2 to cycle 3 was observed in the patellar and Achilles tendon fascicles, respectively. A decline in stiffness of 39% and 60% from cycle 1 to cycle 2, and of 93% and 100% from cycle 2 to cycle 3 was observed in the patellar and Achilles tendon fascicles, respectively. The present data demonstrate that lateral force transmission between adjacent collagen fascicles in human tendons is small or negligible, suggesting that tendon fascicles largely act as independent structures and that force transmission principally takes place within the individual fascicles.     

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.     

Functional and architectural complexity within and between muscles: regional variation and intermuscular force transmission

Over the past 30 years, studies of single muscles have revealed complex patterns of regional variation in muscle architecture, activation, strain and force. In addition, muscles are often functionally integrated with other muscles in parallel or in series. Understanding the extent of this complexity and the interactions between muscles will profoundly influence how we think of muscles in relation to organismal function, and will allow us to address questions regarding the functional benefits (or lack thereof) and dynamics of this complexity under in vivo conditions. This paper has two main objectives. First, we present a cohesive and integrative review of regional variation in function within muscles, and discuss the functional ramifications that can stem from this variation. This involves splitting regional variation into passive and active components. Second, we assess the functional integration of muscles between different limb segments by presenting new data involving in vivo measurements of activation and strain from the medial gastrocnemius, iliotibialis cranialis and iliotibialis lateralis pars preacetabularis of the helmeted guinea fowl (Numida meleagris) during level running on a motorized treadmill. Future research directions for both of these objectives are presented.     

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.     

Myoelectric signal versus force relationship in different human muscles

An analytic study was initiated to investigate whether the normalized surface myoelectric signal vs. normalized force relationship varies in different human muscles and whether it is dependent on training level and rate of force production. The data were obtained from experiments that involved the biceps, deltoid, and first dorsal interosseous of three pianists, four long-distance swimmers, three power lifters, and six normal subjects. The elite performers (among the world's best) were chosen because they exhibited varying degrees of fine motor control, endurance training, and power training in different muscles. Approximately 200 isometric linearly force-varying contractions peaking at 80% of the maximal voluntary contraction level were processed. The results indicated that the myoelectric signal-force relationship was primarily determined by the muscle under investigation and was generally independent of the subject group and the force rate. Whereas this relationship was quasilinear for the first dorsal interosseous, it was nonlinear for the biceps and deltoid. Several possible physiological causes of the observed behavior of the myoelectric signal-force relationship are discussed.     

Residual force enhancement contributes to increased performance during stretch-shortening cycles of human plantar flexor muscles in vivo

It is well known that muscular force production is history-dependent, which results in enhanced (RFE) and depressed (RFD) steady-state forces after stretching and shortening, respectively. However, it remains unclear if force-enhancing mechanisms can contribute to increased performance during in vivo stretch-shortening cycles (SSCs) of human locomotor muscles. The purpose of this study was to investigate whether RFE-related mechanisms contribute to enhanced force and power output during SSCs of the human plantar flexor muscles. Net ankle torques of fourteen participants were measured during and after pure isometric, pure stretch, pure shortening, and SSC contractions when the triceps surae muscles were electrically stimulated at a submaximal level that resulted in 30% of their maximum isometric torque. Dynamic contractions were performed over an amplitude of 15°, from 5° plantar flexion to 10° dorsiflexion, at a speed of 120° s⁻¹. External ankle work during shortening was 11.6% greater during SSCs compared to pure shortening contractions (p = .003). Additionally, RFD after SSCs (8.6%) was reduced compared to RFD after pure shortening contractions (12.0%; p < .05). It is therefore concluded that RFE-related mechanisms contribute to increased performance following SSCs of human locomotor muscles. Since RFD after SSCs decreased although work during shortening was increased, we speculate that the relevant mechanism lies outside actin-myosin interaction. Finally, our data suggests that RFE might be relevant and beneficial for human locomotion whenever a muscle is stretched, but this needs to be confirmed.     

Relationship between mechanomyogram signals and changes in force of human forefinger flexor muscles during voluntary contraction

In previous studies on mechanomyogram (MMG) signals no analysis of these signals accompanying force generation has been performed. Therefore, we have recorded MMG signals (previously referred to as muscle sound or acoustomyographic signals) during voluntary contractions of forefinger flexor muscles in 31 young subjects. These subjects made contractions to produce force records of triangular or trapeziform shape. The peak target force amounted to 10, 20 or 40 N which represented less than 40% of maximal voluntary contraction. The MMG signals during the transient phases of force generation at three different rates were analysed. The MMG intensity level calculated for MMG records and the peak-to-peak amplitude of MMG signals correlated with both the velocity of force increase and the contraction force. The occurrence of the strongest MMG signals corresponded to changes in contractile force. Therefore, it is suggested that measurements of these parameters could be a useful tool in studies of changes in contractile force. Accepted: 11 March 1998     

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.     

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.     

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.     

Modeling the length dependence of isometric force in human quadriceps muscles

Functional electrical stimulation is used to restore movement and function of paralyzed muscles by activating skeletal muscle artificially. An accurate and predictive mathematical model can facilitate the design of stimulation patterns that produce the desired force. The present study is a first step in developing a mathematical model for non-isometric muscle contractions. The goals of this study were to: (1) identify how our isometric force model's parameters vary with changes in knee joint angle, (2) identify the best knee flexion angle to parameterize this model, and (3) validate the model by comparing experimental data to predictions in response to a wide range of stimulation frequencies and muscle lengths. Results showed that by parabolically varying one of the free parameters with knee joint angle and fixing the other parameters at the values identified at 40 degrees of knee flexion, the model could predict the force responses to a wide range of stimulation frequencies and patterns at different muscle lengths. This work showed that the current isometric force model is capable of predicting the changes in skeletal muscle force at different muscle lengths.     

Cellular homeostatic tension and force transmission measured in human engineered tendon

Tendons transmit contractile muscular force to bone to produce movement, and it is believed cells can generate endogenous forces on the extracellular matrix to maintain tissue homeostasis. However, little is known about the direct mechanical measurement of cell-matrix interaction in cell-generated human tendon constructs. In this study we examined if cell-generated force could be detected and quantified in engineered human tendon constructs, and if glycosaminoglycans (GAGs) contribute to tendon force transmission. Following de-tensioning of the tendon constructs it was possible to quantify an endogenous re-tensioning. Further, it was demonstrated that the endogenous re-tensioning response was markedly blunted after interference with the cytoskeleton (inhibiting non-muscle myosin-dependent cell contraction by blebbistatin), which confirmed that re-tensioning was cell generated. When the constructs were elongated and held at a constant length a stress relaxation response was quantified, and removing 27% of the GAG content of tendon did not alter the relaxation behavior, which indicates that GAGs do not play a meaningful role in force transmission within this system.     

EMG and force production of some human shoulder muscles during isometric abduction

Surface EMG was recorded in four subjects on three different occasions from the three parts of the deltoid, the clavicular part of the pectoralis major and from the infraspinatus muscles at different angles of abduction, in the frontal and scapular plane. The integrated EMG was related to the maximum values found for each muscle or muscle part during test contractions (%EMG). Linear relations can be seen for abduction angle vs %EMG. During abduction in the scapular plane the middle and posterior parts of the deltoid muscle showed significantly less activity than in the frontal plane. A simple two dimensional model to calculate the deltoid force out of total external moment at the shoulder is presented. For the middle part of the deltoid an EMG-force relation is presented. The maximal deltoid forces found during test contractions are compared with the absolute muscle force. Also, the length-force relation for the middle part of the deltoid muscle is given between 30° and 90° of abduction.