INTRA-, EXTRA- AND INTERMUSCULAR MYOFASCIAL FORCE TRANSMISION OF SYNERGISTS AND ANTAGONISTS: EFFECTS OF MUSCLE LENGTH AS WELL AS RELATIVE POSITION

2002 ◽  
Vol 02 (03n04) ◽  
pp. 405-419 ◽  
Author(s):  
PETER A. HUIJING

The concepts of intramuscular myofascial force transmission is reintroduced and reviewed on the basis of experiments involving tenotomy and aponeurotomy of dissected rat EDL muscle studied in situ. Results from experiments with measurements of force of EDL muscle, of which the muscle belly was not dissected (i.e. the muscle is surrounded by its natural connective tissue milieu) are discussed. In such experiments, force was measured at proximal as well as distal EDL tendons. Examples of experimental evidence for both extramuscular and intermuscular myofascial force transmission within the rat anterior crural compartment are presented. Evidence is presented also for differential effects of proximal and distal lengthening on myofascial force transmission from EDL, even for the case in which symmetric length changes were imposed on the muscle. It is shown that myofascial force transmission effects are not limited to synergists located within one compartment, but do also play a very substantial role in the interaction between antagonist muscles in neighbouring anterior crural and peroneal compartments.

2003 ◽  
Vol 03 (02) ◽  
pp. 145-168 ◽  
Author(s):  
Huub Maas ◽  
Can A. Yucesoy ◽  
Guus C. Baan ◽  
Peter A. Huijing

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


2003 ◽  
Vol 125 (5) ◽  
pp. 745-753 ◽  
Author(s):  
Huub Maas ◽  
Guus C. Baan ◽  
Peter A. Huijing ◽  
Can A. Yucesoy ◽  
Bart H. F. J. M. Koopman ◽  
...  

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


2003 ◽  
Vol 95 (5) ◽  
pp. 2004-2013 ◽  
Author(s):  
Huub Maas ◽  
Richard T. Jaspers ◽  
Guus C. Baan ◽  
Peter A. Huijing

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.


2005 ◽  
Vol 127 (5) ◽  
pp. 819-828 ◽  
Author(s):  
Can A. Yucesoy ◽  
Guus C. Baan ◽  
Bart H. F. J. M. Koopman ◽  
Henk J. Grootenboer ◽  
Peter A. Huijing

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±0.11N, where as distal EDL force =1.50±0.08N (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 nonzero 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.


1999 ◽  
Vol 202 (16) ◽  
pp. 2139-2150 ◽  
Author(s):  
R.E. Shadwick ◽  
S.L. Katz ◽  
K.E. Korsmeyer ◽  
T. Knower ◽  
J.W. Covell

Cyclic length changes in the internal red muscle of skipjack tuna (Katsuwonus pelamis) were measured using sonomicrometry while the fish swam in a water tunnel at steady speeds of 1.1-2.3 L s(−)(1), where L is fork length. These data were coupled with simultaneous electromyographic (EMG) recordings. The onset of EMG activity occurred at virtually the same phase of the strain cycle for muscle at axial locations between approximately 0.4L and 0.74L, where the majority of the internal red muscle is located. Furthermore, EMG activity always began during muscle lengthening, 40–50 prior to peak length, suggesting that force enhancement by stretching and net positive work probably occur in red muscle all along the body. Our results support the idea that positive contractile power is derived from all the aerobic swimming muscle in tunas, while force transmission is provided primarily by connective tissue structures, such as skin and tendons, rather than by muscles performing negative work. We also compared measured muscle length changes with midline curvature (as a potential index of muscle strain) calculated from synchronised video image analysis. Unlike contraction of the superficial red muscle in other fish, the shortening of internal red muscle in skipjack tuna substantially lags behind changes in the local midline curvature. The temporal separation of red muscle shortening and local curvature is so pronounced that, in the mid-body region, muscle shortening at each location is synchronous with midline curvature at locations that are 7–8 cm (i.e. 8–10 vertebral segments) more posterior. These results suggest that contraction of the internal red muscle causes deformation of the body at more posterior locations, rather than locally. This situation represents a unique departure from the model of a homogeneous bending beam, which describes red muscle strain in other fish during steady swimming, but is consistent with the idea that tunas produce thrust by motion of the caudal fin rather than by undulation of segments along the body.


2019 ◽  
Vol 126 (5) ◽  
pp. 1465-1473 ◽  
Author(s):  
Huub Maas

In the past 20 yr, force transmission via connective tissue linkages at the muscle belly surface, called epimuscular myofascial force transmission, has been studied extensively. In this article, the effects of epimuscular linkages under passive muscle conditions are reviewed. Several animal studies that included direct (invasive) measurements of force transmission have shown that different connective tissue structures serve as an epimuscular pathway and that these tissues have sufficient stiffness, especially at supraphysiological muscle lengths and relative positions, to transmit substantial passive forces (up to 15% of active optimal force). Exact values of lumped tissue stiffness for different connective tissue structures have not yet been estimated. Experiments using various imaging techniques (ultrasound, MRI, shear wave elastography) have yielded some, but weak, evidence of epimuscular myofascial force transmission for passive muscles in humans. At this point, the functional consequences of epimuscular pathways for muscle and joint mechanics in the intact body are still unknown. Potentially, however, these pathways may affect sensory feedback and, thereby, neuromuscular control. In addition, altered epimuscular force transmission in pathological conditions may also contribute to changes in passive range of joint motion.


2015 ◽  
Vol 118 (4) ◽  
pp. 427-436 ◽  
Author(s):  
Michel Bernabei ◽  
Jaap H. van Dieën ◽  
Guus C. Baan ◽  
Huub Maas

In situ studies involving supraphysiological muscle lengths and relative positions have shown that connective tissue linkages connecting adjacent muscles can transmit substantial forces, but the physiological significance is still subject to debate. The present study investigates effects of such epimuscular myofascial force transmission in the rat calf muscles. Unlike previous approaches, we quantified the mechanical interaction between the soleus (SO) and the lateral gastrocnemius and plantaris complex (LG+PL) applying a set of muscle lengths and relative positions corresponding to the range of knee and ankle angles occurring during normal movements. In nine deeply anesthetized Wistar rats, the superficial posterior crural compartment was exposed, and distal and proximal tendons of LG+PL and the distal SO tendon were severed and connected to force transducers. The target muscles were excited simultaneously. We found that SO active and passive tendon force was substantially affected by proximally lengthening of LG+PL mimicking knee extension (10% and 0.8% of maximal active SO force, respectively; P < 0.05). Moreover, SO relative position significantly changed the LG+PL length-force relationship, resulting in nonunique values for passive slack-length and optimum-length estimates. We conclude that also, for physiological muscle conditions, isometric force of rat triceps surae muscles is determined by its muscle-tendon unit length as well as by the length and relative position of its synergists. This has implications for understanding the neuromechanics of skeletal muscle in normal and pathological conditions, as well as for studies relying on the assumption that muscles act as independent force actuators.


2012 ◽  
Vol 134 (11) ◽  
Author(s):  
Can A. Yucesoy ◽  
Önder Emre Arıkan ◽  
Filiz Ateş

Measurement of forces of mono- and bi-articular muscles of an entire intact muscle compartment can allow for a comprehensive assessment of the effects of Botulinum toxin type A (BTX-A) both at and beyond the injection site, and in conditions close to those in vivo. The goal was to test the hypotheses that BTX-A affects (1) the forces of not only the injected but also the noninjected muscles of the compartment, and (2) epimuscular myofascial force transmission (EMFT). Two groups of Wistar rats were tested: Control (no BTX-A injected) and BTX (0.1 units of BTX-A were injected exclusively to the mid-belly of TA). Isometric forces were measured simultaneously at the distal tendons of the tibialis anterior (TA) at different lengths, the restrained extensor digitorum longus (EDL) and the extensor hallucis longus (EHL) muscles and at the proximal tendon of EDL. Five days post-injection, BTX-A did affect the total forces of all muscles significantly: (1) The TA force decreased differentially (by 46.6%–55.9%) for most lengths such that a significant negative correlation was found between force reductions and increased muscle length. The maximum TA force decreased by 47.3%. However, the muscle’s length range of force production did not change significantly. (2) Distal and proximal EDL forces decreased (on average by 67.8% and 62.9%, respectively). (3) The EHL force also decreased (on average by 9.2%). The passive forces of only the TA showed a significant increase at higher lengths. EMFT effects were shown for the control group: (1) at the shortest TA lengths, the EDL proximo-distal force differences were in favor of the distal force, which was reversed at higher lengths. (2) the EHL force measured at the shortest TA length decreased (by 34%) as a function of TA lengthening. After BTX-A exposure, such EMFT effects disappeared for the EDL, whereas they remained as profound for the EHL. Exposure to BTX-A does affect forces of all muscles operating in an intact compartment. For the BTX-A injected muscle, the reduction in muscle force becomes less pronounced at higher muscle lengths. BTX-A also has effects on EMFT, however, these effects are not uniform within the anterior crural compartment. Decreased forces of the noninjected synergistic muscles suggest the presence of unintended additional effects of BTX-A both for the targeted distal joint and for the nontargeted proximal joint.


2003 ◽  
Vol 94 (3) ◽  
pp. 1092-1107 ◽  
Author(s):  
Peter A. Huijing ◽  
Guus C. Baan

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 ≈118%) after distal than after equal proximal lengthening. For proximal force, the reverse occurred (ratio ≈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 ≈ −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.


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