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 ≈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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Implications of Muscle Relative Position as a Co-Determinant of Isometric Muscle Force

Journal of Mechanics in Medicine and Biology ◽

10.1142/s0219519403000703 ◽

2003 ◽

Vol 03 (02) ◽

pp. 145-168 ◽

Cited By ~ 29

Author(s):

Huub Maas ◽

Can A. Yucesoy ◽

Guus C. Baan ◽

Peter A. Huijing

Keyword(s):

Connective Tissue ◽

Relative Position ◽

Muscle Force ◽

Relevant Literature ◽

Force Transmission ◽

Position Effects ◽

Myofascial Force Transmission ◽

Isometric Muscle ◽

Isometric Muscle Force

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.

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

Journal of Biomechanical Engineering ◽

10.1115/1.1992523 ◽

2005 ◽

Vol 127 (5) ◽

pp. 819-828 ◽

Cited By ~ 37

Author(s):

Can A. Yucesoy ◽

Guus C. Baan ◽

Bart H. F. J. M. Koopman ◽

Henk J. Grootenboer ◽

Peter A. Huijing

Keyword(s):

Muscle Length ◽

Substantial Part ◽

Force Transmission ◽

Myofascial Force Transmission ◽

Extensor Hallucis Longus ◽

Edl Muscle ◽

Force Difference ◽

Force Characteristics

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.

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The Relative Position of EDL Muscle Affects the Length of Sarcomeres Within Muscle Fibers: Experimental Results and Finite-Element Modeling

Journal of Biomechanical Engineering ◽

10.1115/1.1615619 ◽

2003 ◽

Vol 125 (5) ◽

pp. 745-753 ◽

Cited By ~ 53

Author(s):

Huub Maas ◽

Guus C. Baan ◽

Peter A. Huijing ◽

Can A. Yucesoy ◽

Bart H. F. J. M. Koopman ◽

...

Keyword(s):

Finite Element ◽

Finite Element Modeling ◽

Relative Position ◽

Isometric Force ◽

Muscle Fibers ◽

Force Transmission ◽

Connective Tissues ◽

Element Modeling ◽

Myofascial Force Transmission ◽

Edl Muscle

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.

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Synergistic and antagonistic interactions in the rat forelimb: acute effects of coactivation

Journal of Applied Physiology ◽

10.1152/japplphysiol.00328.2009 ◽

2009 ◽

Vol 107 (5) ◽

pp. 1453-1462 ◽

Cited By ~ 14

Author(s):

Huub Maas ◽

Peter A. Huijing

Keyword(s):

Median Nerve ◽

Order Effects ◽

Force Transmission ◽

Dynamic Features ◽

Connective Tissues ◽

Constant Length ◽

Myofascial Force Transmission ◽

Antagonistic Muscles ◽

Wrist Flexors ◽

Stimulation Of

The goals of the present study were 1) to assess effects of antagonist coactivation on mechanical interactions between synergistic muscles, and 2) to quantify the extent of epimuscular myofascial force transmission between synergistic and antagonistic muscles in the rat forelimb. Connective tissues enveloping the muscle bellies in the antebrachium were left intact. Forces exerted at the distal tendons of flexor carpi ulnaris (FCU), palmaris longus (PL), and extensor carpi ulnaris (ECU) muscles were measured at various FCU lengths for two different stimulation protocols: 1) simultaneous stimulation of ulnar/median nerve complex (exciting all wrist flexors, including synergistic FCU and PL) and radial nerve (exciting all wrist extensors, including antagonistic ECU); and 2) stimulation of the ulnar/median nerve exclusively. PL and ECU were kept at a constant length. In addition, muscle forces were measured during stimulation of one of the indicated nerves, with later addition of stimulation of the second nerve during the maintained tetanic contraction. Coactivation of antagonistic muscles increased FCU isometric forces (on average, by 10% of optimal force) and PL forces (on average, by 13% of maximal force), but mechanical interaction between FCU and PL was unchanged. Changing the length and relative position of FCU significantly affected PL (by 20%) as well as ECU forces (by 8%). In addition, distal tetanic force of FCU kept at a constant high length was determined by the order of nerve stimulation onset. These results indicate effects of myofascial pathways between synergistic and antagonistic muscles in the rat forelimb. Coactivation may enhance the stiffness of connective tissues between muscles, but the present data suggest that activation of all wrist flexors already preloaded the myofascial pathways to the greatest extent. The stimulation order effects were explained by dynamic features of muscle and connective tissues (i.e., length-history dependence and viscoelasticity).

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

Journal of Biomechanics ◽

10.1016/s0021-9290(01)00055-0 ◽

2001 ◽

Vol 34 (7) ◽

pp. 927-940 ◽

Cited By ~ 122

Author(s):

Huub Maas ◽

Guus C Baan ◽

Peter A Huijing

Keyword(s):

Tibialis Anterior ◽

Extensor Digitorum Longus ◽

Extensor Digitorum Longus Muscle ◽

Extensor Digitorum ◽

Force Transmission ◽

Myofascial Force Transmission ◽

Longus Muscle ◽

Extensor Hallucis Longus

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

Journal of Mechanics in Medicine and Biology ◽

10.1142/s0219519402000496 ◽

2002 ◽

Vol 02 (03n04) ◽

pp. 405-419 ◽

Cited By ~ 5

Author(s):

PETER A. HUIJING

Keyword(s):

Connective Tissue ◽

Relative Position ◽

Muscle Length ◽

Force Transmission ◽

Muscle Belly ◽

Myofascial Force Transmission ◽

Antagonist Muscles ◽

Length Changes ◽

Edl Muscle

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.

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The likelihood of myofascial force transmission between synergistic and antagonistic muscles in vivo

Journal of Biomechanics ◽

10.1016/s0021-9290(06)83144-1 ◽

2006 ◽

Vol 39 ◽

pp. S65 ◽

Cited By ~ 1

Author(s):

P.A. Huijing

Keyword(s):

Force Transmission ◽

Myofascial Force Transmission ◽

Antagonistic Muscles

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Extramuscular myofascial force transmission within the rat anterior tibial compartment: proximo-distal differences in muscle force

Acta Physiologica Scandinavica ◽

10.1046/j.1365-201x.2001.00911.x ◽

2001 ◽

Vol 173 (3) ◽

pp. 297-311 ◽

Cited By ~ 93

Author(s):

P. A. Huijing ◽

G. C. Baan

Keyword(s):

Muscle Force ◽

Force Transmission ◽

Myofascial Force Transmission ◽

Anterior Tibial

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Significant mechanical interactions at physiological lengths and relative positions of rat plantar flexors

Journal of Applied Physiology ◽

10.1152/japplphysiol.00703.2014 ◽

2015 ◽

Vol 118 (4) ◽

pp. 427-436 ◽

Cited By ~ 21

Author(s):

Michel Bernabei ◽

Jaap H. van Dieën ◽

Guus C. Baan ◽

Huub Maas

Keyword(s):

Relative Position ◽

Isometric Force ◽

Unit Length ◽

Knee Extension ◽

Triceps Surae ◽

Force Transmission ◽

Plantar Flexors ◽

Myofascial Force Transmission ◽

Triceps Surae Muscles ◽

Slack Length

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.

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