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TECHNICAL PAPERS: Joint/Whole Body

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

[+] Author and Article Information
Can A. Yucesoy1

Instituut voor Fundamentele en Toegepaste Bewegingswetenschappen, Faculteit Bewegingswetenschappen,  Vrije Universiteit, Amsterdam, The Netherlands and Integrated Biomedical Engineering for Restoration of Human Function, Faculteit Constructieve Technische Wetenschappen,  Universiteit Twente, Enschede, The Netherlands and Biomedical Engineering Institute,  Boğaziçi University, Istanbul, Turkey

Guus C. Baan

Instituut voor Fundamentele en Toegepaste Bewegingswetenschappen, Faculteit Bewegingswetenschappen,  Vrije Universiteit, Amsterdam, The Netherlands

Bart H. Koopman, Henk J. Grootenboer

Integrated Biomedical Engineering for Restoration of Human Function, Faculteit Constructieve Technische Wetenschappen,  Universiteit Twente, Enschede, The Netherlands

Peter A. Huijing

Instituut voor Fundamentele en Toegepaste Bewegingswetenschappen, Faculteit Bewegingswetenschappen,  Vrije Universiteit, Amsterdam, The Netherlands and Integrated Biomedical Engineering for Restoration of Human Function, Faculteit Constructieve Technische Wetenschappen,  Universiteit Twente, Enschede, The Netherlands

1

Corresponding author. Can A. Yucesoy, currently at: Biomedical Engineering Institute, Boğaziçi University, 34342, Bebek - Istanbul, Turkey Fax: +90 212 257 50 30. Email address: can.yucesoy@boun.edu.tr

J Biomech Eng 127(5), 819-828 (May 18, 2005) (10 pages) doi:10.1115/1.1992523 History: Received December 15, 2003; Revised May 18, 2005

## Abstract

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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Topics: Force , Muscle

## Figures

Figure 1

Schematic representation of the experimental setup and the extramuscular connections of the muscles tested. (a) Orientation of the experimental muscles, the leg and the foot in the reference position (i.e., knee joint at 100° and the ankle joint at 90°). (b) The experimental setup used in the first part of the experiment. The Kevlar threads tied to the proximal and distal tendons of EDL, as well as to the distal tendon of EHL muscle were connected to force transducers (FT). Note that before the second part of the experiment EDL muscle was removed fully and EHL force was measured exclusively. (c) Schematic representation of an example of EDL muscle extramuscular myofascial connections exclusively. The tied four distal EDL tendons were connected to a force transducer (FT). Before measuring the length-force characteristics of EHL muscle this force transducer was displaced by 2 mm in the proximal direction with respect to its reference position. It was kept at this location throughout the experiment. The proximal EDL tendon was connected to another force transducer. The position of this proximal transducer was not altered during any part of the experiment. The links drawn connecting EDL muscle to the mechanical ground symbolize the extramuscular connective tissue. Note that the neurovascular tract to EDL muscle, as well as (a part of) the anterior intermuscular septum and interosseal membrane comprise the extramuscular connections of this muscle. (d) Schematic representation of EHL muscle. Its fibers originate from the anterior intermuscular septum and insert on a distal aponeurosis (not shown). In addition the connective tissue matrix of the muscle belly is connected to the septum by its extramuscular myofascial connections. The extramuscular connections of EHL muscle consist of the neurovascular tract to this muscle, anterior intermuscular septum and interosseal membrane. Note that the anterior intermuscular septum is connected to bone at its proximal and distal ends, but also has elastic connections laterally to the general fascia as well as medially to the interosseal membrane. The distal EHL tendon was repositioned in the experiment in order to measure isometric EHL forces at different muscle–tendon complex lengths.

Figure 2

EHL length-force characteristics and EHL length dependence of EDL force. (a) The isometric muscle total and passive length-force curves of EHL muscle. Isometric muscle force was measured at the distal tendon of the EHL muscle tendon complex after distal lengthening. (b) and (c) EHL length dependence of total and passive EDL force measured at distal as well as at proximal EDL tendons, respectively. Both distal EDL total force (b) and proximal EDL total force (c) show a significant decrease after EHL lengthening. Length is expressed as a function of deviation (Δl EHL) from active slack length. Mean results and standard errors of the mean (n=10) are shown. EHL muscle–tendon complex length is expressed as deviation from active slack length.

Figure 3

The EHL length dependence of the proximodistal EDL force difference. The proximo-distal EDL total force difference is the difference in the EDL total force measured at the distal tendon and the EDL total force measured at the proximal tendon (i.e., Fdist−Fprox). The proximo-distal EDL total force difference measured at different EHL lengths was normalized for the proximo-distal EDL total force difference measured at EHL active slack length (ΔFmi EDL distal-proximal). EHL length is expressed as deviation (Δl EHL) from active slack length. Mean results and standard errors of the mean (n=10) are shown. Note that the EDL proximo-distal total force difference decreases with increasing EHL length (distal lengthening), but remains present at all EHL lengths.

Figure 4

Effects of full removal of EDL on EHL length force characteristics. The isometric muscle total and passive length-force curves of EHL muscle measured in the first part of the experiment (i.e., when EDL is intact) are compared to those measured in the second part of the experiment (i.e., after removing EDL muscle). Isometric muscle force was measured at the distal tendon of the EHL muscle tendon complex after distal lengthening. Length is expressed as a function of deviation (Δl EHL) from the active slack length. Mean results and standard errors of the mean (n=10) are shown.

Figure 5

Finite element modeling results for EHL with prestrained extramuscular connections exclusively. (a) The model of rat EHL muscle with extramuscular connections. The geometry of the modeled muscle is defined by the contour of a longitudinal slice of the rat EHL muscle belly. The muscle model is composed of three muscle elements arranged in-series and two in parallel. The elements representing the muscles' extramuscular connections are shown with gray lines. The ends of these links, not connected to the muscle belly, are connected to mechanical ground (i.e., constrained in all degrees of freedom). The proximal aponeurosis elements represent the part of the anterior intermuscular septum from which all EHL muscle fibers originate. This end of the modeled muscle was constrained in all directions. The length changes of the modeled muscle were introduced by moving the distal end. Distributions of fiber direction strain within the fiber mesh of the modeled EHL muscle are shown at high (b) and at low muscle lengths (c). The local fiber direction as well as the proximal and distal ends of the muscle are indicated (c). Muscular geometry at the initial muscle length is represented by dotted lines.

Figure 6

Schematic illustration of the effects of prestrained extramuscular connections. Note that only extramuscular connections are shown. (a) Extramuscular connections of EDL without any pre-strain. Our present experimental results indicate that these connections are not in a neutral position when both proximal and distal EDL tendons are at reference position. If this were the case, initially the extramuscular force (Fext) would be zero (upper panel). After shortening of the muscle by moving the distal tendon in the proximal direction, the nonzero extramuscular force would be directed distally. This would lead to an extramuscular force favoring proximal force (i.e., in distal direction). Note that this is an effect opposite to our experimental result (Fdist>Fprox for this condition). Therefore, the extramuscular connections EDL must be pre-strained at reference position to exert an extramuscular force in the proximal direction (lower panel). (b) Extramuscular connections of EDL with pre-strain. If these connections are pre-strained, with both proximal and distal EDL tendons are at reference position, Fext will be non-zero. It will be acting on the muscle in proximal direction leading to Fdist>Fprox (upper panel). Although, after shortening of the muscle by moving the distal tendon in the proximal direction the magnitude of Fext will be decreased, it will remain non-zero and directed proximally, provided that the pre-strain at reference position is large enough to accommodate the imposed length changes. This will yield Fdist>Fprox, which is in accordance with our present experimental results (lower panel).

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