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Myofascial force transmission
Myofascial force transmission An introduction
3.2
Peter A Huijing
Intramuscular substrates of myofascial force transmission Endomysia constitute tubes for each myofiber. Note, however, that endomysial walls are shared between adjacent tubes (and myofibers). This causes a continuous honeycomb type of structure of muscular connective tissues until the fascicle borders are reached (see Chapter 1.1). The collections of fascicles are made up in a similar way, having the perimysium as borders delimiting fascicles, so that within a muscle a stroma of continuous tubes is present that is delimited by the epimysium, surrounding the whole muscle. Myofascial force transmission limited to the intramuscular domain is called intramuscular myofascial force transmission. This term is used also in the case of force transmission of a single myofiber or fascicle operating within its endomysial or perimysial tunnels (Ch. 8.4). In those cases, and that of a fully dissected muscle, reaction forces have to be exerted via tendons as these are then the only effective connections to the outside world (Huijing et al. 1998).
Epimuscular myofascial force transmission and its substrate If a myofascial load (reaction force from fascial structures) is exerted onto muscle (Huijing & Baan 2001), force is transmitted onto the intramuscular
Q 2012, Elsevier Ltd.
stroma via the epimysium. Therefore, such transmission is called epimuscular myofascial force transmission. Two pathways are available for such transmission:
• Directly between two adjacent muscles (occurring exclusively within a muscle group: synergistic muscles). We call this specific case intermuscular myofascial force transmission. • Between a muscle and some extramuscular structures, such as the neurovascular tract (i.e., the collagen-reinforced structure in which blood vessels, lymphatics and nerves are embedded), intermuscular septa between muscle groups, interosseal membrane, periosteum, general (or deep) fascia, etc. We call this extramuscular myofascial force transmission to emphasize the role of extramuscular tissues. Forces exerted this way may play a role in stabilizing joints, or be exerted on bones and other extramuscular structures, but may also be exerted at other muscles. All of the tissues discussed above (with the exception of the aponeuroses and tendons) are part of a continuous fascial system. By itself, the fact that they are connected will not warrant force transmission; if the connections are very compliant (i.e., not stiff), force will only be transmitted after very high length changes that will stiffen connections. However, experiments indicate that also after more moderate length changes sizable fractions of muscular force may be transmitted. This means that fascial structures that are not dense depositions of collagen fibers may transmit some muscular force, and therefore it has been argued that the term “loose connective
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tissue” for such structures is inadequate (Huijing & Langevin 2009) and the term “areolar” is preferred for such tissues.
Effects of epimuscular myofascial force transmission Proximo-distal force differences Due to additional myofascial loading, forces exerted at the origin and insertion of muscle are not equal (Huijing & Baan 2001). The net myofascial load (i.e., the vector sum of all such loads, involving size and direction) will keep sarcomeres at one end of myofibers within muscle longer than at other locations within the same myofibers, i.e., different active forces exerted locally (Fig. 3.2.1A). A force equal to the additional load is integrated into the force exerted at the opposite end of the muscle. Active force of several muscles may appear also at the insertion of another muscle, as long as myofascial connections to the extratendinous tissues are intact (Rijkelijkhuizen et al. 2005, 2009). Proximally directed net myofascial load
Distributions of sarcomere lengths within muscle and its myofibers Myofascial loading will cause a distribution of lengths of sarcomeres arranged in series within myofibers (serial distribution). Most of such additional force is borne by active sarcomeres (since they are very stiff), but may also be borne by the connective tissue stroma of muscle and will be added to the active force exerted. If the point of application of myofascial loads on myofibers and their size and direction were identical, sarcomere length distributions would be limited to serial ones. However, a simple test illustrates that the situation is more complex. If one suspends equal masses from the tendon of a (horizontal) muscle, the muscle is pulled down exposing the extramuscular neurovascular tract (Plate 3.2.1A), but this tract is pulled down more at the distal tendon than at the proximal tendon. This indicates that the tract is stiffer at the proximal side of the muscle. As a consequence, myofibers located proximally within muscle will, on average, be longer than more distal ones. Therefore, parallel distributions of sarcomere lengths will be present as well. The nature of both types of distributions will vary with the specific conditions of myofascial loading. It is hard Fig. 3.2.1 • Myofascial force transmission and some of its consequences. (A) Proximo-distal force differences. The net myofascial load on the muscle is integrated into either the proximal force (left panel) or the distal force (right panel) depending on the loading direction. (B) Comparison of distal forces of unconnected and myofascially connected muscles after distal lengthening. As the agonistic muscle is lengthened the force in the synergistic muscle drops. (C) Connections and myofascial loading of antagonistic muscles across the intermuscular septum. In these conditions part of the antagonistic muscle force will be exerted at the distal tendon (right) of the agonistic muscle.
Distally directed net myofascial load
Prox
Dist
Lower force
Higher force
Prox
Dist Lower force
A
Synergist unconnected Synergist connected Agonist connected Agonist unconnected B Antagonist
Intermuscular septum
Agonist Synergist
C
118
After
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to measure such distributions, but finite element modeling (Ch. 8.5) allows the study of such principles even in quite complex conditions of loading.
Myofascial interaction between muscles Dissection experiments (Maas et al. 2005) indicate that intermuscular transmission plays a role, but extramuscular myofascial force transmission is the more important mechanism for muscular interaction. Intermuscular mechanical effects are present through two coupled events of extramuscular myofascial force transmission (muscle to extramuscular tissues to another muscle). Myofascial interaction was shown for synergistic muscles involving both intermuscular and extramuscular transmission (Huijing & Baan 2001; Huijing 2003). During experiments this is apparent as follows: After the agonistic muscle is lengthened at its distal tendon while its synergistic muscle is kept at constant length (Plate 3.2.1B), distal force of the isometric synergistic muscle is decreased (compared to the unconnected case) with increasing lengths of its adjacent muscle. The lengthened muscle creates, or enhances, a distally directed myofascial load on the isometric synergistic muscle. At its proximal tendon, this load is integrated into force exerted by the muscle (as in Plate 3.2.1A). In contrast, distally exerted force is decreased because of such loading conditions. Myofascial force transmission between antagonistic muscles is (by definition) only possible via extramuscular mechanisms, as such muscles are separated by compartment walls. Stiff connections are made between compartments by neurovascular tracts, but also other extramuscular fascial structures are expected to play a role. The effects and explanation of myofascial interaction between two muscle groups located at opposite sides of an intermuscular septum or interosseal membrane (Plate 3.2.1B) are similar to those described for synergistic muscles (Huijing 2007; Huijing et al. 2007; Meijer et al. 2007, Rijkelijkhuizen et al. 2007). In a series of experiments in rats, we have shown that such mechanisms and effects are active between all muscles of the lower leg (for an overview of results, see Rijkelijkhuizen et al. 2009). So, even antagonistic muscles located at opposite sides of the leg interact (e.g., m. tibialis anterior and triceps surae muscles, see Ch. 5.8 for similar physiological results in mice), and cannot be considered as fully independent entities. It should be realized that this means that part of the force exerted by active sarcomeres within a muscle may be
CHAPTER 3.2
exerted at the tendon of its antagonistic muscle. In fact, the proximal sarcomeres of myofibers are in series not only with more distal sarcomeres of the same myofiber, but via myofascial loading also with distal sarcomeres (and their adjacent endomysia) in the lengthened antagonistic muscle(s). It is evident that the classical concept of antagonistic muscles (as having opposite mechanical effects) and the nomenclature used to describe them is due for a fundamental update. . . that, however, is beyond the scope of the present chapter.
Muscular relative position also affects muscular force exertion Experiments (Huijing 2002; Maas et al. 2004), as well as finite element modeling (Maas et al. 2003a,b; Yucesoy et al. 2006), indicate that a muscle kept at constant length and moved through its natural fascial context exerts tendon forces in proximal or distal direction that will vary according to the myofascial loading conditions that are altered with changes in relative position (Fig. 3.2.2). Relative movement between synergistic muscles occurs due to differences in moment arms at joints crossed, and for bi- or polyarticular muscles due to movement in a joint not crossed by its adjacent monoarticular synergistic muscle. Relative movement of antagonistic muscles is the order of the day, since movement of a joint will have opposite effects on Muscle
Muscle
Fprox < Fdist
Fprox = Fdist
Extramuscular structure Muscle
Fprox > Fdist
Fig. 3.2.2 • Schematic example of effects of relative position on myofascial connections and loading. As the muscle of constant length is moved its relative position is changed with respect to other structures (e.g., other muscles or extramuscular structures). The effects for myofascial connections and the direction of loading on the muscle are indicated with the consequences for muscle force exerted at proximal (left) and distal (right) tendons.
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muscular length: e.g., joint flexion will lengthen its extensor muscles and shorten its flexor muscles.
Complexity of myofascial loading of muscle Above, we have provided the simplest examples of myofascial loading to clarify its principles. In reality, within the integrated myofascial system loading of muscles will be very complex. Multiple and opposite loads on a muscle are considered common (for example, a proximally directed load by the neurovascular tract and a distally directed load by compartmental fascia). The latter is particularly evident for shorter muscles, but also present at higher lengths. If one cuts a tendon (Chapter 5.4), its passive muscle retracts somewhat. If such tenotomized muscle is activated, it will shorten only a little more, indicating a distal myofascial load keeping the muscle at length. By changing the length and position of muscles, the direction of net loading may change because of (1) rotating a fascial component with respect to muscle or (2) making the mechanical effects of another fascial structure dominant. If simultaneously exerted proximal and distal myofascial loads on a muscle are equal, the proximo-distal force difference will be zero. Therefore, the presence of such a difference constitutes absolute proof of epimuscular myofascial force transmission, but its absence does not necessarily mean that such force transmission is missing! Since myofascial loading of a muscle under consideration may originate from all muscles with the body segment, it is clear that a lot needs to be known before the conditions determining the target muscle’s force are specified in detail. In addition, myofascial force transmission between muscles in adjacent segments is likely, because of the stiffness of the neurovascular tract coursing through the tissues of the body segments. There are some indications that inter-segmental myofascial transmission occurs (Vleeming et al. 1995; Huijing et al. 2009), but this needs further confirmation, particularly for living and active muscles (Huijing 2009). Experiments and modeling performed so far have had proving the feasibility of epimuscular myofascial force transmission and its basic effects and principles as their goal. Therefore, it is clear that we have only scratched at the surface of this intricate and complex system and a lot more scientific and clinical work is needed to reveal the principles of its complexity. 120
Additional factors to consider Experimental work discussed above has many limitations that need to be considered in a more generalized view. It is good to realize that the control needed for solid experimental proof precludes getting close to in-vivo conditions. At the same time, if one experiments in vivo in human or animal studies, it is often impossible to attain sufficient control of the conditions.
Joint movement Joint movement (not included in experiments described above) affects actual stiffness of fascial components; e.g., the length and, particularly, tension within neurovascular tracts are very dependent on joint positions (Huijing 2009). Therefore, a recent study (Maas & Sandercock 2008) extending experiments (to cats) and including actual joint movement constitutes a real contribution to the field. Evidence of epimuscular myofascial force transmission between synergistic muscles of the calf was reported only if soleus muscle was at a length deviating from that imposed by the specific ankle angle. Maas and Sandercock (2008) concluded that epimuscular myofascial force transmission does not occur in physiological conditions in vivo, but may play a role when conditions deviate from normal. There is no doubt of the validity of their finding. However, in its generality, their conclusion about myofascial force transmission occurring exclusively in non-physiological conditions is premature, as evident also from emerging magnetic resonance imaging work in humans (Yaman et al. 2009; Huijing et al. 2011) with similar experiments: changing the knee angle caused local changes of strain, not only in gastrocnemius muscle, but also in synergistic soleus muscle kept at constant length due to a fixed ankle angle. The same was found for the full remainder of antagonistic muscles of the lower leg that also do not cross the knee. Previously, some other studies indicated evidence of in-vivo epimuscular myofascial force transmission (Yu et al. 2007). One could argue, as was done by Herbert and co-authors (2008), that if only a small percentage of muscle force is transmitted myofascially, we could afford to neglect the whole process. However, having epimuscular myofascial force transmission as a fundamental mechanism of intact tissues completely changes the view of functioning of those
Myofascial force transmission
tissues, even if the size of the related phenomena may be small in specific conditions.
Levels of muscular activation One important aspect of the work discussed is that even though different levels of activation have been studied by varying firing rates of muscles (Meijer et al. 2006; 2008), such changes were always imposed uniformly on all muscle studied. In vivo, different muscles or muscle groups are active at varying levels of activation. By stimulating different nerves or their branches (Maas & Huijing 2009) this may be mimicked. Those results do not affect the principles as described above in a major way.
Effects on functioning of the sensory apparatus As our view of in-series and parallel arrangements of structures is renewed, it is clear that our views on neural sensors need to be adapted as well: many more
CHAPTER 3.2
receptors outside of muscle (e.g., in periosteum, intermuscular septa, compartment) will receive information about muscular conditions. Also intramuscularly, conditions for receptors may be different than thought previously. Classically, muscle spindles are considered as arranged in parallel to myofibers, and Golgi tendon organs as arranged in series with them. However, if a part of the stroma that contains muscle spindles is in series with sarcomeres, this receptor will also operate in series. Preliminary results indicate that this may be the case (Arıkan et al. 2009). In any case, in accordance with results on epimuscular myofascial force transmission, receptors in muscle kept at constant muscle-tendon complex length increase their firing rates, as other muscles within the same segment are lengthened. The most important basic principles of epimuscular myofascial force transmission have been discussed. On the basis of that, the conclusion is warranted that if we do not take such force transmission into account we will never fully understand muscular function. Similarly, it is likely that at least acute effects of manual therapy (Chapter 8.5) will involve some of these mechanisms.
References ¨ .E., Huijing, P.A., Gu ¨¸clu ¨, B., Arıkan, O Yucesoy, C.A., 2009. Altered afferent response of restrained antagonistic muscles after passive stretching of gastrocnemius indicates a remarkable role of epimuscular myofascial force transmission in the sensory level. In: Society for Neuroscience’s meeting. Chicago, IL. Herbert, R.D., Hoang, D., Gandevia, S.C., 2008. Are muscles mechanically independent? J. Appl. Physiol. 104, 1549–1550. Huijing, P.A., 2002. Intra-, extra- and intermuscular myofascial force transmission of synergists and antagonists: effects of muscle length as well as relative position. International Journal of Mechanics in Medicine and Biology 2, 1–15. Huijing, P.A., 2003. Muscular force transmission necessitates a multilevel integrative approach to the analysis of function of skeletal muscle. Exerc. Sport Sci. Rev. 31, 167–175.
Huijing, P.A., 2007. Epimuscular myofascial force transmission between antagonistic and synergistic muscles can explain movement limitation in spastic paresis. J. Electromyogr. Kinesiol. 17, 708–724. Huijing, P.A., 2009. ISB Muybridge Award lecture 2007: Epimuscular myofascial force transmission, its ubiquitous presence across species and some of its history, effects and functional consequences. J. Biomech. 42, 9–21. Huijing, P.A., Baan, G.C., 2001. Extramuscular myofascial force transmission within the rat anterior tibial compartment: Proximo-distal differences in muscle force. Acta Physiol. Scand. 173, 1–15. Huijing, P.A., Langevin, H.M., 2009. Communicating about fascia: history, pitfalls and recommendations. In: Huijing, P.A., Hollander, P., Findley, T.W., Schleip, R. (Eds.), Fascia research II. Basic science and implications
for conventional and complementary ¨nchen. health care. Elsevier, Mu Huijing, P.A., Baan, G.C., Rebel, G., 1998. Non myo-tendinous force transmission in rat extensor digitorum longus muscle. J. Exp. Biol. 201, 682–691. Huijing, P.A., Langenberg, R.W., van de Meesters, J.J., Baan, G.C., 2007. Extramuscular myofascial force transmission also occurs between synergistic muscles and antagonistic muscles. J. Electromyogr. Kinesiol. 17, 680–689. Huijing, P.A., Yaman, A., Ozturk, C.O., Yucesoy, C., 2011. Effects of knee joint angle on global and local strains within human triceps surae muscle: MRI analysis indicating in vivo myofascial force transmission between synergistic muscles. Surg. Radiol. Anat. in press. doi: 10.1007/s00276-0110863-1. Maas, H., Huijing, P.A., 2009. Synergistic and antagonistic interactions in the rat forelimb: acute effects of
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coactivation. J. Appl. Physiol. 107, 1453–1462. Maas, H., Sandercock, T.G., 2008. Are skeletal muscles independent actuators? Force transmission from soleus muscle in the cat. J. Appl. Physiol. 104, 1557–1567. Maas, H., Yucesoy, C.A., Baan, G.C., Huijing, P.A., 2003a. Implications of muscle relative position as a codeterminant of isometric muscle force: a review and some experimental results. J. Mech. Med. Biol. 3, 145–168. Maas, H., Baan, G.C., Huijing, P.A., et al., 2003b. The relative position of EDL muscle affects the length of sarcomeres within muscle fibers: experimental results and finiteelement modeling. J. Biomech. Eng. 125, 745–753. Maas, H., Baan, G.C., Huijing, P.A., 2004. Muscle force is determined also by muscle relative position: isolated effects. J. Biomech. 37, 99–110. Maas, H., Meijer, H.J.M., Huijing, P.A., 2005. Intermuscular interaction between synergists in rat originates from both intermuscular and extramuscular myofascial force transmission. Cells Tissues Organs 181, 38–50. Meijer, H.J.M., Baan, G.C., Huijing, P.A., 2006. Myofascial force transmission is increasingly important at lower forces: firing
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frequency-related length-force characteristics. Acta Physiol. (Oxf.) 186, 185–195. Meijer, H.J.M., Baan, G.C., Huijing, P.A., 2007. Myofascial force transmission between antagonistic rat lower limb muscles: effects of single muscle or muscle group lengthening. J. Electromyogr. Kinesiol. 17, 698–707. Meijer, H.J., Rijkelijkhuizen, J.M., Huijing, P.A., 2008. Effects of firing frequency on length-dependent myofascial force transmission between antagonistic and synergistic muscle groups. Eur. J. Appl. Physiol. 104, 501–513. Rijkelijkhuizen, J.M., Baan, G.C., de Haan, A., et al., 2005. Extramuscular myofascial force transmission for in situ rat medial gastrocnemius and plantaris muscles in progressive stages of dissection. J. Exp. Biol. 208, 129–140. Rijkelijkhuizen, J.M., Meijer, H.J.M., Baan, G.C., Huijing, P.A., 2007. Myofascial force transmission also occurs between antagonistic muscles located in opposite compartments of the rat hindlimb. J. Electromyogr. Kinesiol. 17, 690–697. Rijkelijkhuizen, J.M., Baan1, G.C., de Haan, A., de Ruiter C.J., Huijing, P.A., 2009. Extramuscular myofascial force transmission for in situ rat medial gastrocnemius
and plantaris muscles in progressive stages of dissection. J. Exp. Biol. 208, 129–140. Vleeming, A., Pool-Goudzwaard, A.L., Stoeckart, R., et al., 1995. The posterior layer of the thoracolumbar fascia. Its function in load transfer from spine to legs. Spine 20, 753–758. Yaman, A., Ledesma-Carbayo, M., Baan, G.C., et al., 2009. Assessment using MRI shows that inter-synergistic as well as inter-antagonistic epimuscular myofascial force transmission has sizable effects within the entire human lower leg, in vivo. In: Huijing, P.A., Hollander, P., Findley, T.W., Schleip, R. (Eds.), Fascia research II. Basic science and implications for conventional and complementary health care. ¨nchen. Elsevier, Mu Yu, W.S., Kilbreath, S.L., Fitzpatrick, R.C., Gandevia, S.C., 2007. Thumb and finger forces produced by motor units in the long flexor of the human thumb. J. Physiol. 583, 1145–1154. Yucesoy, C.A., Maas, H., Koopman, B.H., Grootenboer, H.J., Huijing, P.A., 2006. Mechanisms causing effects of muscle position on proximo-distal muscle force differences in extra-muscular myofascial force transmission. Med. Eng. Phys. 28, 214–226.
3.2
Peter A Huijing
Intramuscular substrates of myofascial force transmission Endomysia constitute tubes for each myofiber. Note, however, that endomysial walls are shared between adjacent tubes (and myofibers). This causes a continuous honeycomb type of structure of muscular connective tissues until the fascicle borders are reached (see Chapter 1.1). The collections of fascicles are made up in a similar way, having the perimysium as borders delimiting fascicles, so that within a muscle a stroma of continuous tubes is present that is delimited by the epimysium, surrounding the whole muscle. Myofascial force transmission limited to the intramuscular domain is called intramuscular myofascial force transmission. This term is used also in the case of force transmission of a single myofiber or fascicle operating within its endomysial or perimysial tunnels (Ch. 8.4). In those cases, and that of a fully dissected muscle, reaction forces have to be exerted via tendons as these are then the only effective connections to the outside world (Huijing et al. 1998).
Epimuscular myofascial force transmission and its substrate If a myofascial load (reaction force from fascial structures) is exerted onto muscle (Huijing & Baan 2001), force is transmitted onto the intramuscular
Q 2012, Elsevier Ltd.
stroma via the epimysium. Therefore, such transmission is called epimuscular myofascial force transmission. Two pathways are available for such transmission:
• Directly between two adjacent muscles (occurring exclusively within a muscle group: synergistic muscles). We call this specific case intermuscular myofascial force transmission. • Between a muscle and some extramuscular structures, such as the neurovascular tract (i.e., the collagen-reinforced structure in which blood vessels, lymphatics and nerves are embedded), intermuscular septa between muscle groups, interosseal membrane, periosteum, general (or deep) fascia, etc. We call this extramuscular myofascial force transmission to emphasize the role of extramuscular tissues. Forces exerted this way may play a role in stabilizing joints, or be exerted on bones and other extramuscular structures, but may also be exerted at other muscles. All of the tissues discussed above (with the exception of the aponeuroses and tendons) are part of a continuous fascial system. By itself, the fact that they are connected will not warrant force transmission; if the connections are very compliant (i.e., not stiff), force will only be transmitted after very high length changes that will stiffen connections. However, experiments indicate that also after more moderate length changes sizable fractions of muscular force may be transmitted. This means that fascial structures that are not dense depositions of collagen fibers may transmit some muscular force, and therefore it has been argued that the term “loose connective
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tissue” for such structures is inadequate (Huijing & Langevin 2009) and the term “areolar” is preferred for such tissues.
Effects of epimuscular myofascial force transmission Proximo-distal force differences Due to additional myofascial loading, forces exerted at the origin and insertion of muscle are not equal (Huijing & Baan 2001). The net myofascial load (i.e., the vector sum of all such loads, involving size and direction) will keep sarcomeres at one end of myofibers within muscle longer than at other locations within the same myofibers, i.e., different active forces exerted locally (Fig. 3.2.1A). A force equal to the additional load is integrated into the force exerted at the opposite end of the muscle. Active force of several muscles may appear also at the insertion of another muscle, as long as myofascial connections to the extratendinous tissues are intact (Rijkelijkhuizen et al. 2005, 2009). Proximally directed net myofascial load
Distributions of sarcomere lengths within muscle and its myofibers Myofascial loading will cause a distribution of lengths of sarcomeres arranged in series within myofibers (serial distribution). Most of such additional force is borne by active sarcomeres (since they are very stiff), but may also be borne by the connective tissue stroma of muscle and will be added to the active force exerted. If the point of application of myofascial loads on myofibers and their size and direction were identical, sarcomere length distributions would be limited to serial ones. However, a simple test illustrates that the situation is more complex. If one suspends equal masses from the tendon of a (horizontal) muscle, the muscle is pulled down exposing the extramuscular neurovascular tract (Plate 3.2.1A), but this tract is pulled down more at the distal tendon than at the proximal tendon. This indicates that the tract is stiffer at the proximal side of the muscle. As a consequence, myofibers located proximally within muscle will, on average, be longer than more distal ones. Therefore, parallel distributions of sarcomere lengths will be present as well. The nature of both types of distributions will vary with the specific conditions of myofascial loading. It is hard Fig. 3.2.1 • Myofascial force transmission and some of its consequences. (A) Proximo-distal force differences. The net myofascial load on the muscle is integrated into either the proximal force (left panel) or the distal force (right panel) depending on the loading direction. (B) Comparison of distal forces of unconnected and myofascially connected muscles after distal lengthening. As the agonistic muscle is lengthened the force in the synergistic muscle drops. (C) Connections and myofascial loading of antagonistic muscles across the intermuscular septum. In these conditions part of the antagonistic muscle force will be exerted at the distal tendon (right) of the agonistic muscle.
Distally directed net myofascial load
Prox
Dist
Lower force
Higher force
Prox
Dist Lower force
A
Synergist unconnected Synergist connected Agonist connected Agonist unconnected B Antagonist
Intermuscular septum
Agonist Synergist
C
118
After
Myofascial force transmission
to measure such distributions, but finite element modeling (Ch. 8.5) allows the study of such principles even in quite complex conditions of loading.
Myofascial interaction between muscles Dissection experiments (Maas et al. 2005) indicate that intermuscular transmission plays a role, but extramuscular myofascial force transmission is the more important mechanism for muscular interaction. Intermuscular mechanical effects are present through two coupled events of extramuscular myofascial force transmission (muscle to extramuscular tissues to another muscle). Myofascial interaction was shown for synergistic muscles involving both intermuscular and extramuscular transmission (Huijing & Baan 2001; Huijing 2003). During experiments this is apparent as follows: After the agonistic muscle is lengthened at its distal tendon while its synergistic muscle is kept at constant length (Plate 3.2.1B), distal force of the isometric synergistic muscle is decreased (compared to the unconnected case) with increasing lengths of its adjacent muscle. The lengthened muscle creates, or enhances, a distally directed myofascial load on the isometric synergistic muscle. At its proximal tendon, this load is integrated into force exerted by the muscle (as in Plate 3.2.1A). In contrast, distally exerted force is decreased because of such loading conditions. Myofascial force transmission between antagonistic muscles is (by definition) only possible via extramuscular mechanisms, as such muscles are separated by compartment walls. Stiff connections are made between compartments by neurovascular tracts, but also other extramuscular fascial structures are expected to play a role. The effects and explanation of myofascial interaction between two muscle groups located at opposite sides of an intermuscular septum or interosseal membrane (Plate 3.2.1B) are similar to those described for synergistic muscles (Huijing 2007; Huijing et al. 2007; Meijer et al. 2007, Rijkelijkhuizen et al. 2007). In a series of experiments in rats, we have shown that such mechanisms and effects are active between all muscles of the lower leg (for an overview of results, see Rijkelijkhuizen et al. 2009). So, even antagonistic muscles located at opposite sides of the leg interact (e.g., m. tibialis anterior and triceps surae muscles, see Ch. 5.8 for similar physiological results in mice), and cannot be considered as fully independent entities. It should be realized that this means that part of the force exerted by active sarcomeres within a muscle may be
CHAPTER 3.2
exerted at the tendon of its antagonistic muscle. In fact, the proximal sarcomeres of myofibers are in series not only with more distal sarcomeres of the same myofiber, but via myofascial loading also with distal sarcomeres (and their adjacent endomysia) in the lengthened antagonistic muscle(s). It is evident that the classical concept of antagonistic muscles (as having opposite mechanical effects) and the nomenclature used to describe them is due for a fundamental update. . . that, however, is beyond the scope of the present chapter.
Muscular relative position also affects muscular force exertion Experiments (Huijing 2002; Maas et al. 2004), as well as finite element modeling (Maas et al. 2003a,b; Yucesoy et al. 2006), indicate that a muscle kept at constant length and moved through its natural fascial context exerts tendon forces in proximal or distal direction that will vary according to the myofascial loading conditions that are altered with changes in relative position (Fig. 3.2.2). Relative movement between synergistic muscles occurs due to differences in moment arms at joints crossed, and for bi- or polyarticular muscles due to movement in a joint not crossed by its adjacent monoarticular synergistic muscle. Relative movement of antagonistic muscles is the order of the day, since movement of a joint will have opposite effects on Muscle
Muscle
Fprox < Fdist
Fprox = Fdist
Extramuscular structure Muscle
Fprox > Fdist
Fig. 3.2.2 • Schematic example of effects of relative position on myofascial connections and loading. As the muscle of constant length is moved its relative position is changed with respect to other structures (e.g., other muscles or extramuscular structures). The effects for myofascial connections and the direction of loading on the muscle are indicated with the consequences for muscle force exerted at proximal (left) and distal (right) tendons.
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muscular length: e.g., joint flexion will lengthen its extensor muscles and shorten its flexor muscles.
Complexity of myofascial loading of muscle Above, we have provided the simplest examples of myofascial loading to clarify its principles. In reality, within the integrated myofascial system loading of muscles will be very complex. Multiple and opposite loads on a muscle are considered common (for example, a proximally directed load by the neurovascular tract and a distally directed load by compartmental fascia). The latter is particularly evident for shorter muscles, but also present at higher lengths. If one cuts a tendon (Chapter 5.4), its passive muscle retracts somewhat. If such tenotomized muscle is activated, it will shorten only a little more, indicating a distal myofascial load keeping the muscle at length. By changing the length and position of muscles, the direction of net loading may change because of (1) rotating a fascial component with respect to muscle or (2) making the mechanical effects of another fascial structure dominant. If simultaneously exerted proximal and distal myofascial loads on a muscle are equal, the proximo-distal force difference will be zero. Therefore, the presence of such a difference constitutes absolute proof of epimuscular myofascial force transmission, but its absence does not necessarily mean that such force transmission is missing! Since myofascial loading of a muscle under consideration may originate from all muscles with the body segment, it is clear that a lot needs to be known before the conditions determining the target muscle’s force are specified in detail. In addition, myofascial force transmission between muscles in adjacent segments is likely, because of the stiffness of the neurovascular tract coursing through the tissues of the body segments. There are some indications that inter-segmental myofascial transmission occurs (Vleeming et al. 1995; Huijing et al. 2009), but this needs further confirmation, particularly for living and active muscles (Huijing 2009). Experiments and modeling performed so far have had proving the feasibility of epimuscular myofascial force transmission and its basic effects and principles as their goal. Therefore, it is clear that we have only scratched at the surface of this intricate and complex system and a lot more scientific and clinical work is needed to reveal the principles of its complexity. 120
Additional factors to consider Experimental work discussed above has many limitations that need to be considered in a more generalized view. It is good to realize that the control needed for solid experimental proof precludes getting close to in-vivo conditions. At the same time, if one experiments in vivo in human or animal studies, it is often impossible to attain sufficient control of the conditions.
Joint movement Joint movement (not included in experiments described above) affects actual stiffness of fascial components; e.g., the length and, particularly, tension within neurovascular tracts are very dependent on joint positions (Huijing 2009). Therefore, a recent study (Maas & Sandercock 2008) extending experiments (to cats) and including actual joint movement constitutes a real contribution to the field. Evidence of epimuscular myofascial force transmission between synergistic muscles of the calf was reported only if soleus muscle was at a length deviating from that imposed by the specific ankle angle. Maas and Sandercock (2008) concluded that epimuscular myofascial force transmission does not occur in physiological conditions in vivo, but may play a role when conditions deviate from normal. There is no doubt of the validity of their finding. However, in its generality, their conclusion about myofascial force transmission occurring exclusively in non-physiological conditions is premature, as evident also from emerging magnetic resonance imaging work in humans (Yaman et al. 2009; Huijing et al. 2011) with similar experiments: changing the knee angle caused local changes of strain, not only in gastrocnemius muscle, but also in synergistic soleus muscle kept at constant length due to a fixed ankle angle. The same was found for the full remainder of antagonistic muscles of the lower leg that also do not cross the knee. Previously, some other studies indicated evidence of in-vivo epimuscular myofascial force transmission (Yu et al. 2007). One could argue, as was done by Herbert and co-authors (2008), that if only a small percentage of muscle force is transmitted myofascially, we could afford to neglect the whole process. However, having epimuscular myofascial force transmission as a fundamental mechanism of intact tissues completely changes the view of functioning of those
Myofascial force transmission
tissues, even if the size of the related phenomena may be small in specific conditions.
Levels of muscular activation One important aspect of the work discussed is that even though different levels of activation have been studied by varying firing rates of muscles (Meijer et al. 2006; 2008), such changes were always imposed uniformly on all muscle studied. In vivo, different muscles or muscle groups are active at varying levels of activation. By stimulating different nerves or their branches (Maas & Huijing 2009) this may be mimicked. Those results do not affect the principles as described above in a major way.
Effects on functioning of the sensory apparatus As our view of in-series and parallel arrangements of structures is renewed, it is clear that our views on neural sensors need to be adapted as well: many more
CHAPTER 3.2
receptors outside of muscle (e.g., in periosteum, intermuscular septa, compartment) will receive information about muscular conditions. Also intramuscularly, conditions for receptors may be different than thought previously. Classically, muscle spindles are considered as arranged in parallel to myofibers, and Golgi tendon organs as arranged in series with them. However, if a part of the stroma that contains muscle spindles is in series with sarcomeres, this receptor will also operate in series. Preliminary results indicate that this may be the case (Arıkan et al. 2009). In any case, in accordance with results on epimuscular myofascial force transmission, receptors in muscle kept at constant muscle-tendon complex length increase their firing rates, as other muscles within the same segment are lengthened. The most important basic principles of epimuscular myofascial force transmission have been discussed. On the basis of that, the conclusion is warranted that if we do not take such force transmission into account we will never fully understand muscular function. Similarly, it is likely that at least acute effects of manual therapy (Chapter 8.5) will involve some of these mechanisms.
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