Epimuscular myofascial force transmission: A historical review and implications for new research. International society of biomechanics Muybridge award lecture, Taipei, 2007

ARTICLE IN PRESS Journal of Biomechanics 42 (2009) 9–21

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Review

Epimuscular myofascial force transmission: A historical review and implications for new research. International society of biomechanics Muybridge award lecture, Taipei, 2007 Peter A. Huijing a,b, a b

Research Instituut Move, Faculteit Bewegingswetenschappen, Vrije Universiteit, van de Boechorststraat 9, 1081 BTAmsterdam, The Netherlands Biomedisch Technologisch Instituut, Biomedische Werktuigbouwkunde, Universiteit Twente, Enschede, The Netherlands

a r t i c l e in fo

abstract

Article history: Accepted 22 September 2008

Elements of what we call myofascial force transmission today have been on peoples mind for a long time, usually implicitly, sometimes quite explicitly. A lot is there to be learned from the history of our knowledge on muscle and movement. There is little doubt about the presence and effectiveness of the mechanism and pathways of epimuscular myofascial force transmission. However, we should learn much more about the exact conditions at which such transmission is not only of fundamental biomechanical interest, but also quantitatively so important that it has to be considered for its effects in health and disease. Even if the quantitative effects in terms of force would prove small, one should realize that this mechanism will change the principles of muscular function drastically. A new vision on functional anatomy, as well as the application of imaging techniques and 3-D reconstruction of in vivo muscle, will aid that process of increased quantitative understanding, despite usual limitations regarding the mechanics in such experiments. I expect it is fair to say that without understanding myofascial force transmission we will never be able to understand muscular function completely. & 2008 Elsevier Ltd. All rights reserved.

Keywords: Muscle Myofascial force transmission Epimuscular Historical review Rat Human Epimysium Perimysium Endomysium Connective tissue Neurovascular tract Blood vessels Nerves Intermusclular Septa Fascia Periost

Contents 1.

2.

3. 4.

5.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 1.1. Epimuscular myofascial force transmission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 1.2. Purpose of the present work . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 Some historical aspects of myofascial force transmission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 2.1. Connections between nerve and blood vessel connective tissues and muscle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 2.2. Connections between adjacent myofibres and between myofibres and the connective tissue stroma . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 2.3. More specific references to intra- and epimuscular myofascial effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 A call for a revived and new anatomy and biomechanics of myofascial structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 3.1. Examples of relevant exceptions of anatomical work . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 Modern experimental evidence for epimuscular force transmission. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 4.1. Mechanical interaction between antagonistic muscles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 4.2. Single muscle lengthening and relative position change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 Effects of joint movement on muscular relative position and myofascial effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

 Corresponding author at: Research Instituut Move, Faculteit Bewegingswetenschappen, Vrije Universiteit, van de Boechorststraat 9, 1081 BTAmsterdam, The Netherlands. Tel.: +31 20 444 8476; fax: +31 20 444 8529. E-mail address: [email protected]

0021-9290/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbiomech.2008.09.027

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5.1. 5.2. 5.3. 5.4.

Effects of joint movement after tenotomy in human fore-arm muscles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 Effects of complex joint movement in the cat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 Some in vivo evidence for epimuscular myofascial force transmission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 Some attempts at 3-D reconstruction of myofascial structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 5.4.1. In vivo images of the rat lower leg . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 5.4.2. Visible human data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 Conflict of interest statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

1. Introduction

2. Some historical aspects of myofascial force transmission

This review will focus specifically on paths of force transmission arranged in parallel to the myotendinous path of force transmission to bone: i.e. myofascial force transmission. This transmission is called that because supramolecular chains of connections (for a review e.g. Berthier and Blaineau, 1997) between the myofibre cytoskeleton and the collagen reinforced extracellular matrix allow force transmission between cytoskeleton and endomysial–perimysial–epimysial muscular connective tissue stroma. Not widely considered regarding its consequences until molecular biology gave us more information regarding the nature of the connections, a few groups under the direct pressure of unexplained experimental and morphological results have been working on this phenomenon for a few decades (Eldred et al., 1993; Hijikata and Ishikawa, 1999; Hijikata et al., 1993; Loeb et al., 1987; Purslow and Trotter, 1994; Street, 1983; Street and Ramsey, 1965b; Trotter, 1990; Trotter and Purslow, 1992; Trotter et al., 1995). We categorize the type of transmission discussed in these papers as intramuscular myofascial force transmission (as it deals with force transmission within the confines of the continuous epimysium and epitenon enveloping muscle and its tendon(s)).

In relation to this subject, I have been particularly inspired by a number of quotes:

1.1. Epimuscular myofascial force transmission Epimuscular myofascial force transmission is defined as the force transmission between muscle and its surroundings, passing via the outer limits of muscle–tendon complexes (epimysium). My personal first encounters with such ideas (Huijing, 1999) showed that intramuscular myofascial force transmission occurred in rat extensor digitorum longus (EDL) muscle after progressive distal tenotomy (Huijing et al., 1998) and that partial blunt dissection of the perimysium separating the different heads of EDL removed most, but not all, of the effect. We were struck by the structural similarity of intra and intermuscular connective tissues and the ease by which they could be broken by blunt dissection. Because of that we speculated that similar force transmission would be possible between muscle and its surrounding muscular and non-muscular tissues! After this particular publication my research group set out to explore that almost unbelievable possibility and to test it experimentally. 1.2. Purpose of the present work The purposes of this article are threefold: (1) to test, by historical literature study, if ideas related to myofascial force transmission are not quite as modern as one might think. Some ideas that are a least related to force transmission are reviewed, and so or some historical examples dealing with it specifically, (2) to consider consequences for further research and (3) to, review, briefly, the most salient features of epimuscular myofascial force transmission. Due to the limitation of space, a more detailed representation of this part of the Muybridge lecture will be published elsewhere (Huijing, 2009).

Beautiful are things that one sees, More beautiful are the things that one knows, By far the most beautiful are the things that one ignores. Stensent (1673)

If you know something, then say ‘I know’. If you don’t know, then say ‘I don’t know’. Then you really know Confucius 551–479 B.C.

Niels Stensen is an important scientist in myology, as he was among the first to consider muscle in terms of a model, incorporating the phenomenon of constant muscle volume, and to consider myofibres as independent sources and agents of movement. At the XXI ISB congress in Taipei, Savio Woo appropriately presented a quote of Confucius in Chinese, indicating that true knowledge involves awareness of what one does and does not know. Evidently, knowledge of this kind is ancient wisdom. The translation shown above was provided by my colleague and surgeon Dr. Hu, who is a citizen of China and presently a researcher in our faculty. John Gerould is an historian of the sciences, who published on the ideas of, what we today call, connective tissue. He expressed the following: How often it happens that a great discovery, before it finally flashes out upon the world, smoulders for a long time in men’s minds, dimly understood, its full significance unfelt!, John H. Gerould (1922). In retrospect, these quotes seem applicable to the development of the ideas concerning myofascial force transmission and more particularly epimuscular myofascial force transmission. Ideas, related to this concept, have been popping up throughout history of the medical–biological sciences. 2.1. Connections between nerve and blood vessel connective tissues and muscle As neurovascular tracts embedding and (collagen) reinforcing the blood and lymph vessels and peripheral nerves are important candidates for being a major path of force transmission, we should consider detailed description of these structures as a starting point. Ancient Greeks had access to such descriptions (because of the work of, e.g. Galenos (129–210)) (In Greek, with Latin and French translations available since the 16th century, e.g. Galenos, 1538, 1541; Galenos and Canappe, 1541). However, the Renaissance-induced changes, enhanced anatomical activities. A number of anatomists must have spent considerable time dissecting blood vessels and nerves of the human body. Images of these structures were made by Andreas Vesalius, who revolutionized anatomy, but in the 16th century

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also several others (e.g. Casserio 1632) depicted details of muscular anatomical geometry (not shown) in a way that is not often seen in atlases since. Fig. 1A illustrates fully dissected major elements of the human nervous system. It shows what at least I consider to be the modern tragedy of anatomy: to gain knowledge about specific structures, they have to be dissected from surrounding tissues, almost preventing also considering their

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morphology and function when integrated in a higher level of organization. William Croone (1633–1684) reported (Croone, 1664) on the spatial relationship between muscle and nerve (portrait and image in Fig. 1B.) because he was involved in the work on ebullionist theories of muscle contraction, involving increase of muscle volume by a ‘‘spirituous liquor’’ from the nerves. He gave

Fig. 1. Historically important people for development of the concept of muscular myofascial connections I. (A) Anatomist Giulio Casserio (1561–1616) is shown as representing 16th and 17th century scientists who did painstaking dissection isolating almost the whole human system of major nerves and blood vessels. An example of the latter is shown in a posthumous publication (1632). Of course these structures needed to be studied in isolation, before the way was paved to consider them as integrated parts of neurovascular tracts. Casserio also published anatomical images representing more details of muscle architecture than usually shown. (B) Portrait of William Croone and his image of connections between blood vessels, nerve and muscle. The vesicles drawn within the muscle are related to his theories soft muscle contraction: muscles would expand by either the influx of spirits from the brain of effervescent effects of this substance when reacting with blood. Experiments had already been performed by Jan Swammerdam (but published only in 1738) showing that muscle volume does not increase on contraction and this fact used by Niels Stensen (1667) was either not known or ignored by major parts of the scientific community. (C) Image published REF by Alexander Stuart showing the connections between human antagonistic muscles (mm. biceps and triceps brachii) by blood vessels and nerves. (D) An image from the anatomical atlas of Bourgery (1831–1854); Bourgery et al. (1866–1871) showing dissected vessels (i.e. arteries, veins and lymph vessels) and their connection to muscle. The original image was published in full colour. (E) Portrait of Jean-Baptiste Lamarck influential biologist who had definite ideas about the role of connective tissues. (F) Image of Xavier Bichat (1771–1802) (actually his death mask), who in his short life played such an important role in developing ideas about the anatomy, physiology and pathology of fibrous (and other) connective tissues and fascia. (G) Portrait of German anatomist and anthropologist Johann Blumenbach who described (1798; cited from the latter reference; 1817a) the muscular connective tissues and its connection to the contractile substance.

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up that type of work after Niels Stensen (whom he met in person in Montpellier, France), published his book on muscle geometry (Stensen, 1667). However, Croone’s name is still prevalent in modern science, because part of his financial inheritance was used to start the tradition of Croonian Lectures (originally with the suffix ‘‘on muscular motion’’) (see also the title of Stuart, 1737). However, to the chagrin of many myologists, the keepers of the tradition (The Royal Society of London) have seen fit to deviate from the specific subject of myology since the 19th century. The Croonian lecturer of 1977 (lecturing on insect muscle) stated:‘‘ forty-seven out of 163 Croonian Lectures have been on muscleyy in the 229 years of its existence’’ (Pringle, 1978). In fact, since that time only two lectures (1979, 1986) have been myology related. The very first Croonian lecturer Alexander Stuart (1673–1742) published an image (1737 his Fig. 3; see Fig. 1C) of fully dissected connections by nerves and blood vessels of human antagonistic muscles. He was actually interested in the question if one muscle could be excited by injection of nervous spirit, as a consequence of activity of its antagonistic muscles. However, his figure illustrates how nerves and blood vessels can form mechanical connections between antagonistic muscles. If one realises that these structures that pass through intermuscular septa (SI) are embedded within fairly stiff collagen–fibre-reinforced segments of the extracellular matrix, potential pathways for force transmission are clear. In several decennia of the late 18th and early 19th centuries, a renewed interest arose in the tissues that later would be called connective tissues. Evidently, the 16th and 17th century interest did not last to the 18th century, because Xavier Bichat stated in 1799 (i.e. 1771–1802, portrait Fig. 1F): ‘‘Up to the present the membranes have not been a particular research object for the anatomists’’ and ‘‘ystruck by the difference in structure of the organs, the anatomists have forgotten that their membranes could have analogiesyyy’’. His work recognizing common features of connective tissue membranes proved to be important for pathology, recognizing resemblances between diseases of different organs. Lamarck (1744–1829, portrait Fig. 1E.) made further-going inferences (1809): ‘‘It has been recognized for a long time that the membranes that form the envelopes of the brain, of nerves, of vessels of all kinds, of glands, of viscera, of muscles and their fibers, and even the skin of the body, are in general, the productions of connective tissue. However, it does not appear that any one has seen in this multitude of harmonizing facts anything but the facts themselves; and no one as far as I know, has yet perceived that connective tissue is the general matrix of all organization, and that without this tissue no living body would be able to exist nor could have been formed’’ (translation by Gerould, 1922). Lamarck also entertained the concept of, in modern words, a continuous extracellular stroma of the whole body. Very special attention for connective tissue structures of the locomotor apparatus is evident in the beautiful anatomical work (1831–1854 e.g. Fig. 1D) by anatomist Marc Jean Bourgery (1797–1849) and artist Nicolas-Henri Jacob (1782–1871) (see Figs. 1D and 3) showing spatial relationships between (partially dissected) neurovascular tracts, and muscular or other tissues. Disappeared from most modern anatomy books are also the sometimes detailed descriptions of the ‘‘rapport’’ between adjacent muscles found particularly in most French anatomy textbooks of the 19th century. It is not clear to me if such description intended to indicate just morphological aspects of location, or actual functional implications related to potential intermuscular interaction.

2.2. Connections between adjacent myofibres and between myofibres and the connective tissue stroma Jacob Benignius Winsløw (1669–1760), a Danish born anatomist (in fact a second cousin of Niels Stensen), travelled in the course of his studies to Paris, via Holland (studying anatomy in Amsterdam, Haarlem and Leiden). In Paris he remained, using the Gallicised name Jacques Benigne Winslow (Fig. 2A), and became a very important person in myology and medicine. In addition to building an anatomical theatre for the Medical faculty of the University of Paris and serving as dean of that faculty, he worked as a professor of anatomy and surgery at the anatomical theatre of the Royal Gardens (Jardin royal), where King Louis supported surgeons heavily, in contrast to his lack of support of the Paris medical faculty. In addition to many articles, Winslow wrote an important anatomical textbook devoted to a large extent to the anatomy of human muscles and bones. One can find the following citation in this book: (Winslow, 1732) (cited from Winslow et al., 1763, p. 160). ‘‘To understand the uses and contrivance of each muscle in particular, we must consider its situation, direction, lateral connexion, relation and composition of its parts: we ought likewise to examine, how the neighbouring muscles are disposed for producing simple motions, and how those that are at a greater distance, can produce combined or compound motions.’’ So-called lateral connections are considered explicitly in this section of general myology. Therefore, Winslow must have had ideas of presence and potential functional importance of such connections; however, this concept plays a limited role in the specific anatomical descriptions that he provided in the remainder of his book for muscles and their mechanical effects. Johann Friedrich Blumenbach (1752–1840, portrait Fig. 1G) referred to the intimate connections between myofibres and their connective tissues (Blumenbach, 1798) (cited from the later reference: Blumenbach and Elliotson, 1817): ‘‘Every muscle possesses a covering of connective tissue membrane, which is so interwoven with its substance, as to surround the bands, the bundles, and even each particular fibril [i.e. myofibre].’’ Considering short myofibres, in the 19th century (e.g. Amici and Lambl, 1859; Engelmann, 1873; Krause, 1869) and 20th century (e.g. Boga, 1937; Baldwin, 1913; Ciaccio, 1938; Heidenhain, 1911; Ponomarewa, 1911; Street, 1983; Street and Ramsey, 1965a; Tiegs, 1955), researchers were fascinated by histological evidence for the festooning sarcolemma (i.e. combined structures of cell membrane, basal lamina and endomysium). Such results indicate that stiff extracellular connections exist at the Z-lines, and connections are absent or more compliant at the M-lines of the sarcomere. An important anatomist and microscopist of muscle in the second half of 19th century is William Bowman (Fig. 2C). He also showed images of festooning sarcolemma in shortened muscle fibres, without paying very explicit attention to it (1840), but actually described (Fig. 2C) strong unions between sarcomeres within adjacent myofibres (Bowman, 1847). Connections of myofibres to surrounding endomysium and epimysium were imaged (Fig. 2E) in dried muscle preparations by Heinz Feneis and these images were published in 1935 in the Morpologisches Jahrbuch (cited from Ha¨ggqvist, 1956).

2.3. More specific references to intra- and epimuscular myofascial effects Physiologists Hugo Kronecker (1839–1914, portrait and signature Fig. 2B.) and John Cash (1854–1936) published experimental results on epimususcular myofascial force transmission (Kronecker and Cash, 1880). Since only a short German language abstract of

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Fig. 2. Historically important people for development of the concept of muscular myofascial connections II. (A) Jacob Benigne Winslow, anatomist in France referred to the functional importance of connections to muscle in his book (1798; cited from the latter reference; 1817a). (B) Hugo Kronecker (physiologist) performed specific experiments on the mechanical interaction between muscle and its surroundings and the effect of dissection. (C) William Bowman (anatomist, microscopist, as well as clinician) studied the minute details of myofibres (Bowman, 1840) and published images that can be interpreted as tight connections between sarcomeres of adjacent myofibres. The figure (Fig. 289 of Bowman, 1847) shows four adjacent myofibres with remnant sarcomeres of a fifth one tightly adhering. (D) Derek Denny-Brown performed physiological experiments on SOL and noticed that the time course of its force build up during tetanic stimulation is considerably faster (curve a) if some remaining myofascial connections to gastrocnemius muscle are not removed. As a consequence following dissection force is lower and the time course of a slow muscle becomes visible (curve b). (E) Heinz Feneis (cited from Ha¨ggqvist, 1956) prepared a freeze dried preparation of muscle showing the myofibre (perimeter shown by white line) shrunken away from the endomysial tube (perimeter dark line) and revealed the connections between the two.

this work is accessible, it is sometimes hard to interpret exactly the experiment performed. By electrical stimulation they allowed muscles to shorten under various myotendinous loads, while studying mechanical interaction between muscles active within their natural connective tissue context before and after dissection: ‘‘Since usually complete isolation is deemed necessary for muscles to be tested for the magnitude of shortening, it seemed important to determine if, and to what extent, the muscles functioning within their natural context are limited in their movement.’’ They found interesting results: (1) ‘‘A passive muscle is shortened by its neighbouring maximally shortening muscles’’. (2) The shortening in the course of rhythmic dynamic contractions of dissected muscle (load up to 30 g) is enhanced compared to that of non-dissected muscles under identical conditions. This be-

comes very notable at a stimulation frequency of 2 Hz and often clearly remains at a stimulation interval of 5 s. However, they also reported the following: (3) ‘‘On intermediate shortening of the neighbouring muscles, passive muscle is not moved at all’’ and concluded that ‘‘for the range of movement that can be induced by voluntary or reflex activation, muscles are not hindered in any movement by their natural surroundings, and are at the same time protected from damaging effects, which changes the function and configuration of isolated muscle’’. Since no more work by them on this subject seems available, it is likely they dismissed myofascial force transmission as unimportant. Doing so, they probably underestimated the potential importance of low firing frequencies and myotendinous low loads for the in vivo movement.

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Derek E. Denny-Brown (1901–1981), a New Zealand born neurologist (Fig. 2D), worked on the time trajectory of tetanic contractions of mouse soleus and gastrocnemius muscles in relation to their myofibre composition (Denny Brown, 1929). On p. 380 he states: ‘‘In response to a break shock to the popliteal nervey, it is found to be extremely difficult to avoid a, slight early rise of tension, and fall in the plateau [tetanic force of the soleus] due to vibration or pull of gastrocnemius. This transmission of this effect occurs though the tendons be freely separated. A small strip of fascia is attached to the medial border of soleus is the cause of most transmission between the two [mm. gastrocnemius and soleus], and once this strip is removed the twitch of soleus follows the slow curve, which is obtained [also] by stimulation of the small nerve to soleus alone.’’ It is clear that Denny-Brown was fully aware of myofascial connections between these muscles and actually used their effects experimentally in studying how slow and fast muscle work together. Then he cut the connection and looked again at the time trajectories of these fast and slow muscles (Fig. 2D). This historical presentation cannot do without one entry from more modern history: Sibyl F. Street working in collaboration with Robert Ramsey (Street, 1983; Street and Ramsey, 1965b) on myofascial force transmission in active and passive single myofibres and small fascicles. Their very interesting and thought provoking work has been reviewed previously (Huijing, 1999a; Monti et al., 1999).

3. A call for a revived and new anatomy and biomechanics of myofascial structures Above, we indicated a limitation of anatomy related to dissection. Such types of limitations are not unique to this discipline, but additional and specific factors seem to have added to decreased perceived importance of the discipline: (1) satisfaction with describing just morphology, often, accompanied by disregarding functional constraints and advantages imposed by a specific morphology, (2) some anatomists have radiated a sense that the, non-microscopic, anatomical description was fully finished: for the locomotor system, i.e. anatomy could yield no new knowledge, as the description was complete. An example in case was a nestor of Dutch anatomy, Prof. Woerdeman, also author of an important anatomical atlas, who already around 1963 made statements to that effect (personal communication by Prof. R.H. Rozendal). (3) Many anatomists have also taken up valuable, but totally different aspects of research, not concerning the essence of anatomy. Some notable exceptions will be discussed below. As a consequence, in many places in the Western world, anatomy has lost its prime position in biomedical research and education, with concomitant budget cut-backs reorganisation and disappearance of departments. On the basis of the above historical anatomical considerations, it is clear we are in desperate need of better morphological descriptions of the continuous collagen reinforced extracellular matrix stroma than provided in anatomy textbooks and atlases, and even journal articles. This not only has consequences for future research, but also for teaching of the subject. We should revive and make common knowledge (again) and enlarge the type of work for which an example is shown in Fig. 3 by Bourgery (1831–1854) and Bourgery et al. (1866–1871), particularly volumes 2–4). It shows the relation of major neurovascular tracts to muscular compartments and their contents. Such work can be further renewed by making use of modern image techniques such as 3-D reconstruction of images of sliced preparations, and in vivo MRI data. If the resolution of in vivo ultrasound imaging can be shown to be high enough for this type of work, it could also play a

Fig. 3. Cross-sectional anatomy of the human lower leg in 3-D. The original of this image was published in full colour in the editions of Bourgery’s atlas. It shows the tibia (Ti) and fibula (Fi) and intermuscular membrane, as well as SI defining the borders of compartments for muscle groups. Epimysia are also drawn (exaggerated thickness) to show the borders of individual muscles. Embedded in or closely related to the septa are major neurovascular tracts. TA represents m. tibialis anterior (TA); EDL, m. EDL; Per, peroneal muscle group; DF, deep flexor muscle group; Sol, m. soleus and GM and GL medial and lateral heads of m. gastrocnemius, respectively.

role in these developments, as long as its users improve their knowledge of anatomical details to much higher level.

3.1. Examples of relevant exceptions of anatomical work In embalmed human cadavers, Vleeming et al. (1995) loaded the thoracolumbar fascia and showed that hip, pelvic, and leg muscles interact with arm and spinal muscles via this fascia. Despite the limitation of enhanced stiffness due to fixation this is a first indication of potential intersegmental force transmission in humans. Pioneering anatomical work showing the continuity of myotendinous connections and the compartmental, as well as jointrelated connective tissue stroma in humans and rats, was performed by a group led by Drukker and more particularly by van Mameren. However, this work has led to only a limited number of Journal publications (Donkelaar et al., 1996; Mameren and Drukker, 1979; Verhaar et al., 1993) of, unfortunately, not major impact (judging from the citation scores). This work started with description of the human elbow region and culminated in a doctoral dissertation by van der Wal (1988) involving an early 3-D reconstruction study of connective tissue structures within the rat lower forelimb. It focussed on myotendinous pathways of force transmission. A very important conclusion of this work is that the connective tissues of the joint should not be considered as a separate entity from the muscular connective tissue! Our lab had only a limited opportunity to make a start with work on 3-D reconstruction focussed specifically on potential structures of the myofascial pathways. Some of this work will be presented below, in the hope to entice more people in this direction. Ideally, if not incorporated within the imaging methods, imaging work should be accompanied by biomechanical measurements of tissue and network stiffness to provide data that will

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allow more biomechanical modelling work on the subject. In addition, the statements made on imaging techniques by Kai-Nan An from Mayo Clinic at Rochester Minnesota at the opening lectures of the 2007 ISB congress in Taipei indicate the very exciting possibilities for what has been called ‘‘imaging biomechanics’’ (see also Bensamoun et al., 2006, 2007; see also Chen et al., 2007; Jenkyn et al., 2003; Ringleb et al., 2005, 2007) involving magnetic resonance elastography.

4. Modern experimental evidence for epimuscular force transmission Unequivocal proof of such transmission is the presence of proximo-distal force differences. (Such differences were reported for the first time at the turn of the century: Huijing, 1999b; Huijing and Baan, 2001; Maas et al., 2001.) Net force transmitted onto or from the muscle is integrated into force exerted at either the origin or insertion of the muscle. Myofibres or intramuscular connective tissues located between the point of application of this force and either origin or insertion have to bear this load. Such measurements are only feasible for muscles with fairly simple architecture, such as rodent EDL (for references, see Table 1) or some insect flight muscle (Meijer and Huijing, 2007b). Another way of proving myofascial transmission from muscle is showing force exertion onto bone by muscle(s) that has (have) no myotendinous connections to that bone. Target bone(s) have (has) to be isolated mechanically from the skeleton to do this. It is clear that this is not a straight-forward experiment (Fig. 4, for details, see Huijing and Baan, 2008). The collagen reinforced vascular tract containing blood and lymph vessels for the tibial segment and foot is still connected to the body (in Fig. 4B, for experiments this vascular tract was protected by leaving mm. adductor brevis and caudofemoralis over which it runs). Fig. 5 shows changes in passive tibia-femur complex force as a function of EDL length and relative position changes. The graph

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has been drawn to emphasize effects of muscular relative position. Note that after passive EDL proximal lengthening, isometric force exerted on the tibia decreases progressively to attain values close to zero only at high EDL lengths (i.e. at high negative Dlm+t values, oblique arrow). This indicates prestrained myofascial connections between EDL and the tibia at most lengths. EDL force exerted simultaneously increased as a function of length. For distal EDL lengthening (right side of the graph) both EDL passive force and proximal tibia–femur complex force increase as a function of EDL length. Neither force gets very close to zero at low EDL lengths. These types of experiments are not feasible for many muscles. So, more indirect effects are taken as indication of mechanical interaction between muscles: several muscles are kept at constant muscle–tendon complex length and the length of one muscle or muscle group is changed. If no epimuscular force transmission occurs, force exerted by such a constant length muscle should not be affected by the length changes imposed on other muscle (group). Changes in force, therefore, indicate myofascial force transmission (Fig. 6 shows an example of changes in anterior tibial muscles (TA+EHL) as function of EDL length change, see also Table 1). Also note that proximal EDL lengthening causes an, albeit smaller, increase of distal TA+EHL active force. Even in heavily dissected triceps surae, transmission occurred between the constituting muscles of this group (Rijkelijkhuizen et al., 2005). Progressive dissection showed epimuscular myofascial force transmission from plantaris muscle via epitendinous tissues to the calcaneal bone, indicating that not all myofascially transmitted force is ‘‘lost’’ for the exertion of joint moments. Transmission was also shown between muscle and non-muscular connective tissues (Huijing, 2002; Huijing and Jaspers, 2005). 4.1. Mechanical interaction between antagonistic muscles Synergistic epimuscular force transmission has been the subject of investigation for almost a decennium (see references

Table 1 Effects of distal muscle lengthening on force exerted by other muscle (groups) in rat and mouse experiments. Single muscle or single-muscle group lengthened distally

Dlm+t (mm)

Maximal decrease in distal active force at constant length (% of initial force) AC

TA+EHL

EDL

PER

DF

TS

Rat Anterior crural group (AC) TA+EHL EDL Peroneal group (PER) Deep flexor group (DF) Triceps surae group (TS)

11 11–14 9–12 8–10 10 NA

– – – NA NA NA

– – 6–13%a,e,h,i 25–33%d,b,f 58%f NA

– 5–10%a,c,d,e,f 30%g – 5–6%b,d 8%f NA

26%a,b 28–32%b,d,e,f 4–6%a,d,e,b – 52%f NA

NA 45%f NA 44%j,f – NA

11%b 16%e NA NA NA –

Mouse Anterior crural group (AC) TA+EHL EDL Triceps surae group (TS)

NA 5 5 6

– – – NA

– – 11%l 82%k

– 58%k – 27%k,m

NA NA NA NA

NA NA NA NA

NA 43%k NA –

–, Experiment not feasible; NA, data not available. a Meijer et al. (2007). b Meijer and Huijing (2007b). c Huijing and Baan (2003). d Huijing et al. (2007). e Rijkelijkhuizen et al. (2007). f Yucesoy et al. (2009). g Maas et al. (2001). h Huijing and Baan (2008). i Meijer et al. (2006). j Huijing (2007). k Huijing et al. (Unpublished observations). l Meijer and Huijing (2007a). m Meijer and Huijing (2007c).

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Fig. 4. Experimental set-up for measuring muscular force exerted on the tibia–femur complex. (A) The experimental rig in which the whole foot—lower leg–knee complex is mounted. This complex is isolated from the body, except for the tract containing its blood supply (b.s. tract in B) and some muscles (mm. adductor brevis and caudofemoralis not shown in B) to help protect the tract contents mechanically. A screw is screwed through the femur and knee joint into the tibia and fastened. The head of this screw was subsequently attached to the rig. The whole rig with the leg in turn is attached to the force transducer (FT). Forces exerted myotendinously by muscles fully within this system are not registered by FT, as both origin and insertion are within this system. The force of any muscle that has attachments to the world outside of the rig system will be measured, if myotendinous or myofascial connections to the tibia–femur complex are present. (B) The intact foot, lower leg and knee segments used in the experiment. Note that the only further dissection to be performed (partially shown) on this is the freeing of, mostly distal, target tendons for connection to the additional FTs. In addition to the attachment of the tibia–femur complex described above, the foot is tied to a footplate in fully plantar-flexed position to allow free passage of dissected distal tendons. Also the proximal EDL tendon is dissected with a piece of bone and attached to a FT external to the rig system. TA represents m. TA; EDL, m. EDL; PER, peroneal muscle group, and GL, the lateral head of m. gastrocnemius, respectively. The sciatic nerve, transsected and fully dissected from proximal locations within the femoral compartment, is deflected (n.). Its sural, tibial and articular branches were cut. Via an electrode, the nerve was stimulated supramaximally, so that the whole deep peroneal segment is fully active. The smallest division on the scale placed on the leg represents 1 mm.

at Table 1). Over the last few years evidence has been accumulating slowly that myofascial mechanical interaction is feasible also between antagonistic muscles, i.e. force is transmitted across compartmental barriers (Huijing, 2007; Huijing et al., 2007; Meijer et al., 2007; Rijkelijkhuizen et al., 2007 Symposium: Special journal issue) (Huijing and Baan, 2008; Meijer and Huijing, 2007a). It has been concluded (1) that force is transmitted between all muscles of the rat lower limb in potentially substantial quantities, (2) that force is transmitted between muscles and extramuscular connective tissues in that segment and (3) that such transmission occurs even for antagonistic muscle groups that are located at opposite sides of the leg, e.g. between anterior crural and triceps surae muscles, or peroneal and deep flexor muscles (Table 1). This reinforces the concept of connective tissue of a body segment as a potential unit functional element.

Fig. 5. EDL passive forces and the tibia–femur complex forces. For EDL passive forces that are exerted at the proximal tendon are plotted. Also tibia–femur forces are exerted at the proximal tibia end. The left-hand panel shows effects of proximal lengthening of EDL with high length occurring on the left. Similarly the right panel shows effects of distal EDL lengthening with high length on the right. EDL lengths are expressed as deviation from its value at reference position (D‘m+t), corresponding to a knee angle of approximately 1051 and an ankle angle of 901. The surprising and initially counter-intuitive parts of these results are on the left-hand side of the graph: As EDL was lengthened proximally (D‘ EDL-prox), tibial force decreased from relatively high values at low lengths to values approaching zero (oblique black arrow) at high lengths. In contrast, EDL proximal force increased with increasing length. The direction of lengthening is indicated by grey arrows along all curves. For distal lengthening of EDL (D‘ EDL-dist), both tibial and EDL force increase from low, but clearly nonzero values, to higher values at high length. The break in tibia–femur forces (at D‘m+t ¼ 0) indicates historydependent effects due to the distal lengthening which was performed first.

Fig. 6. Changes of force exerted by rat muscles kept at constant length. Active force exerted at the tied distal tendons of m. TA and m. extensor hallucis longus (EHL), which complex is referred to as TA+EHL. The muscle–tendon complex length of this group of muscles is kept constant, as m. extensor digitorum longus (EDL) is lengthened to equal lengths by moving its distal or proximal FT. Note that for distal EDL lengthening, TA+EHL active isometric force falls substantially from its initial set value (mean of 2.9 N). Table 2 gives an overview of percentage force decreases of many muscles in several experiments in rat and mouse. In contrast after proximal EDL lengthening, TA+EHL distal active force rises indicating a reversal of direction of net myofascially transmitted force.

4.2. Single muscle lengthening and relative position change Initially, experiments studying myofascial effects of lengthening and position change have focussed on moving one muscle only

(for references see Table 1). Such experiments played an important role in showing the principles and potentially sizable effects of epimususcular force transmission. However, such

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experiments have clear limitations. In vivo, single muscle length change is limited to pathological conditions, for example, in spasticity (a spastic muscle is a single muscle that tends to be kept short by its morbid neural control), or during a cramp. Smaller differential length changes of muscles are more common, because of variation in moment arms for different muscles. Sometimes such effects are notable; e.g. for mice, mean moment arm at the ankle of TA muscle is 17% higher than that of EDL (Lieber, 1997).

5. Effects of joint movement on muscular relative position and myofascial effects 5.1. Effects of joint movement after tenotomy in human fore-arm muscles The most simple and clear example of epimuscular myofascial effects was shown, several years ago, in patients suffering from spastic paresis of arm muscle, during operations involving flexor carpi ulnaris (FCU) muscle–tendon transposition. These results have been reported (Kreulen et al., 2003) and reviewed (Huijing, 2003; Smeulders and Kreulen, 2007). After performing distal FCU tenotomies leading to a little retraction of that muscle, but prior to transposition the following experiments were performed: (1) The surgeon moved the patient’s hand passively from maximal flexion at the wrist to maximal extension. A surprising effect of that movement was that FCU was lengthened at it distal end, despite the fact that this muscle did not cross the wrist any more. In fact the lengthening was substantial (i.e. 89% of its value in the intact condition). In these circumstances, FCU can only be lengthened if an increasing distal epimuscular myofascial load is exerted on it,

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due to the joint movement, either via synergistic muscles or by non-muscular connective tissues crossing the wrist joint. (2) Ulnar nerve excitation caused tenotomized active FCU to shorten a little more than in the passive state, but not its active slack length. Again, a distally directed epimuscular load keeps the muscle at relatively high active lengths, allowing it to exert active force. (3) Partial dissection of FCU from surrounding tissues, just enough to allow a later smooth transposition to an extensor insertion location with respect to the wrist, removed most but not all of such effects. 5.2. Effects of complex joint movement in the cat After giving the Muybridge lecture, and almost at the final phase of the writing of this article, an elegant experiment, performed by Maas and Sandercock, came to our attention in abstract and conference presentation form (recently published Maas and Sandercock, 2008). Knee joint angles were manipulated during movements of the leg, at constant ankle (and hip) joint angles to impose changes of muscular relative positions of gastrocnemius and plantaris muscles with respect to soleus muscle (SOL). Synergistic, as well as antagonistic, muscles of SOL remained passive. SOL was partially excited each time after changing the position of the cat leg by a robot. The authors present their results as an effect of ‘isolated’ changes of knee angles (70–1401) and found no effect on ankle moment despite proximally imposed changes of length and relative position of passive gastrocnemius and plantaris muscles. However, in agreement with previous work, they reported after performing distal tenotomy on soleus that ankle moment during SOL activity was maintained at 45% of pre-tenotomy values,

Fig. 7. Epimuscular myofascial effects of dorsal flexing the ankle joint. The subject being inclined on his left side is asked to keep his muscles passive. His leg is brought into anteflexion at the hip and the knee is extended (A). The demonstrator supports the leg at the foot and simultaneously is alternating the ankle between dorsal and plantar flexion. (B) and (C) show enlargements of popliteal area with the ankle in plantar flexion and dorsal flexion, respectively. In dorsal flexion (C) the neurovascular tract is raised above the normal level of the skin (just below the demonstrator’s index finger). In addition, also the tendon of the m. semitendinosus is more heavily accentuated through the skin.

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indicating that the SOL at lower length is still contributing to ankle joint moment by epimuscular myofascial pathways. Maas and Sandercock concluded that: (1) in the first part of the experiment, the active SOL acts as an independent actuator (i.e. inferring no major epimuscular myofascial force transmission occurred in these conditions). This conclusion is one of the possibilities for the specifics of the experiment, in which case strong limitations of epimuscular myofascial force transmission between partially active SOL and passive synergistic muscles are present. However, alternative explanations are conceivable: changing the knee angle and leg position will have several potentially counteracting effects also on ankle moment. For an example of effects of proximal lengthening of EDL (one of the effects of knee angle changes) on force exerted by antagonistic peroneal muscles and on net force exerted on the tibia (see Figs. 5 and 6) and on anterior tibial muscles see Huijing and Baan (2008). This means that only net effects are seen, which could be zero, even though epimuscular force transmission is still present. There is some indirect evidence within their results that this may be the case, particularly if one takes potential force transmission between antagonistic muscle groups into account: a minimal effect on net ankle moment is reported for considerable ankle joint movement (from 501 to 1001) with, in this case, the SOL active exclusively. Similar findings have been reported previously (Sale et al., 1982). This has never been explained properly. A conceivable explanation for the very wide plateau of ankle moment is a distribution of fibre mean sarcomere lengths (different fibres within the muscle operating at different mean sarcomere lengths) and possibly also serial distribution of sarcomere lengths within SOL fibres. Enhanced distributions are expected on the basis of epimuscular myofascial force transmission. Other explanations may have to be considered as well. (2) After distal tenotomy, soleus force is exerted on the calcaneus via its synergistic muscles due to its altered distal relative position with respect to its synergistic muscles. Again, alternative explanations should be considered as well. The distal myofascial load exerted on soleus that is preventing it from shortening to its active slack length may originate from nonmuscular connective tissues or via such tissues even from antagonistic muscles. It is clear that resolving these issues requires more work.

(5.3% of their force on the thumb). As there are no intertendinous connections between flexor tendons of the thumb and the index finger, this may be the very first report of in vivo epimuscular myofascial force transmission. In contrast with these effects for voluntary activation, intramuscular stimulation of motor units within FPL did not produce significant forces in any finger. In another study, more indirect evidence that could possibly be explained by effects of epimuscular myofascial force transmission (Oda et al., 2007) was found: a twitch elicited within medial gastrocnemius muscle also elicited a decrease of fascicle length in SOL, suggesting a mechanical connection between these muscles and possibly also explaining similar contraction dynamics of fascicles within these two muscles during isometric, as well as concentric and eccentric, plantar flexion moments. Note that this is similar to the arguments presented in the historical discussion above for the data of Denny Brown (1929). 5.4. Some attempts at 3-D reconstruction of myofascial structures 5.4.1. In vivo images of the rat lower leg Using MRI techniques we acquired serial images of the lower leg of a rat under sedation (i.e. passive muscles, with the knee at 1101 and the ankle in max plantar flexion).

5.3. Some in vivo evidence for epimuscular myofascial force transmission Evidence for myofascial force transmission in vivo is hard to obtain, because usually we have to do, at best, with indirect measures. Fig. 7 shows a simple example of an in vivo anatomy demonstration. After instructing the subject to keep the muscles inactivated, the volunteer’s hip is anteflexed and the knee extended. As the ankle joint is moved passively from plantar to dorsal flexion, the neurovascular tract is accentuated in the popliteal area, as well as the tendon of the m. semitendinosus. Note that, this indicates passive force transmission between the segments of the lower and upper leg. Recently, some in vivo indications for epimuscular myofascial force transmission were reported in human subjects. The most direct evidence is the reports on mechanical interaction between the long flexor of the thumb (m. flexor pollicis longus, FPL) and fingers other than the thumb (Yu et al., 2007). Activity of FPL motor units on other fingers was assessed by time averaging of finger forces using the FPU motor unit activity as trigger. FPU motor units commonly loaded the index finger (42 out of 55 units), but less commonly the other fingers. On average, these motor units exerted significant loading forces on the index finger

Fig. 8. In vivo MRI images of the rat lower leg: 3-D reconstruction. A live rat, under sedation, was brought into the bore of a MRI machine and sequential longitudinal images (pixel size 0.1 mm  0.1 mm, Slice Thickness ¼ 0.5 mm) were recorded on a 7 T MRI scanner with a bore size of 120 mm, controlled by an MR Solutions console. A custom-built 60 mm, 7 turn Solenoid RF Coil with a diameter of 30 mm dedicated for rat hind leg imaging was used. Based on the voxel array constructed from the planar MR image sequence, a 3-D reconstruction was made after selection on the basis of contrast, accentuating the connective tissue structures, such as neurovascular tracts. (A) Schematic representation of the contours of bones and muscles. Abbreviations: Fe ¼ femur Ti ¼ tibia; Fi ¼ fibula; sia ¼ septum intermusculare anterior; BF ¼ m. Biceps femoris; GL m. gastrocnemius lateralis; Sol ¼ m. soleus; PER ¼ peroneal muscle group, Ant tib ¼ anterior tibial muscle group; DF deep flexor muscle group. (B) Medial view of the 3-D reconstruction. (C) Lateral view of the 3-D reconstruction. Comparing images C and D allows distinction of paths of neurovascular tracts medial and lateral to the bones. It is suggested that analysis of strain in such images may advance knowledge on in vivo occurrence of epimuscular myofascial force transmission.

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The planar MRI images were combined into a 3-D image array, using an image analysis program (Amira version 4.1.1, Mercury group computer systems, Me´rignac, France). This program, in the voltex mode, allows visualizing 3-D scalar fields. Each point in a data volume is assumed to emit and absorb light. The amount and color of emitted light and the amount of absorption are determined from the scalar data by comparison with a defined color map including overall (i.e. independent of the variable value) transparency values. Subsequently, the resulting projection from the ‘‘radiating’’ data volume is computed.We used that technique to enhance neurovascular tracts visible within 3-D lower leg image arrays and to decrease the tibia and fibula transparency to intermediate values to be able to recognize lateral and medial passing of the neurovascular tracts relative to the bony structures. Fig. 8 shows both a medial and lateral view of the 3-D image. Note that muscle material per se is not visible in these images but muscle contours can be recognized, certainly in the untreated image stacks. The very diverse branching of neurovascular tracts is seen clearly. The thicker parts of these tracts are in extramuscular locations and their paths through the compartments are visualized; the tracts branch extensively as they enter the muscles at several locations. If one pulls on these tracts during experiments on the rat one feels how stiff they are.

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5.4.2. Visible human data Three-dimensional reconstruction has been performed on images obtained from the Visible Human server (http://zatoka.icm.edu.pl/vh/VisibleHuman.html). Using contrast differences reconstructed images have been manipulated to exclude muscle and muscle fascicle material and keep as much of the connective tissues as possible. Using edge detection techniques enhanced solid aspects of the upper leg connective tissue stroma (Fig. 9). The body of this subject is richly endowed with subcutaneous fat. The medial and lateral aspects of the intermuscular septum are marked. All tissue located anterior to the septum is related to the quadriceps muscle and all tissue located posterior to the septum is related to hamstring and adductor muscles. If one realizes that the endomysial–epimysial stroma of each muscle (part) is continuous with the structures shown, and these structures are stiff enough to be of mechanical importance, perception of an integrating structure into which muscular elements are incorporated arises. We have argued before that it is likely that interaction of muscular elements with such a structure will affect both the properties of the muscle and connective tissue stroma (Huijing, 2003).

Conflict of interest statement None.

Acknowledgements

Fig. 9. The integrating stroma of the left upper leg of a human cadaver in 3-D reconstruction. We look down into the tube that is constituted by the general fascia of the leg (fascia lata, the approximate location of its upper rim is indicated by the dotted line). On the medial side the general fascia curves more inward than on the lateral side so that we look upon this fascia. Dark lines, showing through it, are cutaneous blood vessels passing through the fascia. The outline of the femur representing the periost of that bone is indicated as well. Many connections are seen between the general fascia and the periost of the femur they are formed by septa, epimysia and neurovascular tracts. Two have been marked specifically as the intermuscular septa (SI) separating the quadriceps compartment from the hamstrings and adductor compartments. Dorso-medially a part of the m. gluteus maximus is seen. It is clear that there is hardly any room for its myofibres to insert on the femur and, therefore, they insert predominantly on the fascia lata (see also Huijing, 1999a, b). It is obvious that a detailed morphological and biomechanical analysis is needed of the imaged structures.

The author whishes to acknowledge several people who have contributed not only to the ideas presented in this review, but also sometimes helped in producing some aspects of this article. The most important of those is Guus Baan who is the person who runs my lab and with whom I have been working for more than 30 years. Of all my collaborators, he takes the biggest share of credits for the Muybridge Award that has been awarded by the International Society of Biomechanics for my scientific oeuvre. He has worked hard to produce some of the figures of this article, particularly 3-D reconstruction. Can Yucesoy who let me use some of our unpublished data, and Huub Maas, Hanneke Meijer, Josina Rijkelijkhuizen and Richard Jaspers have contributed ideas during and after their Ph.D. thesis work at either the Vrije Universiteit (VU), or the Universiteit Twente. The same is true for Dr. Mick Kreulen (surgeon) and Dr. Mark Smeulders at the University of Amsterdam Medical Centre. The continued collaboration (Can Yucesoy and Filiz Ates at Bogazic- i University in Istanbul, Turkey) and renewed collaboration (Huub Maas at VU) are highly appreciated. My colleague Drs. Henk Schutte at the Faculteit Bewegingswetenschappen (VU) gave me anatomical advice and helped me create the movie of the in vivo demonstration in a human subject on which Fig. 7 is based. Andor Veltien (Departement of Radiologie, at Radboud University Medical Center, Nijmegen, The Netherlands) helped us to produce in vivo MRI images of the rat leg. References Amici, G.B., Lambl, 1859. Ueber die Muskelfaser. Virchows Archiv Fu¨r Pathologische Anatomie und Physiologie und fu¨r Klinische Medicin 16, 414–422. Baldwin, W.M., 1913. The relation of muscular fibrillae to tendon fibrillae in volontary striped muscles of vertebrates. Gegenbauers Morphologisches Jahrbuch 45, 249–266 (plate VII). Bensamoun, S.F., Ringleb, S.I., Littrell, L., Chen, Q., Brennan, M., Ehman, R.L., An, K.N., 2006. Determination of thigh muscle stiffness using magnetic resonance elastography. Journal of Magnetic Resonance Imaging 23, 242–247.

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