Hui Jing 1999

Journal of Biomechanics 32 (1999) 329—345
ISB Keynote Paper — 1997

Muscle as a collagen fiber reinforced composite: a review of force
transmission in muscle and whole limb
Peter A. Huijing *
Instituut voor Fundamentele and Klinische Bewegingswetenschappen, Faculteit Bewegingswetenschappen, Vrije Universiteit, Amsterdam, Netherlands
Integrated Biomedical Engineering for Restoration of Human Function, Biomedisch Technologisch Instituut, Universiteit Twente, Enschede, Netherlands
Received 17 November 1998; accepted 20 November 1998
Abstract
Even though no direct physiologic evidence proving that myo-tendinous junctions at the end of myofibers are sites of force
transmission is available, these locations are accepted to support this function, because its specialized morphology resembles that of
load-bearing membranes in structure and location: Its design is fit for force transmission of force exerted by myofibers to tendinous
fibrous material. Shearing of the interface between these structures is thought to be stronger than direct tensile transmission. On the
basis of morphological studies of ‘in-series fibered muscle’ and biomechanical modeling it has been argued previously that force could
also be transmitted laterally from the tapered ends of myofibers onto in series myofiber via the intramuscular connective tissue
component. Shearing of the interfaces between myofibers is hypothesized to be the mechanisms of transmission. The interfaces are
made up of basal membranes of both myofibers and their common endomysium. The issue of lateral force transmission from
myofibers has not been addressed for whole muscle, in which myofibers are attached at both ends to tendinous aponeuroses, nor is
any direct experimental evidence available about possible functional importance of this phenomenon in whole muscle.
The primary objective of this presentation is to review available literature on myo-tendinous and myo-fascial force transmission,
present evidence from experiments involving tenotomy, fasciatomy and aponeurotomy regarding its importance and consider
implications for our thinking about muscle(s) and movement. 1999 Elsevier Science Ltd. All rights reserved.
1. Introduction junction’s specialized morphology, regarding folding and

sub-sarcolemmal dense material, resembles that of load-
In vertebrates, in order for controlled bodily move- bearing membranes in structure. Also, its location at the
ment to be possible, force generated by the activation of end of myofibers is perceived as circumstantial evidence
contractile molecules inside muscle fibers has to be for its role in force transmission (Woo and Buckwalter,
exerted onto the bony skeleton of the body. A first step of 1987). This is reinforced by the view that force generated
this force transmission process is to allow force to cross within sarcomeres is transmitted more or less exclusively
the cellular membrane of the muscle cell. to sarcomeres in series and therefore must be delivered to
Even though no direct physiologic evidence is avail- the bony or tendinous attachments via the ends of
able proving myo-tendinous junctions are such sites of myofibers.
force transmission (Woo and Buckwalter, 1987), these However, in the literature some evidence can be found
locations are very widely accepted to support this func- that transmission of force may be more complex and that
tion. A main reason for this acceptance is because the other structures within muscle may also play a role in
force transmission from the intracellular milieu of the
muscle fiber to the extramuscular environment.
The purpose of the present article is to review litera-
* Corresponding author. Present address: Instituut voor Fundamen-
ture and experimental evidence regarding mechanisms
tele & Klinische Bewegingswetenschappen, Faculteit Bewegingsweten- of force transmission and discuss their possible implica-
schappen, Vrije Universiteit, Amsterdam, Netherlands. Tel.: 0031 20 tions and potential functional relevance to in vivo
4448476; fax: 0031 20 4448529; e-mail: p—a—j—b—m—huijing@fbw.vu.nl. movement.
0021-9290/99/$ — see front matter 1999 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 2 1 - 9 2 9 0 ( 9 8 ) 0 0 1 8 6 - 9
330 P.A. Huijing / Journal of Biomechanics 32 (1999) 329 —345
2. Fiber-reinforced composites 3. Elements of extracellular space
The term fiber-reinforced composite is derived 3.1. The extracellular matrix

from material science technology. A composite is a
material comprised of different components, one Modern textbooks of molecular cell biology are ex-
element of which are fibers reinforcing a matrix of other plicit in their descriptions of the extracellular environ-
material. Often these fibers consist of discontinuous ment, however an important role in force transmission is
elements of very strong material arranged with fiber axes not usually made explicit. They do state that the extracel-
in the direction of the applied load. In composites the lular space is largely filled by a network of macro-
fibers are usually coated with a material that binds well molecules constituting the extracellular matrix. It should
to fibers on one interface and has a preference for being be noted that the organized network not only assumes
attached to the amorphous medium at the other in- structural functions, but also may influence cell behavior
terface. The efficiency of stress transfer onto the fiber profoundly. The macromolecules are secreted locally and
determines the mechanical properties of the composite assemble in a network consisting primarily of fibrous
(Termonia, 1987). proteins embedded in a hydrated polysaccharide gel.
The shear modulus is the predominating factor Glycosaminoglycan chains are highly organized to form
for load transfer between the matrix and the fiber. the major constituent of this gel. These molecules bind to
Since the elastic modulus of the fiber is typically larger proteins to form proteoglycans. Collagen fibrils form the
than that of the matrix the axial displacements of the major protein of the extracellular matrix. However, it
components can be different (e.g. Termonia, 1987: should be recognized that in fact collagen fibrils are not
his Fig. 2) isolated structures but should be considered extracellular
Applying this type of approach to biological materials matrix superstructures that result from complex interac-
is not without difficulty due to the complexity of biolo- tion between collageneous and non-collagenous compo-
gical materials. For muscle the large length changes nents (e.g. Lethias et al., 1966). Therefore several classes
the material may undergo, constitutes an additional of collagen types are distinguished (for an in depth treat-
complicating factor. In one of their model approaches, ment see Mayne and Burgeson, 1995).
Purslow and Trotter (1994) considered muscular Non-fibril-forming collagens are also found (e.g. type
endomysium as the composite material in which short VI in the extracellular matrix, endomysium and
straight segments of collagen fibers without direct tensile perimysium). An interesting function of this molecule
connections to each other reinforce the amorphous ex- regarding force transmission is its presumed role in con-
tracellular matrix by shear interaction at their surface. necting cells with the extracellular matrix (Jöbsis et al.,
Obviously, in muscle there are other fibers at play (i.e. 1996). Mutations of type VI collagen are implicated in
muscle cells and fibrous material in the basal lamina). To a specific type of muscular disease: Bethlem’s myopathy
avoid confusion, in the present work the muscle fiber will (Jöbsis et al., 1996), a disease that is marked by generaliz-
be called myofiber to clearly distinguish it from collagen ed muscular weakness in addition to contractures of
molecules, fibrils or fibers within the muscular fascial multiple joints, factors that could be related to altered
apparatus and basal lamina. We will consider muscle as force transmission.
a composite consisting of an extracellular matrix with The organization and size of collagen fibrils and fibers
triple reinforcement by fibrous material. The reinforce- (made of type I collagen) in the extracellular matrix adapt
ment is obtained by (1) an active component (myofibers) to local function. Cells can organize the collagen struc-
being able to generate force and bear loads actively. The tures by exerting force on them (Stopak and Harris,
load bearing capacity is shared, but only passively, by (2) 1982). For example, in endomysium it takes on the form
the basal lamina and (3) the passive fascial apparatus of of a feltwork of collagen fibers (Rowe, 1981) with fibrils in
the organ. many directions (Trotter and Puslow, 1992), whereas in
The similarities between some properties of the tendon and aponeurosis they are organized in more par-
coating of reinforcing fibers in technological applications allel bundles (e.g. Leeson et al., 1985). Because collagen
and the basal lamina is striking. In this context, it is fibers are very stiff in their longitudinal direction, tendon
quite surprising to see that in early literature (e.g. and aponeuroses will be resisting tension predominantly
Häggqvist, 1920) the basal lamina is already referred in their longitudinal direction, whereas the endomysium
to as a cement or glue. The basal lamina is a very is expected to resist tension in many directions.
complex structure found in the body at the interface
between two tissues. In muscle that means that the basal 3.2. The basal lamina
lamina is coating the myofibers on one side and interfa-
ces with collagen fibers of the endomysium on its other Descriptions of the basal lamina can be found in
side (see description of intramuscular connective tissue many textbooks and reviews. Fig. 1 shows a schematic
below). representation. In transmission electron microscopy of
P.A. Huijing / Journal of Biomechanics 32 (1999) 329 —345 331
Type IV collagen differs biochemically from fibrilar (or

type I) collagen found in tendinous material. It forms
a laminar meshwork that is described as a thin but
mechanically tough mat (e.g. Alberts et al., 1994, pp.
988—991). This laminar meshwork completely envelopes
individual myofibers, and it functions as selective cellular
barrier, excluding fibrocytes from muscular tissue. It also
plays an important role as a scaffold for regenerating
myofibers. In literature there is a tendency to generalize
the properties of the basal lamina as if it were a uniform
Fig. 1. A schematic representation of the elements of the muscle basal structure. However, very local specialization of functions
lamina and their relationship to sarcolemma and endomysium. Note should be reckoned with. A prominent example of this
that the scale of the elements is exaggerated individually for clarity. the site of a motor endplate on the myofiber’s basal
lamina, which position is marked by a persistent chem-
ical specialization of the basal lamina, even after the
chemically fixed material it is seen to consist of lamina myofiber and its nerve have been destroyed. In view of
lucida (light band), which forms the interface with the this, differentiation also of mechanical function accord-
plasmalemma of the myofiber, and a lamina densa (dark ing to specific location does not seem unlikely.
band), but it should be noted that in cryofixed freeze- Generalizing information regarding many types of
substituted preparations these laminae cannot be distin- cells, it is clear that the basal lamina influence profoundly
guished (Lindblom and Paulsen, 1996) Together these the cells it covers In general, effects are identified on
layers appear in micrographs as a fuzzy coating of the phenotype, shape, motility and substrate attachment,
myofiber. Some authors do not include a reticular layer which are mediated by interactions between cell surface
in their description, but some do (e.g. Purslow and receptors and molecules of the basal lamina (Lindblom
Duance, 1990). Lindblom and Paulsson (1996) describe and Paulsen, 1996). In this mediation, laminins and col-
the reticular layer (or pars fibroreticularis) as a constitu- lagen IV appear to be particularly important (Lindblom
ent of the basement membrane, but one that is a poorly and Paulsen, 1996) Distinguishing the roles of different
limited group of elements forming the transition to the molecules in these functions from a possible role in force
connective tissue layer (i.e. the endomysium). This means transmission will require close cooperation of molecular
that the question, if this reticular layer is different from cell biologists and biomechanists.
the endomysium persists implicitly even in modern litera- One of the goals of the present work is to emphasize
ture. If it is different from the endomysium the mechan- the importance of the basement membrane for muscle
ical nature of the relationship remains unclear. biomechanics and therefore biomechanics of movement,
Probably because the functional importance of the because of its role in force transmission.
basal lamina is not always apparent in the older descrip-
tions, in biomechanics of muscle and modeling of move- 3.3. (Intra)muscular connective tissue: endomysium,
ment, its role and/or possible functional effects are al- perimysium and epimysium
most completely ignored.
The basal lamina should be considered a specialized The study of morphology of intramuscular connective
component within the extracellular matrix composed tissue is clearly hampered by the plethora of muscle tissue
mainly of a type IV collagen, heparan sulfate proteog- within a muscle: Myofibers take the overwhelming role in
lycans, as well as the glycoproteins enactin and laminin. almost any view of muscle. Despite that fact it has been
The basal lamina is synthesized by the cells that rest on it a subject of contemplation and publication for more than
(i.e. the myofiber) and performs diverse and complex three centuries (e.g. Leeuwenhoek, 1695, Holmgren, 1907;
functions. Some models of the molecular structure are Feneis, 1935; Bairata, 1937; Nagel, 1935; Rowe, 1974;
available (e.g. Yurchenco and Schittny, 1990). 1981, Borg, 1980). In general, muscular connective tissue
Laminin is considered as one of adhesive glycoproteins is described as a lattice fiber network composed of col-
and thought to play a role in adhesion of cells and other lagen. Collagen fibers run in may directions, but a prefer-
molecules to the matrix. This cell adhesion has become red direction can be recognized by distribution analysis
an important concept in cell behavior, with implications (e.g. Purslow and Trotter, 1994). Three levels of organiza-
far beyond simple attachment (Engval and Wewers, tion are distinguished (e.g. Borg and Caulfield, 1980): (1)
1966). Merosin is a generic name for any molecule contain- Epimysium surrounding the whole muscle, (2) perimy-
ing a specific (alpha 2) chain of laminin. The deficiency of sium surrounding fascicles of myofibers and is connect-
merosin is implicated in some muscular dystrophies and is ed to the epimysium and (3) endomysium surrounding
thought to play a very important role in the maintenance each myofiber and which is interconnected to the
of healthy muscle (e.g. Engval and Wewers, 1966). perimysium.
Descriptions of intramuscular connective tissue and transmitted from the intracellular milieu of the myofiber
their connections have not lead to a general awareness of (the finger like structures) onto the collagen fibers.
the importance of the fascial apparatus of the muscle for A first step in the process of myotendinous force trans-
force transmission. An important reason for that is pos- mission is applying force from the contractile proteins
sibly the rather unimpressive nature of the representation onto the structures within the sarcolemma. The sar-
of muscular connective tissue in longitudinal as well as colemma is predominantly but not exclusively a fatty
cross-sectional images obtained with transmission elec- bi-layer structure: Removal of the fatty components does
tron microscopy (e.g. Trotter and Purslow, 1992: their not prevent force transmission (Trotter et al., 1981) indic-
Fig. 4). The application of scanning electron microscopy ating that force is borne by some of the carbohy-
(SEM) improved the situation considerably (e.g Borg and drate—protein components of the membrane. At the
Caulfield, 1980; Ishikawa et al., 1983; Rowe, 1981). How- myo-tendinous junction, myofibrils do not seem to at-
ever, it was not until the SEM images of Trotter and tach directly to the sarcolemma, but thin filaments attach
Purslow (Purslow and Trotter, 1994; Trotter and Pur- to dense material thought to consist of so called ‘attach-
slow, 1992) that some of the real excitement of a new ment proteins’ (e.g. McComas, 1996, p. 8, Fig. 1.4). In the
vision was introduced. In retrospect it is not surprising process of in vitro biochemical analysis of such proteins,
that such images were obtained only after muscle tissue they have been given names as vinculin, talin, paxilin and
was removed from the organ. In particular, Fig. 1 of tensin. It is clear that relating results of in vitro biochemi-
Trotter and Purslow (1992) allows the mental picture of cal analysis in an unequivocal way to mechanics of force
muscle as an extensive 3D set of organized tunnels or transmission is very difficult, but at least there are pro-
tubes in which myofibers operate. It is this image of spective candidates for the important mechanical tasks
tunnels that has been applied at other levels of organiza- related to force transmission.
tion as well, with the goal of making inferences regarding The invaginations effectively increases the surface area
potential functional significance (Huijing, 1999, Huijing available for force transmission. More importantly, they
and Winters, 1988). Possible consequences of this idea allow shear stress to be the predominant mechanism over
will be discussed. tensile stress (Tidball, 1991; Woo and Buckwalter, 1987),
because of the low angle of application of the force. In
addition, this low the angle of loading is thought to be
4. Myo-tendinous force transmission crucial for determination of the breaking strength of the
connection (Tidball, 1983; Woo and Buckwalter, 1987).
In a most simple view of force transmission, muscle Force is transmitted onto the collagen fibers by shear-
force generated by the myofibers is transmitted to the ing of the basal lamina. Usually the collagen fibers within
tendon and from there onto the bony skeleton to cause the invaginations are referred to as being tendinous.
movement. In myology and biomechanics, particularly in Many such fibers will combine to form a sheet-like intra-
modeling approaches, in many cases this path of force muscular aponeurosis, which is reshaped into a more or
transmission is implicitly assumed to be the exclusive less round tendon outside of the muscle belly.
channel. A number of factors in myotendinous force transmis-
Reviewing possible mechanisms involved in myo-tension merit more attention in future study:
dinous transmission of force below will lead to elements
of understanding that are also useful for a more general (1) In general, little attention is paid to the relationship
view of muscular force transmission. of the tendinous fibers originating from within the
myo-tendinous invaginations to other collagenous
4.1. Transmission to and across the myo-tendinous junc- structures surrounding the myofibers. Collagen fibers
tional sarcolemma, basal lamina and tendinous collagen from the endomysium, surrounding the myofiber’s
lateral perimeter are also expected to be constituents
The mechanism of myo-tendinous force transmission of the tendon.
involves a morphological specialization of the ends of (2) It should be noted that there are some indications
myofibers. As myofibers approach their tendinous origin (e.g. Kvist et al., 1991, Akster et al., 1995) that both
or insertion their diameter decreases substantially (e.g. the length of invagination and the length along which
Loeb et al., 1987) and the sarcolemma folds extensively in a decrease of myofiber diameter is encountered are
the myofiber’s longitudinal direction These folds may a function of myofiber type: with smaller values for
described in two ways: either as invaginations of the these lengths in type I fibers. The myofiber type
plasma membrane into the myofiber or finger-like pro- specific consequences for force transmission need ex-
cesses protruding from the myofiber. Only very rarely are perimental attention. Based on geometric consider-
any of these structures seen at locations other than the ations, the length of the invaginations is also expected
ends of a muscle fascicle. Collagen fibers are located to decrease acutely with increasing myofiber dia-
within the invaginations and force is expected to be meters found as the myofiber shortens. Therefore
myo-tendinous force transmission may be less effec- 5.2. Classical experiments indicating lateral force
tive at shorter myofiber lengths. transmission
(3) The basal lamina covering the myofiber’s sarcolemma
within the invaginations is more than twice as thick as 5.2.1. From single myofibers
at the lateral surface of the myofiber (Kvist et al., 1991). Dissecting intact single and living myofibers from verte-
However consequences of this finding for force trans- brate muscular fascicles essentially consists of removing
mission have not been considered. If basal lamina neighboring myofibers until the target intact myofiber
material properties are similar at the two locations, with its basal lamina and its surrounding connective tissue
more shear strain would be expected for a given shear remains. Anyone with some experience in this Sisyphus
force at the myo-tendinous junction. work knows that it is very easy to damage the myofiber
(4) Several molecular models of trans-sarcolemma struc- surface and that such damage causes severe (and some-
tures based on in vitro studies have been proposed. times delayed) contractions that devastate the sarcomeric
However, it should be noted that, in the discussion contractile protein morphology: Contraction clots form
molecular structures which may play a role in myo- within the myofiber leaving segments of it apparently
tendinous force transmission by crossing the myo- empty of contractile proteins (Fig. 2). Such damaged
tendinous junctional sarcolemmal membrane (e.g. preparations have been used to study mechanical proper-
McComas, 1996; Woo and Buckwalter, 1987), the ties of the sarcolemma-basal lamina-endomysium troika
sarcolemma is viewed implicitly as a homogenous (e.g. Fields, 1970; Ramsey and Street, 1940; Street and
structure that is not specialized according to location. Ramsey, 1965). Despite the very unphysiological condi-
In such a view, information, regarding trans-sar- tion of such myofibers, this work has led to a number of
colemmal molecules at any location, is applied also important observations regarding transmission of force
for the region of the myo-tendinous junction. In con- (Ramsey and Street, 1940; Street and Ramsey, 1965):
trast, there have been suggestions (e.g. Monti et al., force exerted by the active single myofiber decreases only
1998, this issue) that specific molecules may play relatively little after infliction of the damage. Therefore,
a more important role in force transmission at the there must be pathways parallel to that of the mechanical
myo-tendinous junction, whereas others could be interaction of sarcomeres in series. The only possible way
more important at the lateral surface of the myofiber. seems to be transmission of force onto extracellular com-
A more local approach in the future study of the ponents associated with the single myofiber.
specific structures and mechanisms of force transmis-
sion at the myo-tendinous junction is indicated. 5.2.2. Within small fascicles of myofibers
Very convincing evidence for myo-fascial force trans-
mission was provided by Street (1983), who studied the
5. Force transmission from the lateral perimeter surface behavior of a single myofiber in relation to that of its
of myofibers: myo-fascial transmission surrounding myofibers of a small fascicles. Fig. 2 shows
the essence of the preparations used and the results:
5.1. Early inference and experimental evidence
(i) The middle of a fascicle is dissected as to leave
The idea that force transmission is not limited to the a single myofiber intact and isolated. In contrast, at other
myo-tendinous junction is certainly not new (see e.g. locations along its length, the target myofiber is sur-
Lindhard, 1931). In fact, in this early work, the intuitive rounded by its neighboring myofibers. If stretch is im-
inference was based on the established histological conti- posed on the passive fascicle, sarcomere lengths in all
nuity between the connective tissue stroma and tendon myofibers remains at approximately 2.1 lm, except for
collagen fibrils (Häggqvist, 1920; 1926) as well as as- the bare part of the target myofiber in the middle. As
sumed connections to intracellular environment Also in sarcomere lengths of 3.3 lm are reached in the bare part
some modern papers on myo-tendinous force transmis- of the target myofiber, the passive force becomes large
sion, one can recognize this idea of force transmission at enough to cause redistribution of lengths of sarcomeres
the full perimeter of the myofiber. Usually, the idea in series with in the target myofiber, i.e. shear strain with
remains implicit, but sometimes it is stated explicitly (e.g. respect to its neighbors is found.
Tidball, 1991). However, generally no experimental evid- (ii) In a second type of preparation, neighboring my-
ence is provided. The textbook Grays’ anatomy (e.g. ofibers were dissected only at one end of the fascicle
edition 1973, 1978) states this view on force transmission leaving a bare target myofiber at that location. The cut
as a fact, without referencing of sources of proof for such ends of neighboring myofibers and their connective tissue
a mechanism. It also does not supply much explanation were fixed by a pin to the environment. Active force
or discussion of mechanisms, other than referring to exerted by the target myofiber was similar, with its bare
‘viscous adhesion between myofibers and ground sub- end attached or unattached to the environment. This is
stance’. evidence that sufficient force is exerted, by the pinned
parts of the fascicle onto the part of the active target

myofiber they surround, to allow this part of the target
myofiber to remain at a length at which it can exert force.
In contrast, if unconnected at its end to the environment,
the bare end of the target myofiber is expected to shorten
to its active slack length on activation.
From these experiments it is clear that that in some

way force is transmitted laterally, bypassing myo-tendi-
nous paths. It should be noted that similar force trans-
mission has also been reported for cardiac muscle
(Winegrad and Robinson, 1978).
5.3. Molecular cell biology: myofiber cytoskeleton and

trans-sarcolemmal connections to the basal lamina
Molecular structures that may play a role in lateral

force transmission from the sarcomere to the basal
lamina were reviewed recently (Patel and Lieber, 1997)
and will therefore not be treated in detail here. Those
authors distinguished intra- and extra-sarcomeric ele-
ments of the cytoskeleton. To illustrate the general prin-
ciple of known connections to the outside world, an
illustration of extra-sarcomeric elements is provided in
Fig. 3. Four essential categories of proteins can be distin-
guished: (1) those belonging to the cytoskeleton proper,
(2) intracellular sarcolemma-associated cytoskeletal pro-
teins, (3) extracellular sarcolemma-associated proteins,
Fig. 2. Some classical experiments indicating lateral force transmission and (4) Matrix proteins (introduced above in the para-
from myofibers. (A) Image of a damaged single myofiber with a con- graphs on the matrix and basal lamina). The sar-
traction clot in the center, an ‘empty’ sarcolemma on the right side, and
presumably intact contractile proteins on the left. Such myofibers were colemma-associated cytoskeletal protein dystrophin was
reported by Ramsey and Street (Ramsey and Street, 1940; Street and given its name to emphasize the importance of the fact
Ramsey, 1965) to generate only little decreased force at its ends com- that a decreased or absent ability to synthesize this pro-
pared to the force before the damage was inflicted. (B) Sibyl Street’s tein will lead to serious muscular disease (Luna and Hitt,
elegant preparation of a small bundle to study the passive interaction 1992; Ozawa et al., 1995; Worton, 1995). This is the case
between a single myofiber and its neighboring tissues. The target
myofiber was dissected bare in the central part (indicated by ‘single in Duchenne and Becker types of muscular dystrophy.
myofiber’) by cutting away neighboring myofibers and their connective Patients with these afflictions have great difficulty keep-
tissue. On stretch of the ends of the whole fascicle, sarcomere lengths ing their muscles morphologically and functionally
increased exclusively in the single part of the target myofiber up to the
value indicated. The sarcomeres within the parts of the target myofiber,
which are in contact via the endomysium with its neighbors, as well as
the sarcomeres within the neigboring myofibers themselves, remained
approximately at the lengths indicated for those parts (2.1 lm). The
bimodal distribution of sarcomere length of the target myofiber was
redistributed after higher sarcomeres lengths than 3.3 lm were attained
in the bare center of the target myofiber (redrawn from Street, 1983). (C)
Sibyl Street’s elegant preparation of a small bundle to study the force
transmission between an active myofiber isolated at one of its ends, but
surrounded by endomysium and its neighboring myofibers at the other
end. (redrawn from Street, 1983). Only the target myofiber is activated
by electrical stimulation. Regardless if the tendon clip on the right was
attached to ‘‘ground’’ or not, a similar force was exerted at the force
transducer. This indicates that the ‘surrounded’ part of the target
myofiber did not shorten to its active slack length but was kept at
similar length with the fber end attached to ground or not.
Fig. 3. Schematic representation of general connections from within the
myofiber to extracellular space. The protein dystrophin is connected to
a dystroglycan complex associated with and crossing the sarcolemma.
This group of compounds is connected by laminin to the basal lamina.
The figure is modified from Worton (1995).
intact, which is a direct indication of the a functional used simple geometric models to argue a constant surface
importance of this molecule. Also proteins (muscle LIM area of the tapered myofiber at all sarcomere lengths. The
protein) related to the dystrophin pathways are im- endomysium was modeled using geometrical models
plicated in myocardial disease (Leiden, 1997). (Trotter and Purslow, 1992) and collagen fiber directions
Monti et al. (1998, this issue) suggest that dystrophin studied. At high sarcomere lengths, collagen fibers are
may play a more important role in force transmission at more aligned with the longitudinal direction of the my-
the myo-tendinous junction, whereas vinculin could be ofiber, but these in plane properties of the fibers are not
more important at the lateral surface of the myofiber. considered to influence trans-endomysial shear. Since it
Even though it is an inviting concept to link directly was also argued that the endomysial thickness is likely to
functional importance of molecules to possible lateral be constant, trans-endomysial shear properties may be
force transmission, however more direct evidence is constant at physiologically relevant sarcomere lengths.
clearly needed for validation of such ideas. It should be noted that these authors inferred the
existence of lateral force transmission across the sar-
5.4. Experimental evidence in whole muscle colemma within the fascicles of ‘in series myofibered’
muscles and that force is thought to be transmitted
With respect to continuity of myofibers within a fas- between adjacent non-spanning myofibers via shearing of
cicle, two types of muscles can be distinguished: (1) their common endomysium. Force would then be trans-
Muscles, consisting exclusively of myofibers which are ferred to tendinous tissues at the myo-tendinous junction
attached at both ends to either aponeuroses or bone, i.e. of the second non-spanning myofiber.
the myofibers span the full length of the fascicle. Below In his lecture at the Tokyo ISB conference, Dr. Edger-
we will refer to this type of muscle as ‘spanning myo- ton indicated that the morphology of non-spanning
fibered muscle’. (2) A type of muscle commonly referred myofibered muscle is more complex: Non-spanning my-
to as ‘in series (myo-)fibered muscle’, that is composed ofibers may be next to spanning myofibers. Such mor-
predominantly, but not necessarily exclusively, of over- phology would make the endomysial apparatus itself
lapping myofibers that do not extend from one bony or a more likely candidate for bearing the transmitted force.
aponeurotic or tendinous fiber attachment location to
the other. Such myofibers end within the length of fas-
cicles and have no typical myo-tendinous junction mor- 5.4.2. Spanning myofibered muscle
phology at least at one end: Instead these myofibers taper 5.4.2.1. Effects of partial recruitment. In a study of the
to very thin ends over relatively long distances compared compartmentalization of innervation of rat EDL muscle
to myo-tendinous myofiber ends (e.g. Eldred et al., 1993). (Balice-Gordon and Thompson, 1988) it was noticed
Sometimes this type of myofiber is referred to as a non- stimulating a branch of the peroneal nerve entering the
spanning myofiber (Hijikata et al., 1993) Muscles consist- muscle caused force to be exerted in a part of the muscle
ing partially or fully of non-spanning myofibers are very shown (by glycogen depletion) not to be innervated by
interesting objects of study, since force cannot be trans- that branch. The authors concluded that ‘there is a con-
mitted directly onto an aponeurosis at, at least, at one of siderable mechanical coupling’ between the innervation
the ends of a substantial number of myofibers. Therefore, compartments of the muscle. They hypothesized that the
mechanisms of force transmission other than myo-tendi- source of this coupling could be the ‘intramuscular con-
nous ones must be active. Experimentally, these two nective tissue and or the common connective tissue
types of muscles can be easily distinguished by the num- sheath which wraps the distal tendons’.
ber of motor end plate zones within the muscle: one zone 5.4.2.2. Acute effects of cumulative tenotomy. The par-
for the former type, two or more zones for the latter type. ticular anatomy of the EDL muscle of the lower or upper
extremity in many species makes it a very appropriate
5.4.1. Non-spanning myofibered muscle model for study of myo-fascial force transmission, be-
Functional morphology and control aspects of this cause it easily allows experimental interference with
type of muscle was reviewed fairly recently (Trotter et al., myo-tendinous force transmission without damage to the
1995) and will not be treated in full detail here. muscle (Huijing et al., 1998). In rat EDL of the leg, at its
On the basis of morphological work as well as bio- proximal end the muscle belly resembles a common
mechanical modeling, Trotter and co-workers made very unipennate muscle with rather small angles of pennation
significant contributions to our understanding of some of (e.g. Huijing et al., 1994). Myofibers attach to a common
the processes of force transmission within this type of aponeurosis, which is continuous with a tendon attached
muscle (Trotter, 1991, 1990; Trotter and Purslow, 1992; to the origin. However, at its distal end the morphology
Purslow and Trotter, 1994). Their relevant morphologi- is very specialized (Balice-Gordon and Thompson, 1988)
cal work started off with a description of tapering of to allow exertion of force on four digits of the foot
myofibers (e.g. Trotter, 1991) and considering the func- (Fig. 4). Groups of myofibers can be distinguished by
tional implications of such morphology. Trotter (1991) their distal attachments to four separate aponeuroses
(T—II—IV), EDL muscle force would be expected to drop

substantially. The magnitude of this decrease in force
would then be expected to be related to the physiological
cross-sectional area of the tenotomized head(s) (or ac-
cording to their muscle mass if the number of sarcomeres
in series within myofibers of the heads are similar, as is
the case in EDL). Fig. 4c shows some results: Optimum
force does not change appreciably after T—II and is only
altered significantly after T—IV. However, despite the fact
that, for approximately 55% of the total muscle mass, the
capability of myo-tendinous force transmission is re-
moved approximately 85% of optimum force is still
exerted after T—IV.
Length—force characteristics (Fig. 5a) show a progress-
ive shift of optimum length to higher muscle lengths with
cumulative tenotomy (Huijing et al., 1998). Results for
myofiber lengths (Fig. 5a and b) indicate three major
findings: (1) The capability to attain higher proximal
myofiber lengths at higher muscle lengths is decreased
with cumulative tenotomy. (2) This capability was not
fully removed even after T-IV, since significant increases
in proximal myofiber length are encountered. (3) No
changes in myofiber lengths of non-tenotomized part
V could be shown. The principle of the mechanism is
Fig. 4. The experimental setup, specialized morphology of rat extensor schematized in Fig. 6. It shows that active tenotomized
digitorum muscle (EDL) muscle and acute effect of progressive myofibers will exert a shear stress through the basal
tenotomy II—IV on optimum force. (A) EDL has four distal tendons
attaching to the digits of toe II—IV. The foot was clamped onto a plate lamina onto the endomysium. This will allow
and the ankle fixed at 90°. The common proximal tendon was released a tenotomized myofiber to shorten only to the limited
from its origin and attached to a force transducer. (B) Distal tenotomy extent until mechanical equilibrium reached. The
was performed cumulatively, close to the muscle belly of head II, III amount of shortening is limited by the shear strain of its
and IV. Active length force characteristics were determined. (C) Histo- basal lamina and possibly that of the endomysium shared
grams showing segment mass, cumulative muscle mass of muscle heads
connected to distal tendons and optimum force. All variables are shown with the ‘fixed’ myofiber. This process is repeated cumu-
as a percentage of their whole EDL value. Experimental conditions are latively for myofibers further removed from the un-
indicated on the x-axis: whole EDL and post tenotomy II—IV. Note tenotomized one (Fig. 6B). Therefore, myofiber length is
that, due to similar number of sarcomeres in series within myofibers of expected to decrease (i.e. a distribution of myofiber
EDL heads (Huijing et al., 1998), muscle mass connected to the distal lengths develops or is enlarged) with increasing distance
tendon should be a good relative estimator of physiological cross-
sectional area of the EDL muscle with such a connection. Note that any from the endomysial apparatus connected at both ends
decrease of optimum force with progressive tenotomy is much less than to an aponeurosis-tendon complex.
any decrease in muscle mass connected to distal tendons. Previously it has been argued that length-force charac-
teristics of the perimysium are such as to make this
structure unfit for a role in intramuscular force transmis-
each of which are continuous with four long distal sion (Purslow and Duance, 1990). Such arguments are not
tendons. These muscle heads are identified with the num- compatible with the experimental results presented above.
ber assigned to the digit they serve (II—V). Tenotomy of In fact, if one views muscle as a fiber reinforced composite
the distal tendon close to the muscle belly effectively one would expect, in general, that structures containing
removes myo-tendinous force transmission of a particu- more fibrous material would bear a higher load.
lar head and results are not affected by connections of Similar to events proposed for non-spanning fibered
any mechanical nature distal to the cut. For the particu- muscles (e.g. Trotter, 1990; 1993; Trotter et al., 1995), it is
lar conditions of this experiment, it is clear that any force conceivable that this force could be transmitted onto
exerted locally on the endomysial fascia of tenotomized active fibers of untenotomized heads and exerted through
heads will have to be transmitted, eventually, to the the myo-tendinous junctions onto the tendon(s). In our
tendon(s) of heads with intact tendons, or myofibers will experiment this would mean that, after tenotomy IV,
not be exposed to reaction forces preventing them from almost twice the force has to be carried by fibers of head
shorting to their active slack length. If myo-fascial force V. However, the length of the most distal fascicle, con-
transmission is not a very important feature of muscle, in taining myofibers of head V is not changed significantly
a progressive distal tenotomy II—IV experiment by progressive tenotomy (Fig. 5B). This is taken as an
Fig. 6. Schematic representation of the effects of tenotomy on the length

of myofibers. Hatching used to indicate basal lamina and endomysium
are identical to that of Fig. 1. (A) The initial condition after tenotomy,
indicating one myofiber still attached to ‘ground’ at both ends via its
tendon, and two myofibers for which this connection has been severed
at on one end. The endomysium between the fixed myofiber and the
first loose myofiber is also connected to ‘ground’. The contractile force
of all loose myofibers will cause shortening until an equilibrium is
reached with an opposing force, which can only be delivered by shear
stress from the basal lamina and / or endomysium. (B) Equilibrium
between shear stress and contractile force is obtained and initially
‘loose’ myofibers are prevented from further shortening. For the first
‘held’ myofiber shortening from the initial condition was made possible
only by shear strain of its basal lamina. However, for consecutive
myofibers this shortening was due to shear strain in both this structure
Fig. 5. Acute effect of progressive tenotomy II—IV on rat extensor as well as endomysium.
digitorum muscle (EDL) on length-force characteristics and the relation
between muscle length and length of the most proximal and most distal
myofibers. Mean values and standard deviations are shown. (A) EDL experimental group, the effect of interference with the
length-force characteristics are shown before and after tenotomy. Note interface between EDL head IV and V was studied (Huij-
the progressive decrease of force accompanied by a shift of optimum ing et al., 1998). Fig 7 illustrates the way partial ‘fas-
length to higher lengths. For reference percentage of muscle mass ciatomy’ was induced experimentally in two steps: (1)
connected to distal tendons is indicated in the legend following the
symbol. (B) Length of the most distal myofiber as a function of muscle First, the tendon of head IV was separated from head
length, expressed as the deviation from optimum length. This myofiber V and lifted with very little force until the most proximal
is located in EDL head V and its does not change appreciably as point of the distal aponeurosis of head V could be seen.
a consequence of tenotomy. (C) Length of the most proximal myofiber A priori, this step appeared to be a minor one. However,
as a function of muscle length, expressed as the deviation from optimum the intervention acutely caused a partial separation (ap-
length. This myofiber is located in EDL head II. Note that, although
decreased significantly and progressively with cumulative tenotomy, proximately 30%) of head IV and V at the fiber interface.
the ability to attain higher myofiber lengths at high muscle lengths is (2) The second more invasive separation of head IV and
not removed even after tenotomy IV. V was obtained by cutting intramuscularly with a scalpel
parallel to the fiber direction to about 75—80% of the
length of the interface between the heads. Fig. 7B shows
indication that the force exerted by heads II—IV in this that, from the initial condition (post T—IV), optimum
experiment was not exerted fully onto the fibers of head force decreased with progressive fasciatomy, but not
V. Instead, the force must be transmitted predominantly quite to the level expected on the basis of muscle mass.
parallel to them onto aponeurosis-tendon complex V. The observation that the degree of interference with
Therefore, the force at least partially bypasses the myo- interface between heads diminishes force transmission
fibers. This indicates transmission of force through the proportionally, suggests that fascicle connective tissue
integral connective tissue apparatus of the muscle (the sheaths are important force transmitting structures.
endomysial-, perimysial, epimysial complex, or aspects A paradoxical feature of this experiment is that very
thereof onto the aponeurosis of head V. little force is needed to interfere with the integrity of the
connective tissue at the IV—V interface and yet its is
5.4.2.3. Acute effects of progressive fasciatomy. After proposed that a large force is transmitted onto and
cumulative tenotomy using four animals of the same through that same tissue. Two factors have to be
Fig. 8. Acute effects of cumulative fasciatomy on rat extensor digitorum

muscle (EDL) length—force characteristics and the relation between
muscle length and length of the most proximal myofibers. Mean values
and standard deviations are shown. The curves for post tenotomy IV
Fig. 7. The inducement and effect of partial fasciatomy of the interface (TIV:ref) are shown as a reference. The curves after partially separating
between EDL head IV and V. Top panel: Partial fasciatomy was the head IV—V interface are indicated by the percentage of intact
induced in two ways: (a) The cut tendon of head IV was lifted until the interface lengths (70% intact and 30% intact respectively). (A)
most proximal end of aponeurosis V was exposed. Despite the minimal Length—force characteristics altered after fasciatomy: progressively de-
force needed for this intervention it caused the interface to tear for creasing force and shifts of optimum length to higher lengths. (B)
approximately 30% of the myofiber length for the whole width of the Proximal myofiber length decreases progressively with fasciatomy.
muscle (V70% intact). (b) The interface between head IV and V was However, note that even with only 30% of the interface between head
further interfered with by actually cutting through the endomysia for IV and V intact, at higher muscle length myofiber length can still be
the whole width of the muscle along an additional 1/3 of the length of its increased.
myofibers. This left only approximately 30% of the connective tissue
interface intact as measured along the length of the myofibers (V30%
intact). Bottom panel: The effect of cumulative partial fasciatomy on shift of optimum length is compatible with results on
optimum length. Note that the starting condition of this experiment most proximal myofiber lengths (Fig. 8), which shows for
was post tenotomy IV (TIV). For reference whole EDL values are also
shown (EDL). The histogram shows muscle mass, as an estimate for
cumulative fasciatomy a further decreased, but not ab-
physiological cross-sectional area, still connected to the distal tendon, sent, capability to attain higher lengths at higher muscle
to be constant (i.e. that of head V). Optimum force decreased with lengths. Fig 9 illustrates the general principle: Since no
cumulative fasciatomy but is still approximately 10% higher than reaction forces are exerted by the torn or cut en-
optimum force expected on the basis of untenotomized muscle mass. domysium a part of the myofiber not attached to ground
This indicates that myofascial force transmission from tenotomized
heads to head V is decreased but not fully prevented.
at its distal end will shorten, presumably to its active
slack length. That part of this myofiber on which shear
reaction forces are still exerted via the endomysium-basal
considered: (1) In intact muscle the force is exerted by lamina will shorten until this force is in equilibrium with
shearing, while during the process of separation of the myofiber shear forces. Therefore, the distribution of
heads a tensile force exerted at much higher angles. (2) sarcomere lengths for sarcomeres in series within the
Tensile stress—strain properties of the connective tissue myofiber is altered. Further away from the location of
network are likely to be quite different from those under fasciatomy the active principle will be similar to that after
shear (e.g. Purslow and Trotter, 1994). For studying tenotomy.
so-called ‘loose’ connective tissue this phenomenon will
have to be taken into account. 5.4.2.4. Acute effects of aponeurotomy. Aponeurotomy
It should be noted that as a consequence of cumulative involves the sectioning of the intra muscular aponeurosis
fasciatomy, length-force characteristics changed by approximately at right angles to its longitudinal direction
a shift of muscle optimum as well as active slack length to (Fig. 10). Clinically, this surgery is performed in spastic
higher muscle lengths (Huijing et al., 1998). Again the young human patients (Baumann and Koch, 1989,
Fig. 9. Schematic representation of effects of partial fasciatomy on

length of myofibers. Hatching used to indicate basal lamina and en-
domysium are identical to that of Fig. 1. (A) The initial condition after
inflicting partial fasciatomy, indicating one myofiber still attached to
‘ground’ at both ends via its tendon (fixed myofiber), and two myofibers
(‘first held myofiber’ and ‘nth held myofiber’ respectively) for which this
connection has been severed at on one end. The endomysium between
the fixed myofiber and the first loose myofiber is no longer connected to
‘ground’ due to the cut. From this initial condition, the contractile force
of all loose myofibers will cause shortening until an equilibrium is
reached with an opposing force, which can only be delivered by shear
stress from the basal lamina and endomysium. (B) Equilibrium between
shear stress and contractile force can no longer be obtained at a length
at which it can exert force for that part of the myofiber that is next to
the cut (‘slack myofiber part’): Since no opposing force is present this
part will shorten to its active slack length. For the remaining part of this
myofiber (‘partially held myofuber part’), the situation is similar to that
after tenotomy: It will be held by shear stress of the inter-myofiber
structures. However, its length is lower than after tenotomy. For con-
secutive myofibers (‘nth myofiber’), this increased shortening relative to
the tenotomy equilibrium condition (cf. Fig. 6) is passed on, due to
shear strain in both basal laminas as well as endomysia.
Fig. 10. Intramuscular aponeurotomy and its acute effects in rat medial
gastrocnemius muscle. (A) The proximal intramuscular aponeurosis is
bisected at approximately half of its length. As the muscle is stretched
Brunner, 1998). A clinical observation for these patients and / or activated it will tear the endo-perimysium complex that is
is that they have relatively short muscles, which causes, immediately below the cut. The active muscle is shown at a relatively
for example, sustained plantar flexion at the ankle. The low length with a considerable separation of aponeurosis ends but
ultimate goal of the intervention is restoring more nor- a relative superficial tear of the muscle. (B) At higher lengths the
mal patterns of gait. progressive nature of the damage to the fascia in the middle of the active
muscle belly is apparent by deepening of tear of into the muscle along
Some preliminary results of a proximal aponeurotomy the direction of the myofibers. (C) The opening of the tear is quantified
experiment on unipennate medial gastrocnemius (GM), by ‘gap length’ (l gap), i.e. the distance between severed ends of the
in situ, of a healthy rat are presented below. An acute aponeurosis. This length is a function of muscle length. Note that
effect of aponeurotomy is a tearing of the active muscle if during determination of length-force characteristics immediately after
brought to high lengths. Fig. 10B and C illustrates this aponeurotomy the muscle is altered by progressive tearing of the
endomysial structures. However, the tear is stabilized in the following
for a typical example. It shows that during the first run runs: The tear opens for the active muscle at higher lengths and now
after aponeurotomy a gap opens at higher muscle lengths this process is reproducible.
due to progressive tearing of the muscle. This tearing
resembles that of the fasciatomy experiment described for
EDL above, but is not caused directly by the experi- most proximal and most distal fascicle to muscle length.
mental intervention, as the muscle tears itself apart. The The most proximal fascicle, the myofibers of which are
results of the second and third run show that the relation still capable of myo-tendinous force transmission, does
between muscle length and ‘gap length’ did become not alter length appreciably as a result of the interven-
stable. It should be noted that this aponeurotomy pre- tion. In contrast, distal myofibers, prevented from myo-
vents myo-tendinous force transmission for the distal half tendinous force transmission, show a severely decreased
of GM. Fig. 11 shows the relationship of the length of the capability to attain higher lengths as the muscle is
5.5. Observations and implications
5.5.1. Intramuscular myo-fascial force transmission

implicates parallel pathways
The results presented for EDL above indicate that in
the partial absence of the capability of myo-tendinous
force transmission all of the force generated by afflicted
parts of the muscle is transmitted via the myo-fascial
mechanical connections to muscle parts capable of myo-
tendinous transmission. The observed decrease in force, if
any, should be ascribed to altered fiber lengths. This
means that for intact muscle, in situ, two parallel path-
ways are available: A path for transmission from sar-
comere to sarcomere in series, as well as a myofascial
path (Fig. 12)
The question arises if, in intact EDL, myofascial force
transmission is also a factor of quantitative importance.
The conclusive way to decide that would be to consider
the mechanical stiffness of the two parallel components
under many conditions: the sarcomere to sarcomere to
myo-tendinous junction pathway as well as the myofas-
cial pathway. Most force will be carried by the stiffer
component. Unfortunately little is know about the rela-
Fig. 11. A typical example of the acute effects of intramuscular tive stiffness of these components. Nevertheless, the ob-
aponeurotomy on length-force characteristics and most proximal and servations on EDL (Balice-Gordon and Thompson,
most distal myofiber length in rat medial gastrocnemius muscle. Raw
data points and fitted curves are shown for one muscle. Muscle length is 1988), would indicate there is a substantial role for non-
expressed as the deviation from optimum length of the muscle before myo-tendinous force transmission in intact EDL. As
aponeurotomy (Pre). (A) Length—force characteristics before and im- there is no evidence that rat EDL connective tissue is
mediately after aponeurotomy. During the first determination (post 1) specialized regarding this function, myo-fascial force
the changes described in Fig. 10 occur progressively, and therefore transmission is likely to be as general a feature of muscle
should not be considered proper length force characteristics. During the
second and third determination (post 2 and post 3, respectively) the as myo-tendinous force transmission.
relation between muscle length and ‘gap length’ has stabilized (Fig. 10).
However small differences can still be seen in length force curves. (B) 5.5.2. Are non-spanning myofibered muscles made up of
The effect of aponeurotomy on length of the most distal myofibers. myofibers in series?
Note that this length has decreased abruptly for the ‘post 1’-condition It should be noted that, if the mechanism of
to values that do not differ from the ‘post 2’ and ‘post 3’ condition..
However, despite the fact that distal myofibers are not connected any myo-fascial force transmission is similar for ‘in series’
longer to the muscle’s origin by the aponeurosis, they attain higher myofibered muscle, this very name is to be considered
lengths at higher muscle lengths. This is indicative of myofascial force a misnomer. If force is transmitted from myofibres onto
transfer. (C) Aponeurotomy has no appreciable effect on length of the the the intramuscular connective tissue, the myofibers are
most proximal myofibers. These myofibers remain connected to the arranged in parallel. This argument supersedes the char-
muscle’’s origin and insertion via aponeuroses. This indicates that these
myofibers in this part of the muscle act in a way comparable to that in acter of simple semantics as it would indicate a significant
the intact muscle in situ. flaw of our understanding of the mechanics of the force
transmission in such muscles. Viewing the functional
implications of parallel force transmission in muscles, in
brought to higher lengths. It should be noted that this which fascicles are longer than their myofibers, the length
capability to attain higher lengths is not fully absent. range of active force exertion, the fraction of that length
Such behavior of myofibers is indicative of diminishing range used for in vivo motion, total physiological cross
but not obliterated intramuscular myo-fascial force sectional area and maximal force should be considered.
transmission in aponeurotomized GM. Study of length—force characteristics in relation to quan-
Several points should be made which contrast with tified muscle morphology may help to settle this issue.
results from EDL fasciatomy experiments: The initial
drop in isometric force is more severe, but subsequently 5.5.3. Shear, pennation and effectiveness of myofascial
decreases less progressively than in the EDL experiment. force transmission
Also, hardly any shifts of optimum lengths are seen. The Since shearing is shown above to play such an impor-
explanation for these differences are not immediately tant role in myo-fascial force transmission it is important
apparent and will have to be analyzed in more detail. to ask if shearing occurs in all muscles in all conditions.
mission may different for muscles of different degrees of

pennation and dependent on muscle length for a given
muscle. It is clear that such issues should not be ad-
dressed only in a geometrical context but can be better
tackled in the context of mechanical equilibrium, using
finite element models of muscle (e.g. Donkelaar et al.,
1996; Linden et al., 1995).
5.5.4. Muscular connective tissue as a carrier of blood

vessels, nerves and receptors
It should be realized that the endomysial—peri-
mysial—epimysial complex not only plays a role in force
transmission but also is the carrier of vessels, nerves an
some receptors. Viewing corrosion casts of blood vessels
in a muscle (e.g. Ishikawa et al., 1983; Kessel and Kardon,
1979) shows the likelihood that blood vessels will affect
mechanical properties of the intramuscular connective
tissue apparatus in which they are laid down (see also
Nagel, 1934). The same will be true for nerves: It is
common knowledge among micro-dissectors of muscle
that more resistance is encountered at locations at which
even small nerves cross myofibers transversely. Detailed
descriptions of muscle receptors (spindles, tendon organs,
Pacianian corpuscles, Golgi-, Ruffini and free endings)
have been reported (e.g. Barker, 1974). Since, for example,
Fig. 12. Observations on aspects of myo-fascial force transmission. (A) muscle spindles have diameters of the same order of
Myo-facial force transmission implicate parallel pathways: The myo- magnitude as extracapsular myofibers it is clear that they
fascial path and the path of sarcomeres in series (sarcomere or ‘CE’ will affect the local mechanical properties of the connect-
path). This is shown by Hill type models. (B) For any experiment using
an in situ muscle, which is isolated from its surrounding tissues, the
ive tissue in which they are embedded and therefore
parallel paths have to come together at the aponeurosis or tendon to be possibly local force transmission. Considering myofascial
able to exert force onto the force transducer. (C) This may not always be force transmission, a review of the function of these
true for the same muscle in vivo, as its connective tissue apparatus is receptors and the type of information they are thought to
continuous with that of other muscles of the limb and that of the limb encode, seems indicated but is beyond the scope of the
itself. Therefore, it is conceivable that force is transmitted out of
a muscle and is exerted onto bone by structures parallel to the source
present work.
muscle’s tendon. In such a case the concept of the morphologically
defined muscle as a functional unit would not be valid. (D) Shear strain
along the length of myofibers is an essential element of myo-fascial force 6. Force transmission in limbs in vivo
transmission. This simple geometric schema indicates that the acute
angle of pennation of myofibers will have a substantial influence on the
amount of strain which may indicate effects of muscle length as well as
Scientific progress can be very dependent on appropri-
of degree of pennation on the efficacy of this type of force transmission. ate imaging. The early definition of a muscle as an entity
goes all the way back to the 16th century work of
Vesalius (e.g. 1555). His beautiful drawings caused
a break with the past (e.g. Bastholm, 1950) and put
A simple start in addressing this question may be made human anatomy and knowledge of the locomotor appar-
by viewing Fig. 12D which shows schematically the cross atus in one major step on a much higher level. Those
section of two slanted cylinders representing myofibers. drawings clearly show individual muscles as morphologi-
As myofibers shorten they will always increase the angle cal units after dissection. The definition of muscle as
with their attachments which involves shear. The mark- a such a morphological unit is based on the epimysial
ing on the myofibers shows clearly that the amount of system. In our present view, dissection may be regarded
shear strain is dependent on the actual myofiber angle as liberating the muscle, or the connective tissue tunnel
(higher shear at higher angles) and thus myofiber length or tube in which it is operating, from its surrounding
(higher shear at lower lengths). The effectiveness myo- (connective) tissues.
fascial force transmission is dependent on the resistance In myology, most animal experiments aimed at the
against shear. For a given myofiber length change more organ level are performed on dissected muscle in situ,
resistance is likely to be encountered at higher myofiber with nerves, blood vessels and tendons intact. To review
angles. Therefore the effectiveness of myo-fascial trans- implications of this work for force transmission in vivo,
differences between in situ preparations of muscle and with the classical anatomical definitions of muscles and
the fully intact in vivo situation have to be considered. ligaments. They also argued that the organization of the
After dissecting a muscle free, from its surrounding con- neural receptor apparatus is compatible with such new
nective tissues, the morphological unit also must be the views of limb connective tissue architecture. Due to this
functional unit. This means that experiments on isolated result, our classical system of definitions seems to break
muscle-tendon complex in situ, are designed in such down. This can also be illustrated for intermuscular septa,
away that force has to be transmitted via the endomysial which are structures separating major muscle groups (e.g.
apparatus and/or via the myo-tendinous junctions onto flexors or extensors of a joint). Septa are continuous with
the tendons to be exerted onto the bones (or force trans- the general fascia, and together they group sets of epi-
ducers). In our particular EDL experiment involving mysia. On these structures van der Wal (1988) reported
tenotomy (Huijing et al., 1998), force had to be transmit- the following: ‘‘For instance a structure like the supinator
ted exclusively onto the endomysial apparatus in parts of septum may be classified as epimysial fascia but also as
the muscle before it could be exerted on the aponeur- aponeurosis or tendon2’’ (Wal, 1988, p. 54).
osis—tendon complex. (2) Mechanical studies involving comparison of, in vivo
The perimysium is regarded as a continuous system of and in situ, muscular properties in animals. Differences
tunnels or tubes in which fascicles of myofibers operate. were reported for the cat soleus muscle regarding muscu-
It is continuous with the endomysial system of tunnels. lar mechanical variables during gait as measured with
In the same way, epimysia may considered a system tendon force transducers (Gregor et al., 1988): 2. ‘‘Force
of tunnels for the operation of muscle, which is continu- and power generated at a given velocity of shortening
ous to higher levels of connective tissue organization during late stance in vivo were greater at the higher
(general fascia) as well as lower levels (peri-end speeds of locomotion than the force and power generated
endomysia). Therefore, in vivo there is a potential at the same shortening velocity in situ’’. It should be
additional route for force transmission out off the realized that this comparison is made for maximally ac-
muscle, bypassing completely the tendon of the muscle tivated muscles in situ to submaximally active muscles
which was the source of the generated force (Fig. 12C). during gait. Gregor et al. concluded rightly that ‘‘some
Considering this possibility, the question needs to be mechanical perturbation must be present in concert with
asked if, in vivo, the muscle may also be considered an active muscle’’. Explanations put forward by these
a morphological and functional unit? If force is actually authors were potentiation by previous stretch and/or
transmitted out of the muscle in this way this is not the elastic contribution to shortening. Ingen Schenau et al.
case. In view of these idea’s, we suggested that the con- (1997) indicated that the question if, in vivo movements,
cept of muscle should be scrutinized for possible revision myofibers are stretched at all even if muscle tendon
and evaluation of functional consequences (Huijing, complexes are. In the same work series elastic energy was
1999: Huijing and Winters, 1988). argued against as a general contributor (Ingen Schenau
However, before even accepting the theoretical possi- et al., 1997). Instantaneous moment angular velocity
bility of intermuscular force transmission it would be characteristics of human jumping compared to a more
wise to search for some experimental evidence that could classical moment angle curve during isokinetic ergometer
be regarded as direct or at least indirect support main- controlled movement (Bobbert and van Ingen Schenau,
taining such views. Three catagories of reports of findings 1990) showed similar results as those of Gregor et al.
were encountered in literature that are quite surprising However, it should be realized that in this human move-
and may be explained by, or are at least be compatible ment the same level of muscular activation was experi-
with, this concept: mentally strived for or modeled. Therefore, it is a major
difference in level of activation in Gregor’s experiment
(1) Morphological study of interrelationships of muscle that allows room for alternative explanations. Thus, it is
and other structures. The study of 3D reconstruction of conceivable that the mechanical perturbation at hand
the architecture of the forelimb of the rat by van der Wal was force transmitted myo-fascially from other plantar
et al. (1988, see also Strasmann et al., 1990) seems to cast flexors onto the Achilles tendon.
some doubt on an affirmative answer to the proposal of (3) Studies after surgical intervention in patients. Fig. 13
muscle as a functional unit. First of all, they showed that shows schematically the experimental setup of an experi-
muscular and joint connective tissue are generally not to ment performed on human subjects and patients in which
be considered separate entities, but that muscle epi- and the moment exerted by the rectus femoris muscle (RF)
perimysium are continuous with collagenous fibers of was determined during intramuscular stimulation
joint capsule so that new functional muscular-connective (Riewald and Delp, 1996). In agreement with the general
tissue units are to be distinguished. Secondly it was view, in healthy subjects a knee extension moment was
reported (Wal, 1988), that particularly proximally in the found. In surgery on patients, the insertion of RF was
rat forelimb (i.e. the elbow region), these muscular-con- transplanted to a site posterior or lateral of the knee joint
nective tissue functional units do not always coincide axis (either the m. semitendinosus insertion or iliotibial
become its own antagonist with as a net result knee

extension moments.
Beyond studying these preliminary indications, con-
clusive experiments should be designed, specifically
aimed at validating the occurrence of intermuscular force
transmission. It is clear that such experiments should
involve a number of approaches: (1) a biomechanical
approach in animal experimentation in which the inter-
face of target muscles is interfered with and the effects on
force transmission studied. (2) imaging and analysis of
fully intact in vivo muscle of humans and experimental
animals under conditions of controlled co-activation. To
Fig. 13. A schematic representation of methods and results of an
experiment on human subjects and patients with transfer of the distal
once more stimulate scientific progress, appropriate
tendon of knee extensor rectus femoris muscle (RF) to assumed flexor imaging may be obtained by applying ultrasound imag-
positions. The figures are modified from (Riewald and Delp, 1996). (A) ing (e.g. Fukunaga et al., 1997) or magnetic resonance
Rectus femoris muscle of all subjects was stimulated intramuscularly. imaging (MRI) The advantage of the former is that fas-
Two groups of subjects are compared: 1. Healthy subjects and 2. cicles of myofibers can be easily seen, whereas for MRI
Patients after transfer of the distal tendon of RF to the location of either
the insertion of semitendinosus muscle or of the tractus iliotibialis. It
special techniques can be applied to identify and track
should be noted that in both cases RF tendon passes posterior to the defined volumes of tissue (e.g. Sheehan et al., 1999). (3) If
axis of the knee joint leading to expectation of flexor knee moments on possible combinations of the biomechanical and imaging
stimulation of RF. (B) Moments exerted at the knee for control subjects approaches should be aimed for.
and patients. The latter show, counter to expectations, extensor mo-
ments rather than flexor moments. This is compatible with myo-fascial
force transmission in the proximal part of RF in patients to the
connective tissue apparatus of the limb on the extensor side of the knee 7. Conclusions
joint. In such a case, RF would be its own antagonist exerting flexor
moments transferred through its tendon across the knee joint and Within in situ muscle, two parallel pathways for intra-
extensor moments originating from its proximal parts transferred muscular force transmission can be distinguished: (1) in
through connective tissue other than that of RF. The net effect of these
two actions still being a knee extension moment.
series sarcomere to sarcomere to tendon (myo-tendinous
transmission), and (2) sarcomere to myo-fascial complex
(myo-fascial to tendon transmission). In maximally
band) for reasons of stiff knee gait, due to spasticity. active isolated muscle in situ, each of these paths
Surgery was clinically successful as knee range of motion seem to be able to bear the full isometric force production
improved, but that may also be attributed to additional of the muscle. Interference with the myofiber interface
orthopedic procedures performed in surgery. However, (as in intramuscular fasciotomy) interferes with the
very surprisingly these patients still showed knee exten- efficacy of the myo-fascial force transmission. In addi-
sor moments on intramuscular stimulation of RF, in tion, in muscle within an intact limb it is conceivable
contrast to expected larger or smaller flexor moments. that at least some force is transmitted via the connective
Riewald and Delp (1996) concluded that force may have tissue system to bone by paths other than by a muscle’s
been transmitted in some way from RF onto other knee own tendon. Some experimental observations are
extensors. compatible with that idea. This suggests that the
morphologically defined muscle is not the functional unit
The authors indicated that, in surgery, RF was not in all cases.
freed from surrounding fascia along the proximal half of Considerable further biomechanical as well as physio-
the muscle. Using the concept of myofascial force trans- logical work on these phenomena is indicated. For
mission their result may be interpreted as follows. Part of modeling, both finite element models and models de-
the force is transmitted along each of the parallel path- scribing the fiber-reinforced composite nature of muscle
ways: (1) laterally in the proximal part of RF onto the may help to advance our understanding. Clinical im-
fascial apparatus of RF and the remainder of the force is plications should be considered as well.
transmitted longitudinally through sarcomeres in series Even if the idea of intermuscular force transmission
onto the myo-tendinous junction (2) Part or all of the would be validated, it is not indicated to cease all experi-
myo-fascially transmitted force is transmitted via the mental work on muscle in situ. On the contrary, a lot of
connective tissue apparatus onto neighboring knee ex- that type work will be necessary to answers questions
tensors (as in rat EDL tenotomy experiments) yielding raised here. However, as an additional activity, much
extensor moments at the knee. Any force transmitted to more attention should be focused on the issue that, in
the distal RF tendon will, because of the transplantation, vivo, the muscular action may be more than the sum of
yield knee flexor moments. In effect the muscle has the parts involved.
Acknowledgements Eldred, E., Ounjian, M., Roy, R. R., Edgerton, V.R., 1993. Tapering of
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duction of the manuscript and their enthusiastic support: Biophysical Journal 10, 462—479.
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E Guus C. Baan, Guido Rebel and Richard Jaspers pres- Determination of fascicle length and pennation in a contracting
ently at the Vrije Universiteit, Amsterdam; human muscle in vivo. Journal of Applied Physiology 82, 354—358.
E Bart Koopman, Henk Grootenboer, Kenneth Meijer, Gregor, R.J., Roy, R.R., Whiting, W.C., Lovely, R.G., Hodgson, J.A.
Bart van der Linden, Johan Pel, Guido Rebel formerly and Edgerton, V.R., 1988. Mechanical output of the cat soleus during
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comparative animal experimental work. locomotor apparatus and neuromuscular control of movement. In:
Crago, P., Winters, J.W., (Eds.), Biomechanics and Neural Control of
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Journal of Biomechanics 32 (1999) 329—345

ISB Keynote Paper — 1997

1. Introduction junction’s specialized morphology, regarding folding and

2. Fiber-reinforced composites 3. Elements of extracellular space

The term fiber-reinforced composite is derived 3.1. The extracellular matrix

Type IV collagen differs biochemically from fibrilar (or

parts of the fascicle onto the part of the active target

From these experiments it is clear that that in some

5.3. Molecular cell biology: myofiber cytoskeleton and

Molecular structures that may play a role in lateral

(T—II—IV), EDL muscle force would be expected to drop

Fig. 6. Schematic representation of the effects of tenotomy on the length

Fig. 8. Acute effects of cumulative fasciatomy on rat extensor digitorum

Fig. 9. Schematic representation of effects of partial fasciatomy on

5.5. Observations and implications

5.5.1. Intramuscular myo-fascial force transmission

mission may different for muscles of different degrees of

5.5.4. Muscular connective tissue as a carrier of blood

become its own antagonist with as a net result knee

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