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Force Transmission between Synergistic Skeletal Muscles through Connective

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Hindawi Publishing Corporation
Journal of Biomedicine and Biotechnology
Volume 2010, Article ID 575672, 9 pages
doi:10.1155/2010/575672

Review Article
Force Transmission between Synergistic Skeletal Muscles
through Connective Tissue Linkages

Huub Maas1 and Thomas G. Sandercock2

1 Research Institute MOVE, Faculty of Human Movement Sciences, VU University, Van der Boechorststraat 9,
1081 BT Amsterdam, The Netherlands
2 Feinberg School of Medicine, Northwestern University, 303 East Chicago Avenue, Chicago, IL 60611, USA

Correspondence should be addressed to Huub Maas, h.maas@fbw.vu.nl

Received 30 November 2009; Accepted 1 February 2010

Academic Editor: Henk L. M. Granzier

Copyright © 2010 H. Maas and T. G. Sandercock. This is an open access article distributed under the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.

The classic view of skeletal muscle is that force is generated within its muscle fibers and then directly transmitted in-series, usually
via tendon, onto the skeleton. In contrast, recent results suggest that muscles are mechanically connected to surrounding structures
and cannot be considered as independent actuators. This article will review experiments on mechanical interactions between
muscles mediated by such epimuscular myofascial force transmission in physiological and pathological muscle conditions. In a
reduced preparation, involving supraphysiological muscle conditions, it is shown that connective tissues surrounding muscles are
capable of transmitting substantial force. In more physiologically relevant conditions of intact muscles, however, it appears that the
role of this myofascial pathway is small. In addition, it is hypothesized that connective tissues can serve as a safety net for traumatic
events in muscle or tendon. Future studies are needed to investigate the importance of intermuscular force transmission during
movement in health and disease.

1. Introduction The most recognized pathway of force transmission from

muscle fibers to bone is via the specialized myotendinous
When skeletal muscle fibers are excited, a cascade of events junction [1] and tendon, named myotendinous force trans-
is triggered, which ultimately leads to forces exerted on the mission. Classical anatomy has defined each muscle as a
skeleton. Muscle forces are needed for movements, such as separate entity with a unique function at the joint(s) it spans.
locomotion, and the maintenance of body balance. There Therefore, it has long been common to view muscles as
are many structures involved at several levels organization: mechanically independent actuators. This is readily apparent
from actin, myosin, and titin of the sarcomeric cytoskele- from biomechanical models of the musculoskeletal system
ton, desmin of the intermyofibrillar cytoskeleton, transsar- in which muscles are connected to the skeleton at their
colemmal proteins such as dystrophin and integrin of the origin and insertion [2, 3]. However, many scientists from
subsarcolemmal cytoskeleton, endo-, peri-, and epimysium, the last century were aware of mechanical interactions
as well as tendon and aponeurosis at the muscle level to inter- between muscles (for a historical overview see [4]). For
and extramuscular connective tissues (e.g., the neurovascular example, during measurements of soleus muscle forces in
tract, fascia) at the compartmental level. For understanding the cat, upon stimulation of the lateral gastrocnemius-
how forces are transmitted from sarcomere to the bony soleus nerve branch Denny-Brown [5] noticed that “. . .it
skeleton in normal and diseased muscle, it is necessary to is found to be extremely difficult to avoid a slight early rise
investigate the role of each of these structural elements as of tension, and fall in the plateau, due to the vibration or
well as their interaction. The present review focuses on the pull of gastrocnemius.” More recently, Nichols [6] stated
connective tissues that are found in the direct environment of “Mechanical artifacts due to direct mechanical action of
skeletal muscles and their potential effects in muscle function the stretched muscle on those isometrically constrained were
during movement. indicated by essentially instantaneous latencies or by effects
2 Journal of Biomedicine and Biotechnology

observed after pharmacological block of heterogenic reflexes.” Muscle fiber MTJ Tendon Bone
Note that in these experiments the tendons are severed
from their insertion site and individually connected to force 1. Intramuscular
transducers. This means that the mechanical linkage was connective tissue
provided by structures at the muscle belly boundary (i.e., the Intermuscular Tendon
2.
epimysium). connective tissue
The purpose of this article is first to review the initial Extramuscular
3.
connective tissues
series of systematic experiments on mechanical interactions
between synergistic muscles (i.e., neighboring muscles which
produce the same movement at the joint) via connective 3.
tissue linkages (named epimuscular myofascial pathways)
that revealed the presence and capacity of this phenomenon 1.
(mechanical interactions between antagonistic muscles have
been reviewed elsewhere; see [7]); second, to discuss the
current debate on the importance of epimuscular myofascial 2.
force transmission during normal movements; and third, to
discuss the potential functions of inter- and extramuscular Figure 1: The different pathways via which force generated within
connective tissues for pathological muscle-tendon condi- muscle fibers can leave the muscle to be transmitted to the skeleton.
tions. Two epimuscular pathways are distinguished. (i) Intermuscular:
force transmission between two neighboring muscles via the
continuous connective tissue at their muscle belly interface. (ii)
Extramuscular: force transmission between a muscle and adjacent
2. Mechanical Interaction between Muscles nonmuscular structures. The term epimuscular myofascial force
through Connective Tissue Structures transmission is used to indicate transmission via inter- or extramus-
cular pathways.
2.1. Epimuscular Myofascial Pathways. Epimuscular myofas-
cial force transmission is defined as transmission of muscle
forces to the skeleton via pathways other than the muscular
origin and insertion. A direct proof of epimuscular myofas- muscle). Tendons appear to run together. Pushing or pulling
cial force transmission is a difference in force exerted at the on one muscle leads to movement of a neighbor. Thus,
origin (proximal) and insertion (distal) of a muscle. Another muscles are unquestionably linked. The question is how
feature of this phenomenon is that length changes in one significant these links are to the normal function of muscle.
muscle can affect forces exerted at the tendons of muscles
that are kept at a constant length. 2.2. Mechanical Interactions between Muscles in the Anterior
Two epimuscular pathways are distinguished (Figure 1): Crural Compartment. An in-depth analysis of transmission
(i) intermuscular, if force is transmitted between two neigh- of extensor digitorum longus (EDL) muscle force in the rat,
boring muscles via the continuous connective tissue at their which is embedded within the anterior crural compartment
muscle belly interface, and (ii) extramuscular, if force is together with extensor hallucis longus (EHL) and tibialis
transmitted between the epimysium of a muscle and an anterior (TA) muscles, has been performed. Because both
adjacent nonmuscular structure. The direct intermuscular the proximal and distal tendons of EDL can be attached
pathway is provided by an areolar connective tissue layer to force transducers, EDL is a very suitable muscle for
at the interface between muscle bellies (for images see [8]). the assessment of epimuscular myofascial effects. Isometric
Several structures provide an anatomical substrate for the forces were measured simultaneously at the proximal and
extramuscular myofascial pathway: (i) the matrix supporting distal tendons of EDL muscle as well as at the tied distal
nerves and blood vessels, that is, the neurovascular tract tendons of TA, and EHL muscles. These tendons can all
(see [8, 9]) (Note that the neurovascular tract is continuous be dissected with minimal disruption of the compartment,
with the extensive intramuscular connective tissue network, leaving epimuscular myofascial pathways mostly intact. By
which reinforces the nerves innervating muscle fibers and manipulating the position of the force transducers, the
the blood vessels entering the muscle.), (ii) fascia layers muscle-tendon complex length of one or all muscles as well
forming the borders of synergistic muscle groups that are as muscle relative position were changed.
continuous with more superficial layers (e.g., subcutaneous Mechanical interactions between EDL and TA + EHL
connective tissue), and (iii) connective tissue around tendons were found for various experimental conditions. Length
(for images the reader is referred to previous publications, changes of the TA + EHL complex affected the forces exerted
e.g., [10–13]). at the proximal and distal tendons of EDL, which was kept
Dissection of a limb shows a vast network of collagen- at a constant length [9]. More specifically, lengthening TA
based structures linking muscles together. Clearly muscles + EHL distally increased proximal EDL force (by 37%),
are connected by fascial sheets, loose areolar tissue, vascular but decreased distal EDL force (by 39%). The mechanical
links, nerves, and supporting collagen. Sometimes muscle interactions between synergistic muscles can be ascribed
fibers originate from neighboring muscle (e.g., in the cat to changes in the position of one muscle relative to the
there are some LG fibers that seem to terminate in MG other [15] and, consequently, changes in the configuration
Journal of Biomedicine and Biotechnology 3

Proximal Distal Proximal Distal Position effects can be explained by changes in the configu-
F↑ F↓ ration of the tissues representing the epimuscular myofascial
pathways (Figure 2). In general, the muscle end that is
positioned farthest in a particular direction (e.g., distal) will
Figure 2: Schematic drawing to illustrate changes in the configu- draw force from neighboring muscles.
ration of connective tissue between two muscles if one muscle is
lengthened. Modified from Maas et al. [14].
2.3. Do Mechanical Interactions between Muscles Occur In
Vivo? The above in situ studies have shown the potential of
force transmission between skeletal muscles via inter- and
(length and angle) of inter- and extramuscular connective extramuscular connective tissues. The functional relevance
tissues (Figure 2). It may appear obvious to explain these of this phenomenon is dependent on the magnitude of the
results by mechanical effects of intermuscular connective effects found in physiological muscle conditions. However,
tissue. However, EDL, TA and EHL are also linked to each this mode of force transmission may be small in normal mus-
other via extramuscular structures. A clear example is the cles during physiological conditions, because (1) the above
neurovascular tract that runs in between the muscles while studies all used tetanic stimulation. This rarely occurs during
giving off branches of nerves and blood vessels which enter voluntary movement, so observations may be relevant only
the endo-perimysial network of the muscle [8, 9]. Therefore, to lab conditions; (2) the muscle-tendon complex length of a
we conducted a followup study to investigate the contribu- single muscle was changed while the length of its synergists
tion of each pathway [16]. Equal experimental conditions was kept constant, compared to simultaneous length changes
were imposed before and after disruption of the connective in synergistic muscles during normal movements; (3) when
tissue layer between EDL and TA + EHL, thereby eliminating individual muscles are stimulated alone and together, the
force transmission via intermuscular myofascial pathways. force sums linearly which is surprising if the epimuscular
This significantly decreased the effects of TA + EHL length pathway is used; and (4) a recent experiment studying force
on force exerted at the distal tendon of EDL. However, the transmission between cat soleus (SO) and its synergistic
interaction between TA + EHL and proximal EDL force muscles in an intact animal showed little epimuscular force
did not change. Therefore, we concluded that mechanical transmission. Each of these points will be discussed below.
interactions between synergistic muscles originate from both In the studies described up to this point, the effects
inter- and extramuscular connective tissues. Besides the of epimuscular pathways on muscular force transmission
above-described study [16], there is only one other study were tested predominantly during simultaneous maximal
[10] that reports data indicating that the areolar connective activation of both synergistic and antagonistic muscles.
tissues are stiff and strong enough to transmit force. Changes Coactivation of synergistic and antagonistic muscles has
in the length-force characteristics were found following been observed in the awake, freely moving animal (e.g.,
disruption of the intermuscular myofascial pathway [10]. [18]), but in most cases at submaximal levels of activation
In the above-described studies, relative displacements (e.g., [19]). Recently, using the in situ setup described above,
of muscle bellies were the result of length changes in a substantial proximo-distal EDL force differences (up to 30%
single muscle group. To distinguish between effects of muscle of maximal force at each frequency) as well as mechanical
length and relative position, isolated effects of muscle relative interactions with TA + EHL were found during nerve
position were studied [14]. The muscle-tendon complex stimulation at submaximal frequencies (10–30 Hz) [20]. This
length of EDL and TA + EHL was kept constant. The position suggests that also at firing frequencies encountered in vivo
of EDL muscle relative to its surroundings was changed by muscle forces can be transmitted via epimuscular myofascial
moving both the proximal and the distal tendons to an equal pathways.
extent and in the same direction. Displacements of EDL in Another experimental condition of the studies described
distal direction decreased force exerted at the distal tendons in Section 2.2 that was different from the conditions under
of TA + EHL. Simultaneously, distal EDL force increased and which muscles function in vivo was changing the length
proximal EDL force decreased. Force changes in opposite of only one muscle. Due to differences in moment arms
direction were found if EDL muscle was repositioned more between synergists [21, 22], the change in length of one
proximally. Each movement affected the proximo-distal force muscle can be different from that of its neighbor, but the
difference and, thus, the magnitude of net epimuscular relative movements imposed during lengthening a single
myofascial force transmission. In addition, the sign of the muscle were beyond the physiological range. Recently, this
force difference between proximal and distal EDL forces issue was addressed by investigating proximal-distal force
changed. Similar effects of muscle relative position were differences in EDL muscle while lengthening EDL, TA, and
reported for slightly different experimental conditions [17]. EHL simultaneously, as is the case during ankle movements
Length-force characteristics of EDL muscle obtained by [23]. Also in these experimental conditions, a large force
movements of the distal tendon were significantly different difference (up to 30% of maximal force) was found. At
from its length-force characteristics if EDL muscle was submaximal stimulation frequencies, however, the difference
lengthened by moving its proximal tendon. (5%) and, hence, net epimuscular myofascial force transmis-
In conclusion, the position of a muscle relative to sion became small [23]. It should be noted that different
surrounding tissues codetermines isometric muscle force. myofascial pathways can be arranged in such a way that
4 Journal of Biomedicine and Biotechnology

they exert forces on a muscle in opposite direction (see [9,

Figure 8]) and that the proximo-distal force difference is
the net result of all myofascial loads [7]. A small difference Hip fixation
can thus be explained by limited epimuscular myofascial
force transmission or opposing myofascial loads of similar
magnitude.
If force transmission through epimuscular pathways is
substantial, then nonlinear summation of force is expected
when different muscles are activated alone and together.
Nonlinear force summation is defined as the difference Ankle
between the force exerted when two muscle parts are excited Knee
simultaneously and the sum of the forces exerted when each 90◦
muscle part is excited individually [24]. Force transmission 6 degree-of-freedom
between the medial gastrocnemius (MG) and lateral gas- load cell on robotic arm
trocnemius/soleus muscles (LG/SO) was studied in the cat
hindlimb [25, 26]. The muscles were activated by stimulation
LG and PL
of the nerve branches to each of the muscle groups. LG and
SO
SO muscles were stimulated together because of the difficult
surgery required to separate their nerves (see [27]). The cat Figure 3: A schematic presentation of the cat hindlimb in the
hindlimb was left intact and the foot attached to a 6-degree- experimental setup used to investigate inter-synergist interactions
of-freedom (dof) load cell to measure force and torque. The [28].
femur was fixed to a rigid frame. MG was stimulated alone,
LG/SO alone, and then both together. When both muscles
were stimulated together, the resulting forces and torques
(all 6 dof) were less than the sum of the individual forces. (PL) muscles share an interface with SO [29]. Ankle moment
The peak error occurred during the onset of activation where exerted upon the isolated excitation of SO was measured
force was about 9% less compared to the plateau where at various knee angles while the ankle was kept at a
steady state force was about 2% less. There was no evidence constant position (∼90◦ ), using a 6-degree-of-freedom load
that the direction of the forces changed during simultaneous cell coupled to a 6-degree-of-freedom robotic manipulator
activation of the muscles compared to activation of the (Figure 3). Note that knee movements will only alter the
muscles independently. These results suggest that when both length and relative position of the two-joint muscles, but
muscle groups were activated together there was increased not of SO. This involves the greatest relative displacements
shortening of the muscle fibers, and hence less force due between these muscles in vivo. We hypothesized that force
to a higher velocity of shortening during force onset. Thus, transmission from SO muscle fibers will be affected by length
there is some interaction, either between the muscle bellies or changes of its synergists through configuration changes of
between their tendons. However, the interaction was small, connective tissues between these muscles.
and during steady state, it was almost immeasurable. Similar Changing the knee angle from 70◦ to 140◦ lengthened
experiments were performed on the vastus medialis and LG and PL profoundly (4.5–7.2 mm), as calculated using
rectus femoris in cat. Both muscles are knee extensors. They the geometric model presented by Goslow et al. [30]. In
share a border and a tendon and thus may be expected contrast to our expectations, active ankle moment generated
to show nonlinear summation. Nonlinear summation error by SO and the rate of muscle relaxation were not significantly
was small in all 6 degrees of freedom. The average peak affected by changes in knee angle. These results demonstrate
error was 8.4% and the mean average error during the that the presence of relative muscle movements does not
contraction was 1.3% (unpublished observations). Note necessarily mean force transmission between muscles. To
that these experiments do not preclude epimuscular force further test the apparent independency of SO, an additional
transmission, but rather suggest that in normal muscle it has set of experiments was performed. With minimal disruption
little functional effect on the overall force delivered to the of the connective tissues at the muscle belly level, the distal
skeleton. tendon of SO was dissected free from the other tendons
To tackle some of the concerns of previous studies, a new in the Achilles tendon complex, cut, and connected to a
experimental approach was developed to measure directly force transducer. As this eliminated force transmission to
the mechanical interactions between muscles in conditions its insertion on the calcaneus, any ankle joint moment
that simulate those present during normal movements [28]. following SO excitation was attributed to force transmission
The latter was assured by testing the muscles in a nearly intact via epimuscular myofascial pathways to the Achilles tendon.
limb of the cat. The tendons were not cut, but left attached If the tendon of SO was placed at its original position,
to their insertion sites. Length changes were obtained by corresponding to the above reported ankle joint angle, the
movements of the joints and, thus, only physiological relative moment exerted at the ankle was close to zero while force
movements could be imposed. The mechanical interactions exerted at the distal tendon of SO was near its optimal value.
between the one-joint SO and its two-joint synergistic A substantial ankle moment was found only if SO was excited
muscles were studied. The muscle bellies of LG and plantaris at positions distant from physiological. These results confirm
Journal of Biomedicine and Biotechnology 5

distally than proximally (Sandercock and Maas, unpublished

observations). Also in line with this hypothesis are the
results of an earlier study in the rat in which lengthening a
muscle distally resulted in substantial force changes exerted
at the distal tendon of a neighboring muscle, while effects of
proximal lengthening were not significant [17].
A major difference between the experiments on epimus-
cular myofascial force transmission in the rat (see above)
and the cat [28] is the number of muscles that is activated
simultaneously. In the rat studies all synergists and some
antagonists were activated versus a single muscle in the
cat. Coactivation leads to several changes within the muscle
compartment that may affect the mechanical interaction
between adjacent muscles. Muscle fibers contract and, hence,
the muscle belly shortens and expands radially. The former
Figure 4: Drawings to illustrate length changes of connective tissue
will result in a small change of the muscle relative position,
linkages between passive (grey) and active (red) synergistic muscles.
Changing the length of one muscle results in reorientation as
whereas the expansion will increase the lateral tension of the
well as unfolding of those linkages. Unfolding is also seen with connective tissue network. In a recent study, we tested the
coactivation. Such straightening of macroscopic crimp in collagen hypothesis that the net effect of coactivation is an increase in
fibrils is correlated to the toe region of the stress-strain curve [35]. the stiffness of the epimuscular pathways (Figure 4), which
Modified from Maas and Sandercock [28]. will facilitate force transmission between muscles. Effects of
antagonist coactivation on mechanical interactions between
synergistic muscles in the rat forelimb were assessed [36]. In
contrast to the hypothesis, changes in force of the restrained
that for in vivo muscle lengths and relative positions force muscle with length changes of its synergist were unaffected
generated in SO muscle fibers is transmitted to its distal by antagonist coactivation. Testing intermuscular interaction
tendon. with other combinations of active muscles (e.g., excluding
The above-described nearly linear force summation the activity of some synergistic muscles) may be necessary to
between MG and LG/SO as well as between rectus femoris elucidate the effects of muscle coactivation on the magnitude
and vastus lateralis is in agreement with this finding. Others of epimuscular myofascial force transmission.
have found that human SO fascicle length was not affected Finally, it is also conceivable that the mechanical charac-
by changes in knee angle, as measured in both passive and teristics of the connective tissue system are different between
maximally active conditions of the ankle plantar flexors muscle groups within an animal and across species. The
[31]. In contrast, recent imaging studies in humans suggest muscle-connective tissue architecture and composition of
that mechanical connections between gastrocnemius and each synergistic group is different. Therefore, generalizing
SO muscles are effective also within the in vivo length the current results to the whole musculoskeletal system
range. Isolated excitation of MG at a fixed angle of the should be done with caution. Although mechanical inter-
ankle and knee joints elicited a decrease in fascicle length, actions between synergistic muscles have been shown in
not only in the excited muscle, but also in SO [32, 33]. many animals (e.g., mouse, rat, cat, locust, frog), differences
However, MG activation did not cause displacements in in connective tissue mechanical properties or differences
flexor hallucis longus muscle [33], suggesting that not all in animal size may affect the importance of such force
muscles are equally connected. In addition, effects of knee transmission. In contrast to mammals, it has been reported
movements on SO muscle have been reported [33, 34]. Note that amphibians have a relatively poorly developed con-
that the mechanical effects (e.g., ankle moment) of such nective tissue network [37] and that insects contain very
displacements in SO were not measured. little connective tissue [38, 39]. Another aspect that should
How can the different results between the rat and be taken into account is the scaling of muscle surface
cat studies be explained? We have hypothesized that the area (to the 2nd power) versus muscle volume (to the 3rd
intermuscular linkages between SO and adjacent muscles power). This means that, for example, mice have a relatively
within the intact cat may be slack or operate on the toe larger epimysial surface to volume ratio than humans. To
region of their lumped stress-strain curve (Figure 4, see date, whether these variations between species lead also to
also [28]). The steep portion of this curve and, hence, different mechanical interactions remains unclear.
epimuscular force transmission will then be attained only The contradictory findings between the rat and cat
with supraphysiological displacements. The stiffness of the studies are not fully understood and, thus, the responsi-
intermuscular linkages may also be a local property, being ble mechanisms requires further investigation. Specifically,
more compliant in the proximal region of the cat ankle future studies should continue to test if the magnitude
extensors. Note that Maas and Sandercock [28] lengthened of intermuscular force transmission is dependent on the
the two-joint muscles by knee movements; thus, there number of muscles that is simultaneously activated. Is the
was more movement proximally. Preliminary data suggest extent of force transmission between muscles the same
indeed that cat SO muscle is more rigidly connected to LG throughout the body? This is another question that needs to
6 Journal of Biomedicine and Biotechnology

be addressed. In conclusion, the importance of epimuscular 10

myofascial pathways for muscle function during normal
movements remains unclear. 8

Total force TA + EHL (N)

6
2.4. Connective Tissue Function in Pathological Muscle-Tendon
Conditions. Besides a potential role for normal muscle func-
tion, epimuscular myofascial pathways may be important 4
in pathological conditions of the musculoskeletal system.
Street observed [41], “After the distal tendon of a frog’s 2
semitendinosus muscle is cut, pathological changes appear first
in the distal part. We found that when part of a muscle was 0
normal the muscle as a whole generally developed the normal
amount of tension and we guessed that some cell component
−2
other than the myofilament arrays served as a tension bypass 0 100 200 300 400 500 600 700
through or around the damaged areas (Ramsey and Street, Time (ms)
unpublished).” In the same paper, Street suggested [41],
(a)
“In injured whole muscle it is probable that the connective
tissue sheath near damaged fibers can pick up and transfer
active tension generated in normal areas and, at the same 2
time, stabilize abnormal areas against length changes. This
might promote healing.” This suggests the hypothesis that the
1.6
connective tissue network may act also as a safety net for
traumatic events in muscle or tendon. In other words, due
Total force EDL (N)

to the presence of myofascial pathways, the acute effects of 1.2

muscle or tendon trauma are limited and muscle function is
preserved.
Injury within a muscle or tendon is a common occur- 0.8
rence, especially during sport activities (e.g., [42, 43]). Thus,
it is essential that basic function is maintained while the
injury is healed. In the same study by Maas and Sandercock 0.4
[28] that showed little epimuscular force transmission in
intact SO, they also showed that during complete tendon
0
transection the SO can produce substantial force. The 0 100 200 300 400 500 600 700
insertion of the SO on the calcaneus was completely severed, Time (ms)
yet the SO produced an extensor moment at the ankle that
was about 45% of normal. There was greater shortening, Distal
17 mm compared to 1 mm, than before tendon transection. Proximal
Yet function was partially maintained possibly allowing use (b)
during recovery.
The results of several previous studies support the idea Figure 5: Waveforms of simultaneously measured force exerted
that connective tissues within and surrounding muscles at the distal tendon of TA + EHL (a) and forces exerted at the
can limit injury and support repair. It has been reported tendons of EDL muscle (b). During isometric contraction, the
connection between TA + EHL and the force transducer was severed
that one of the four distal tendons of rat EDL (a mul-
(t ∼ 200 ms). TA + EHL force dropped to zero and at the same time
titendoned muscle, see [44]) can be cut or considerably proximal EDL force decreased and distal EDL force increased. These
shortened with minimal effects on force measured at the results have been presented in abstract form [40].
proximal tendon [45, 46]. This can only be explained by
transmission of force from the tenotomized muscle fibers
to the intact distal tendons via the endomysial-perimysial
network. Similar phenomena have been reported following
transection of the whole distal or proximal tendon. During suddenly. Proximal TA + EHL force was not measured, but
some of the above-described rat experiments, the connec- the changes in proximal and distal EDL forces clearly indicate
tion between tendon and force transducer was suddenly mechanical interactions between these synergistic muscles
severed. Following such a release of the proximal EDL (Figure 5).
tendon, a substantial force was still found at the distal In addition to the acute backup from connective tissues
tendon [47]. The muscle fibers of EDL are thus prevented following muscle and tendon trauma, long-term adaptations
from shortening all the way, most likely by inter- and/or also suggest that myofascial pathways serve temporarily
extramuscular connective tissues. In a different experiment, as a safety net. It has been reported that the integrin-
the connection of the TA + EHL tendon was released vinculin mediated connections between the subsarcolemmal
Journal of Biomedicine and Biotechnology 7

cytoskeleton and extracellular matrix are temporarily rein- Acknowledgments

forced in ruptured muscle fibers [48, 49]. As a consequence,
force generated within the sarcomeres of these damaged The authors thank professor Peter Huijing and Guus Baan
fibers will be transmitted via the endomysium. This will who coauthored the manuscripts that part of this work
reduce the load on the injured site allowing repair with less was based on. Huub Maas is currently supported by Marie
chance of rerupture. In the case that not the muscle fibers but Curie International Reintegration Grant no. MIRG-CT-
the tendon is fully or partially torn, connective tissue linkages 2007-203846 within the 7th European Community Frame-
with adjacent structures may in a similar fashion prevent work Programme. T. G. Sandercock is currently supported
further trauma and facilitate the recovery process. Such by NIH NS034382 and NS061208.
adhesions have been reported in chronically tenotomized
muscle in the rat, cat, and rabbit [50–52], which ultimately
results in reattachment of the tendon. Nonsurgical treatment References
(e.g., immobilization at low length) is also frequently applied
following tendon ruptures in humans (e.g., [53]). Preserving [1] J. A. Trotter, A. Samora, and C. Wofsy, “A morphometric
and restoring function after injury clearly is important in analysis of the muscle-tendon junction,” Anatomical Record,
wild animals and will be selected for. In contrast to humans, vol. 213, no. 1, pp. 26–32, 1985.
where the damage can be treated in a hospital, most animals [2] J. L. McKay, T. J. Burkholder, and L. H. Ting, “Biomechanical
must maintain some degree of function while the muscle- capabilities influence postural control strategies in the cat
tendon injury heals. hindlimb,” Journal of Biomechanics, vol. 40, no. 10, pp. 2254–
2260, 2007.
Epimuscular myofascial transmission may also be impor-
tant during reconstructive surgery. Several surgical interven- [3] S. H. Yeo, M. C. Tresch, and D. K. Pai, “Optimal design of
musculoskeletal models using force field data,” in Proceedings
tions include manipulation of tendon, muscle, and/or the
of the 30th Annual International Conference of the IEEE
surrounding connective tissues (e.g., fasciotomy in compart- Engineering in Medicine and Biology Society (EMBS ’08), pp.
ment syndrome, tendon transfer in cerebral palsy). In tendon 3710–3714, Vancouver, Canada, August 2008.
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