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Advances in Neuromuscular Physiology of Motor Skills and Muscle Fatigue, 2009: 285-302
ISBN: 978-81-308-0365-4 Editor: Minoru Shinohara

14. Mechanical interactions between

skeletal muscles
Huub Maas1,2
1
Research Institute MOVE, Faculty of Human Movement Sciences, VU University
Van der Boechorststraat 9, 1081 BT Amsterdam, The Netherlands; 2Department of
Physiology, Feinberg School of Medicine, Northwestern University, 303 E.
Chicago Avenue, Chicago, IL 60611, USA

1. Abstract. Force transmission from skeletal muscles to bone is a

key element in the control of limb movements. Several in situ studies
have now shown that connective tissues linking adjacent muscles to
each other and to other surrounding structures can bear substantial
forces. However, there is little data available to indicate if such
epimuscular myofascial pathways are important during normal in
vivo movements. Therefore, it remains unclear if the actuators
commanded by the central nervous system within an intact body are
mechanically inter- or independent. This chapter will review some
earlier and the most recent experiments on mechanical interactions
between muscles in physiological and pathological muscle
conditions. In addition, the potential role of epimuscular myofascial
force transmission (MFT) in neuromuscular control will be addressed.

2. Introduction
Synergistic muscles as well as muscles crossing different joints are
functionally connected to each other through rapid spinal reflex pathways [1-3].

Correspondence/Reprint request: Dr. Huub Maas, Research Institute MOVE, Faculty of Human Movement
Sciences, VU University, Van der Boechorststraat 9, 1081 BT Amsterdam, The Netherlands
E-mail: h.maas@fbw.vu.nl
286 Huub Maas

Spinal reflexes are important for the regulation of joint and limb mechanics [4].
For an overview of excitatory and inhibitory intermuscular connections see
Nichols [1]. Such spinal circuitry is among others responsible for stretch-
evoked reflexes between soleus (SO) and lateral gastrocnemius (LG) muscles
[5]. In understanding the neural control of limb movements it is as important
to know if the actuators commanded by the central nervous system are
independent functional units or are mechanically connected. The extent of
intermuscular interdependence determines the 3D mechanical action at the
joints when the muscle is recruited, but also the nature of proprioceptive
feedback.
The most recognized pathway of force transmission from muscle fibers
to bone is via the specialized myotendinous junction and tendon, named
myotendinous force transmission. Classical anatomy has defined each muscle
as a separate entity with a unique function at the joint(s) it spans. Therefore,
it is common to view muscles as mechanically independent actuators. This is
readily apparent from biomechanical models of the musculoskeletal system in
which muscles are connected to the skeleton exclusively at their origin and
insertion. Although implicitly, several references to mechanical connections
between muscles have been made in the past century. For example, Denny-
Brown [6] stated that when force records of cat SO are made through
stimulation of the LG-SO nerve branch ‘…it is found to be extremely difficult
to avoid a slight early rise of tension, and fall in the plateau, due to the
vibration or pull of gastrocnemius.’ For the same muscles, Nichols [7] noted
‘Mechanical artifacts due to direct mechanical action of the stretched muscle
on those isometrically constrained were indicated by essentially
instantaneous latencies or by effects observed after pharmacological block of
heterogenic reflexes.’
Such intermuscular interactions occur either at the tendon or the muscle
belly. Muscles can be connected to each other via a common tendon. Within a
muscle, such a common elasticity can explain the non-linear summation of
motor unit forces [8]. Note that in the above examples the tendons are severed
from their insertion site and individually connected to force transducers. This
means that force was transmitted across the muscle boundary (i.e., the
epimysium) at the shared muscle belly interface. Unequivocal evidence for
such force transmission between a muscle belly and its immediate surrounding
structures, named epimuscular MFT [9], was shown only recently [10, 11].
Influential for these and other studies on muscular force transmission
were the elegant studies of Street [12, 13] in which the first direct evidence
for force transmission from muscle fibers to the connective tissue framework
was reported. Street referred to this phenomenon as lateral transmission of
tension, which explains the usage of both ‘lateral’ and ‘myofascial’ in the
Mechanical interactions between skeletal muscles 287

literature. As for force transmission within a whole limb lateral may be

confused with the anatomical medial-lateral direction, myofascial is
considered as a more appropriate term and will be used here. MFT within
muscle has been reviewed recently by several authors [14-17].
In this chapter, the initial series of systematic experiments on mechanical
interactions between synergistic muscles via myofascial pathways as well as
the most recent contributions to this topic will be reviewed. In addition, the
importance of epimuscular myofascial pathways in physiological muscle
conditions, for neuromuscular control as well as in muscle-tendon injury will
be addressed. For other aspects of epimuscular MFT (e.g., mechanical
interactions between antagonistic muscles, MFT in spastic paresis) the reader
is referred to recent reviews [9, 18, 19].

3. Intermuscular interaction through connective tissue structures

3.1. Epimuscular myofascial force transmission
Epimuscular MFT is thus defined as force transmission from a muscle to
its surroundings via pathways other than the muscular origin and insertion. The
most direct proof of such force transmission is a difference in force exerted at
the proximal and distal tendons of a muscle. Two epimuscular pathways are
distinguished (Fig. 1). If force is transmitted between two neighboring muscles
via the continuous connective tissue at their muscle belly interface, it is
classified as intermuscular MFT. If force is transmitted between the
intramuscular connective tissue network of a muscle and adjacent non-
muscular structures, it is classified as extramuscular MFT. Recent work [20]
has shown that mechanical interactions between adjacent muscles are mediated
by both intermuscular as well as extramuscular myofascial pathways (see
below). In theory, force could also be transmitted from one muscle to the other
through frictional forces between the muscle belly surfaces without the
presence of connecting structures, but there is no empirical evidence for such a
mechanism.

F-myofascial
F-origin F-insertion
Neighboring muscles (intermuscular)
Non-muscular structures (extramuscular)

Figure 1. The different pathways via which force generated within muscle fibers can
leave the muscle to be transmitted to the skeleton (see text for explanation).
288 Huub Maas

The connective tissue layer between the epimysia of adjacent muscles

[for images see 21] is often characterized as ‘loose’. Analogous to previous,
but now disputed [e.g., 14] claims that the perimysium acts as a membrane
that allows muscle fascicles to slide past each other [22], it has also been
suggested that the epimysium decreases the friction between muscles as well
as between muscles and intermuscular nerves [23]. To date, physiology texts
still indicate that ‘the epimysium protects muscles from friction against other
muscles and bones’ (e.g., the online sources Wikipedia and Teach PE).
Although intermuscular connective tissue can be easily broken by blunt
dissection, it appears to be stiff and strong enough to transmit force if loaded
under physiological conditions (i.e., by shearing). Several structures provide
an anatomical substrate for the extramuscular myofascial pathway. (i) The
neurovascular tract, which is reinforced with a thick layer of connective
tissue to protect the nerves and blood vessels [Fig. 2, see also 11, 21]. Note
that the neurovascular tract is continuous with the extensive intramuscular
connective tissue network, which further supports the nerves innervating
muscle fibers and the blood vessels entering the muscle. (ii) Fascia layers
forming the borders of synergistic muscle groups that are continuous with
more superficial layers (e.g., subcutaneous connective tissue) as well as
connective tissue around tendons [for images the reader is referred to
previous publications, e.g. 24-27].

Figure 2. Cross-section of neurovascular tract between tibialis anterior (TA), extensor

hallucis longus and extensor digitorum longus (EDL) muscles in the rat. Arteries (A),
veins (V) and nerves (N) are embedded in a thick layer of connective tissue (stained
with Sirius Red, dark). Note also the extensive intramuscular connective networks of
TA and EDL. Enlarged detail of Fig. 7 in Maas et al. [11].
Mechanical interactions between skeletal muscles 289

3.2. Intermuscular mechanical interactions

Up until recently, the only indications of mechanical interactions between
muscles were some anecdotal references (see above) and preliminary results
from explorative experiments [28]. This lead to a series of in situ experiments
in which force transmission from extensor digitorum longus (EDL), extensor
hallucis longus (EHL) and tibialis anterior (TA) muscles, all embedded within
the anterior crural compartment in the rat, was investigated. Isometric forces
were measured simultaneously at the proximal and distal tendons of EDL
muscle as well as at the tied distal tendons of TA and EHL muscles (Fig. 3).
These tendons can all be dissected with minimal disruption of the
compartment, leaving epimuscular myofascial pathways mostly intact.
Several experimental conditions resulted in mechanical interactions
between EDL and TA+EHL. It was found that changing the muscle-tendon
unit (MTU) length of TA+EHL did not result only in force changes exerted at
the distal TA+EHL tendons, but also altered forces exerted at the proximal
and distal tendons of EDL [11]. More specifically, lengthening TA+EHL
distally increased proximal EDL force (by 37%), but decreased distal EDL
force (by 39%). Such interactions between synergistic muscles can be
ascribed to changes in the position of TA+EHL relative to EDL muscle [29]
and, consequently, changes in the configuration (length and angle) of inter-
and extramuscular connective tissues (Fig. 4A). It may appear obvious to
explain these results by intermuscular MFT. However, EDL, TA and EHL
are also linked to each other through shared extramuscular connective tissues

To force transducer
TA+EHL distal

TA + EHL

.
To force transducer To force transducer
EDL distal EDL proximal

EDL

lmtu EDL

Figure 3. Schematic view of the experimental set-up used to investigate intermuscular

interaction through myofascial force transmission. For explanation see text. The distal
tendons of the TA+EHL complex were connected to a force transducer via a low
friction pulley (~). lmtu: muscle-tendon unit length. Modified from Maas et al. [11].
290 Huub Maas

(not visible in Fig. 4). A clear example is the neurovascular tract (Fig. 2) that
runs in between the muscles while giving off branches of nerves and blood
vessels which enter the intramuscular space also reinforced with a layer of
connective tissue [11, 21]. Therefore, a follow-up study was performed to
investigate the contribution of each pathway to inter-synergist mechanical
interactions [20]. The same experimental conditions were repeated before and
after disruption of the connective tissue layer between EDL and TA+EHL.
The previously found effects of TA+EHL length on proximal and distal EDL
forces were confirmed. Eliminating force transmission via intermuscular
myofascial pathways decreased the interaction between TA+EHL and force
exerted at the distal tendon of EDL. However, the interaction between
TA+EHL and distal EDL force was not changed. In conclusion, mechanical
interactions between synergists originate from both inter- and extramuscular
connective tissues. The relative contribution of each pathway is likely
dependent on the length of each muscle and their relative position.
To distinguish between length and relative position, isolated effects of
muscle relative position were studied [30]. The position of EDL muscle was
altered, while the MTU length of EDL and TA+EHL was kept constant.
Changing the relative position of EDL in distal direction decreased force
exerted at the distal tendons of TA+EHL (illustrated schematically in Fig.
4B). Simultaneously, proximal EDL force decreased and distal EDL force
increased, changing the magnitude and sign of net epimuscular MFT. Force
changes in opposite direction were found if EDL muscle was repositioned
more proximally (Fig. 4C). Effects of disrupting intermuscular connective
tissues have not been studied yet for these experimental conditions.
From these and other experiments on epimuscular MFT [reviewed in 18]
a general picture regarding intermuscular interactions has emerged. The
muscle end that is positioned farthest in a particular direction (e.g., distal)
will draw force from neighboring muscles. Thus, force previously transmitted
to the tendon of muscle can change its pathway to be transmitted to the
skeleton via the tendon of its neighbor. This pattern also seems to hold for
mechanical interactions between antagonistic muscles [e.g., 9].

3.3. Are muscles independent actuators in vivo?

From the above, it is clear that inter- and extramuscular connective
tissues are capable of transmitting force between adjacent muscles. However,
several aspects of the experimental muscle conditions were different from
those in vivo. It should be kept in mind that the main purpose of those studies
was to investigate the presence and capacity of mechanical connections
between muscles. The muscles of the anterior crural compartment were
Mechanical interactions between skeletal muscles 291

excited maximally. However, muscles generally function at submaximal

levels of activation during in vivo movements [e.g., 31]. It was recently found
that inter- and extramuscular MFT is also present when muscles are
stimulated at submaximal frequencies (10-30 Hz) [32], but this is only of
substantial magnitude (up to 30% of maximal force) if a single muscle of a
synergistic group is lengthened [33]. However, length changes of a single
muscle are hardly found during normal movements. Due to differences in
moment arms, the change in MTU length of one muscle can be different from
its neighbor [e.g., 34, 35], but the relative movements imposed in the above
described studies were clearly beyond the physiological range.
In a pilot experiment, ankle joint movements in the rat were simulated by
changing the length of EDL and TA+EHL simultaneously. As the moment
arm of TA is higher than the moment arm of EDL [36], 20% higher length
changes were imposed on the TA. Distal EDL force was found to be higher
than proximal EDL force at all lengths tested (Fig. 5). Lengthening all three

F↑ F↓ F↑ F↓

F↓ F↑

A B

proximal distal

D C

F↓ F↑

F↑ F↓

Figure 4. Schematic drawings to illustrate changes in the configuration of inter- and

extramuscular connective tissues. The muscles are connected to each other as well as
to non-muscular structures in the direct environment (represented as a rectangle). (A)
Effects of lengthening one muscle of a synergistic group. Effects of moving a muscle,
kept at a constant MTU length, in distal (B) and proximal (C) direction. (D) Effects of
lengthening two synergists to different extents. Not visible in these 2D drawings are
the connections between adjacent muscles via extramuscular connective tissues.
Modified from Maas et al. [30].
292 Huub Maas

muscles of the anterior crural compartment, simulating ankle plantar-flexion,

slightly increased the EDL force difference (by 0.05 N). Note that the
position of TA+EHL was changed relative to EDL in distal direction.
According to the above described general pattern of intermuscular
interactions (see section 3.2.), TA+EHL will attract force from EDL muscle
decreasing distal EDL force. However, the position of EDL muscle relative to
non-muscular fixed structures is also altered with MTU lengthening favoring
force transmission to its distal tendon (Fig. 4D). This is confirmed by the
observed passive force exerted distally, while proximal passive force
remained zero. These results indicate that inter- and extramuscular
connections can be arranged in such a way that they exert forces on a muscle
in opposite direction [see also Fig. 8 in 11]. Effects of simultaneous
lengthening of synergists on proximo-distal force differences were studied
systematically by Meijer et al. [27]. It was found that net epimuscular MFT
from EDL decreased with added lengthening of TA+EHL compared to distal
lengthening of only EDL muscle. With the muscles in passive state the
highest force was measured at the distal tendon, while more force was
exerted at the proximal tendon during a tetanic contraction. This lead to the
same conclusion that different myofascial pathways acting on the muscle in
opposite directions contribute to the proximo-distal force difference.
Although closer to the real case, all these studies used protocols that
required severing the tendons from their origin and/or insertion. This means
that muscle length was varied by moving the force transducer as opposed
to changes in joint angle. Also, MTU length of the antagonistic muscles was

2.1 0.02 0.16

Distal
Fdistal - Fproximal (N)
EDL passive force (N)
EDL active force (N)

Proximal
2.0
0.12
1.9

1.8 0.01 0.08

1.7
0.04
1.6

1.5 0 0.00
40 60 80 100 120 140 160 40 60 80 100 120 140 160

Simulated Ankle Angle (deg.) Simulated Ankle Angle (deg.)

Figure 5. Forces exerted at the proximal and distal tendons of EDL muscle (left
panel) as well as the difference in active force between the two locations (proximal
subtracted from distal, right panel). The different ankle angles were simulated by
changing the MTU length of EDL and TA+EHL simultaneously, but with different
magnitudes to account for differences in moment arm. Data from a single experiment
are shown. Unpublished observations (Maas and Huijing).
Mechanical interactions between skeletal muscles 293

generally kept constant. Therefore, a new experimental approach was

designed to investigate effects of epimuscular MFT for physiological lengths
and relative muscle positions [37]. This was assured by testing the muscles in
a nearly intact limb; the tendons were not cut, but left attached to their
insertion sites and length changes were obtained by movements of the joints.
Specifically, mechanical interactions between SO and the synergistic muscles
(LG and plantaris, PL) were studied in the cat. Ankle moment exerted upon
excitation of SO was measured at various knee angles (70-140°), while the
ankle was kept at a constant position, using a 6 degree-of-freedom load cell
coupled to a 6 degree-of-freedom robotic manipulator (Fig. 6). As SO is a
one-joint ankle extensor, knee movements will only alter the length and
relative position of its two-joint synergists. It was hypothesized that force
transmission from SO muscle fibers will be affected by length changes of its
synergists through configuration changes of connective tissues between these
muscles (see dark grey area in between muscles in Fig. 6).
Despite a substantial change in length of LG and PL (4.5-7.2 mm), active
plantar flexor moment generated by SO was not significantly affected by
changes in knee angle. These results suggest that the intact SO muscle acts
mechanically as an independent actuator. To further test this conclusion an
additional set of experiments was performed. With minimal disruption of the
connective tissues at the muscle belly level, the distal tendon of SO was
dissected free from the other tendons in the Achilles complex, cut and
connected to a force transducer. As this eliminated force transmission to its
insertion on the calcaneus, any ankle joint moment following SO excitation
was attributed to force transmission via epimuscular myofascial pathways to
the Achilles tendon. If the tendon of SO was placed at its original position,
corresponding to the above reported ankle joint angle, SO ankle moment was
close to zero while force exerted at the distal tendon was near its optimal
value. A substantial ankle moment of SO was found only if the muscle was
excited at positions distant from physiological (see below). These results
confirm that for in vivo muscle lengths and relative positions force generated
in SO muscle fibers is transmitted to its distal tendon.
A similar conclusion has been drawn for connectivity between medial
gastrocnemius (MG) and the LG-SO complex as well as between rectus
femoris and vastus lateralis muscles [38, 39]. For both muscle combinations
nonlinear force summation, defined as the difference between the force
exerted when both muscles are excited simultaneously and the sum of the
forces exerted when each muscle (complex) is excited individually [8], was
assessed by measuring forces and moments in the x, y and z directions.
During the tetanic phase of an isometric contraction, summation was nearly
linear (< 3%) in all 6 degrees of freedom. It should be noted that SO force
294 Huub Maas

Figure 6. A schematic presentation of the cat hindlimb in the experimental set-up

used to investigate inter-synergist interactions [37]. The effects of SO muscle force
were measured for different positions of the knee joint while the ankle was kept at a
constant position. Shearing of the interface between SO and LG-PL due to changes in
muscle relative position is indicated with a dark grey plane. The results of this study
(see text) indicate that such shearing due to changes in muscle relative position does
not necessarily imply force transmission.

transmission as well as non-linear summation were not tested for all possible
joint angle configurations. It is also reasonable to assume that not all
synergistic muscle groups within the musculoskeletal system are equally
connected. Therefore, generalizing these results to the whole musculoskeletal
system should be done with caution. It is suggested to repeat the experiments
as presented by Maas and Sandercock [37] with other combinations of
hindlimb and forelimb muscles. This should also include testing the effects of
co-activation of synergistic as well as antagonistic muscles.

3.4. Force transmission between muscles across joints

The standard atlas of cat anatomy [40] indicates that the biceps femoris
(BF) and semitendinosus (ST) muscles in the cat extend the hip and flex the
knee. The insertion of the BF is described as a fascia connected to the patella
and the tibia. The distal tendon of the ST inserts also into the tibia. More
detailed studies on the anatomy of these muscles revealed that ST and BF
Mechanical interactions between skeletal muscles 295

have extensive connections to the crural fascia [41-43]. The crural fascia is a
connective tissue sheet that covers the posterior aspect of the leg. This fascia
is attached distally to the calcaneus through thick tendinous bands on the
medial and lateral side [44, 45], suggesting a mechanical action of BF and ST
at the ankle.
In a preliminary report, a plantar-flexion moment was found at the ankle
upon simultaneous excitation of BF and ST muscles [46]. Ankle moment was
substantial (i.e., up to three times higher than that generated by SO) and
varied with ankle angle. This was studied in more detail by Carrasco and
English [47]. By stimulating the nerve branches that divide BF in different
compartments [42], it was found that, in addition to moments at hip and knee
joints, the posterior and middle compartment can exert a moment at the ankle
joint. Surprisingly, cutting the connection of the crural fascia with the
calcaneus did not fully eliminate the BF ankle moment. On the condition that
the limb segments were rigidly fixed, this means that BF force is transmitted
to the calcaneus via different pathways: (i) via the crural fascia and (ii) via
the superficial ankle extensors (LG and MG) and the Achilles tendon. The
latter can be qualified as a myofascial pathway. These results indicate
mechanical interactions between muscles across joints.
Recently, the role of force transmission through the crural fascia for
intra-limb coordination during walking has been studied [45, 48]. In the
premammilary cat, joint kinematics was assessed following disruption of
the distal part of the crural fascia. This resulted in more flexion in the ankle
joint in the stance phase, which confirms the mechanical action of the
crural fascia at the ankle during locomotion. In addition, knee and hip
flexion were also increased. Disrupting the crural fascia distally may have
resulted in a redirection of BF-ST forces to the more proximal insertions on
the tibia, causing more knee flexion. However, the effects at the hip joint
need a different explanation. Previous studies have shown that fasciotomy
decreases the maximal force of the muscles that are enveloped by the
specific fascia [21, 24]. In a similar way, disrupting the crural fascia could
have diminished the force potential of the hip extending BF and ST. It is
clear that the crural fascia in the cat plays an important role for the control
of limb movements.
Across joint force transmission between muscles can also be mediated by
connective tissue supporting the nerves and blood vessels running through
the leg. In human cadavers, it has been observed that hip flexion can cause an
increase in strain and relative movement of the tibial nerve at the knee and
ankle [49]. As strong linkages exist between the neurovascular tract (Fig. 2)
and surrounding muscles, this may also be a pathway for intermuscular
mechanical interactions across joints.
296 Huub Maas

3.5. Inter- and extramuscular connective tissues as safety net

Besides a potential role for normal muscle function, inter- and
extramuscular connective tissues may also be important in pathological
conditions of the musculoskeletal system. Street [12] noted: ‘After the distal
tendon of a frog’s semitendinosus muscle is cut, pathological changes appear
first in the distal part. We found that when part of a muscle was normal the
muscle as a whole generally developed the normal amount of tension and we
guessed that some cell component other than the myofilament arrays served
as a tension bypass through or around the damaged areas (Ramsey and
Street, unpublished).’ As described in section 3.3, force transmission from
SO muscle was also tested with its distal tendon connected to a force
transducer [37]. When during a contraction the connection between tendon
and force transducer was suddenly severed, SO force is redistributed via
epimuscular myofascial pathways to the Achilles tendon (Fig. 7). Using the
words of Street [12], the inter- and extramuscular connective tissues ‘served
as a tension bypass’. In the same paper Street also stated: ’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 time, stabilize abnormal areas against length changes. This might
promote healing.’ Based on these earlier observations by Street and the
results from Maas and Sandercock, a new hypothesis was recently formulated
[37]: inter- and extramuscular connective tissues act as a safety net for
traumatic events in muscle or tendon.
Tendon transection is a common element in reconstructive surgery (e.g.,
tendon transfer) or may result from trauma. Tenotomy has also been used
frequently as a model to study the effects of use and disuse on muscle
properties [e.g., 50, 51, 52]. Immediately following this surgical procedure,
force transmission to the muscle’s insertion via the myotendinous junction
and tendon is eliminated. Therefore, this experimental model is also very
suitable to study MFT.
In a previous study, force transmission within a fully dissected EDL
muscle was investigated in the rat [53]. EDL is a multi-tendoned muscle,
which has a single proximal origin from which emerge four muscle heads
each with a separate distal aponeurosis and tendon [54, 55]. It was found that
one of the four distal tendons could be cut with minimal effects on force
measured at the proximal tendon. Only after transection of three distal
tendons a significant decrease in proximal force was measured. Even then,
optimal force decreased by 16% while the direct myotendinous pathway was
eliminated for 55% of the muscle physiological cross-sectional area. This can
only be explained by force transmission from tenotomized muscle fibers via
Mechanical interactions between skeletal muscles 297

the endomysial-perimysial network (i.e., intramuscular MFT). More recently,

it was also shown for both isometric and dynamic muscle conditions that
substantial length changes of a single EDL head cause only minor effects on
force exerted at the proximal tendon [54, 56]. Thus, due to the presence of
myofascial pathways, the acute effects of tendon trauma or length
perturbations are limited and muscle function is preserved.
Similar phenomena have been reported following transection of the whole
distal or proximal tendon. During experiments in the rat using a similar set-up
as described in Fig. 3, the connection between tendon and force transducer was
suddenly severed. Following such a release of the proximal tendon of EDL, a
substantial force was still found at the distal tendon [28]. The muscle fibers of
EDL are thus prevented from shortening all the way, most likely by inter-
and/or extramuscular connective tissues. Effects of epimuscular MFT were also
observed with transection of the distal tendon of SO in the cat [37]. The
experimental conditions of this study have been described in section 3.3.
Despite the fact that myotendinous force transmission via the distal tendon of
SO was removed, excitation of SO still resulted in a substantial ankle moment
(45% of the intact condition). These results confirm the presence of strong
linkages via which force can be transmitted between SO muscle fibers and the
Achilles tendon. However, even with SO at this non-physiological muscle
position the stiffness of the lumped myofascial connections was lower (2.8
N/mm) than the stiffness of the myotendinous pathway [~10-25 N/mm, 57].
Note that in the intact animal the pathway with the stiffest properties will
transmit the greatest fraction of muscle fiber force.
In a recent paper, the residual ankle moment during stimulation of the
common peroneal nerve immediately after distal tenotomy of EDL was fully
attributed to force generated by the intact TA muscle [58]. Similar to the SO
tenotomy experiment, it is likely that EDL muscle fibers were still exerting
force and also contributed to the measured moment about the ankle.
In addition to the acute backup from connective tissues following muscle
and tendon trauma, long-term adaptations also suggest that myofascial
pathways serve (temporary) as safety net. It has been reported that the
integrin-vinculin mediated connections between the subsarcolemmal
cytoskeleton and extracellular matrix (a myofascial pathway between
sarcomeres and endomysium) are temporarily reinforced in ruptured muscle
fibers [59, 60]. This likely reduced to load on the injured site allowing repair
with a reduced chance of re-rupture. If not the fibers but the tendon is fully or
partially torn, adhering to adjacent structures may prevent further trauma and
facilitate the recovery process. Such adhesions have been reported in
chronically tenotomized muscle in the rat, cat and rabbit [51, 52, 61],
which ultimately results in reattachment of the tendon. Non-surgical treatment
298 Huub Maas

0.12 Ankle Moment 30

Tendon Force
0.10 25

Ankle Moment (Nm)

Tendon Force (N)

0.08 20

0.06 15

0.04 10
0.02 5

0.00 0

-0.02 -5
0 500 1000 1500 2000 2500
Time (ms)

Figure 7. Simultaneously measured ankle moment and force exerted at the distal
tendon of SO in the cat. During SO muscle contraction, the connection between
tendon and force transducer was suddenly severed (t ∼ 860 ms). Note that the ankle
moment was very small (~0.01 Nm) when the connection was still intact. Unpublished
observations (Maas and Sandercock).

(e.g., immobilization at low length) is also frequently applied following tendon

ruptures in humans [e.g., 62]. In contrast to humans, wild animals cannot be
treated in a hospital and such a natural mechanism could, thus, be life-saving.

3.6. Proprioception of myofascial force transmission

One of the features of muscles subject to epimuscular myofascial loads is
a difference between force exerted at the origin and force exerted at the
insertion. To use this for the control of posture and movement, it is required
that the neural circuitry can sense such regional force differences. The
sensory receptors in muscles that signal contractile force are Golgi tendon
organs (GTOs), which are located at the junction between muscle fibers and
tendinous tissue [63]. It should be noted that GTOs have been found at both
proximal and distal aponeuroses [64, 65]. Thus in theory, these subgroups of
GTOs can provide information regarding origin-insertion force differences.
Moreover, GTOs at an aponeurosis that is shared by muscle fibers of two
adjacent muscles may signal mechanical interactions [66]. It has been shown
that Ib-afferents of GTOs respond predominantly to contractions of muscle
fibers that are in the same muscle region [67]. Subsequent studies are
required to determine if this so called sensory partitioning is also present
between proximal and distal regions.
How could such region specific force feedback be used by the spinal
circuitry? Two-joint muscles may be particularly suited to play a potential
Mechanical interactions between skeletal muscles 299

role here as such a mechanism could yield joint specific feedback. It is

known that there exist inhibitory spinal pathways between triceps surae and
quadriceps muscles [1, 68]. According to the above, the strongest Ib
projections to the quadriceps may originate from the proximal GTOs of the
two-joint gastrocnemius (i.e., the synaptic potential generated in quadriceps
motoneurons by impulses from gastrocnemius), while the strongest Ib
projections to the triceps surae may originate from the GTOs at the distal
aponeurosis of gastrocnemius. It has been reported that for most of the stance
phase during cat walking MG force exerted at the distal tendon is highly
correlated with ankle plantar-flexion moment [69]. In contrast, MG force was
correlated with knee flexion moment only in the first 30% of stance. Thus in
late stance, MG satisfies the mechanical demands of only the ankle joint.
Such a single-joint function of a two-joint muscle may require sensory
partitioning between origin and insertion. It is clear that this hypothesis
warrants further investigation.

4. Concluding remarks
In the last decade, several experiments on muscular force transmission
have unequivocally proven that inter- and extramuscular connective tissues
are capable of transmitting force between adjacent muscles. More recent
efforts have resulted in new insights regarding effects of epimuscular MFT in
more physiologically relevant muscle conditions (e.g., in vivo relative muscle
movements). Future studies should investigate force transmission during
muscle activation patterns that resemble those of normal movements. In
particular, changes in muscle independence with co-activation of synergistic
as well as antagonistic muscles need to be addressed. In addition, the
potential consequences of mechanical interactions between adjacent muscles
for neuromuscular control should be elucidated.
While the significance of epimuscular MFT for normal muscle function
in vivo remains unclear, potential functions for pathological muscle-tendon
conditions (e.g., tendon rupture) have emerged. Several surgical interventions
include manipulation of muscle and/or the surrounding connective tissues
(e.g., fasciotomy in compartment syndrome, tendon transposition in cerebral
palsy). Therefore, knowledge of the acute, as well as long-term, effects of
disrupting connective tissues has important implications for surgical practice.

5. Acknowledgements
I would like to thank my wife Geke for her courage to join me to the
USA. This chapter would not have existed without her perseverance and
300 Huub Maas

continuous support. The author further wishes to thank Prof. Peter Huijing,
Guus Baan and Dr. Thomas Sandercock who coauthored the manuscripts that
part of this work was based on.
The research reviewed in this chapter was partly supported by the
National Institute of Arthritis and Musculoskeletal and Skin Diseases Grant
AR-041531 (Sandercock) as well as by the NIDRR Advanced Rehabilitation
Research Training Grant H133P040007 (Rymer, Zhang).

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