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PII: SOO21-9290(96)00171-6



Tetsuo Fukunaga, Yasuo Kawakami, Shinya Kuno, Kazuo Funato and Senshi Fukashiro
Department of Life Sciences. University of Tokyo, 3-8-1, Komaba, Meguro, Tokyo. Japan

Abstract-The present study focused on architectural factors which are considered to influence the linkage of
muscle fiber and joint actions. By means of real-time ultrasonography we can observe clearly and noninvasively
in oiao the movement of fascicle and aponeurosis in human muscle and measure directly the changes in pennation
angle and length of fascicle during muscle contraction. During dorsi and plantar flexion without load the
movement of tendinous tissue in human tibialis anterior muscle (TA) appeared to synchronize with the displace-
ment of the ankle joint, indicating that the muscle-tendon complexes are stiff relative to the applied force. which is
fairly small in the case of foot shaking motion. On the other hand, when the ankle joint was fixed and the TA
contracted ‘statically’ the ultrasonic echo from deep aponeurosis in the TA was observed to move proximally,
indicating the elastic component (i.e. mainly tendinous tissue) was stretched significantly by the contraction force
of muscle. In the case of the knee joint, a length of fascicle in vastus lateralis decreased by 18% with the extension of
the knee passively from a 100’~ flexed position. When the knee extensors contracted ‘statically’ the fascicle length
decreased at every joint angles and its magnitude was greater (30%) when the knee was closer to full extension than
(5%) at the flexed positions. The present results clearly show that the architecture of actively contracting muscle
tibers differ considerably than that which occurs when movement is passively induced. The use of cadaver data in
the study of architecture and modeling of muscle functions would result in inaccurate, and in some cases even
erroneous results. (1) 1997 Elsevier Science Ltd. All rights reserved.
Kr! I\YI&S: Ultrasonography: Architecture; Muscle fibre; Tendon.

INTRODUCTION 1993, 1994, 1995; Fukunaga et al., 1992, 1996; Narici
et al., 1992; Rugg et al., 1990). In this article, the behavior
Muscle contraction generates movements of the tendon, of the muscle-tendon complex in humans revealed by
which produce joint motions. Because behavior of these techniques is reviewed, the changes in the penna-
a muscle during contraction in humans cannot be di- tion angle and the fascicle length during muscle contrac-
rectly observed, in vivo functions of human muscles have tion are especially formulated.
been evaluated from joint actions. In fact, however,
joint actions not only reflect the intrinsic character-
istics of muscle fibers but are affected by anatomical VISUALIZATION OF TENDINOUS MOVEMENT
factors within a muscle, and within a joint system DURING JOINT ACTION
(Bobbert et ul., 1990; Powell et al., 1984; Roy and Edger-
ton, 1992; Trotter, 1993; Wickiewicz et al., 1983). The A previous paper (Fellows and Rack, 1987) has shown
force-velocity relationship of human elbow flexor some possibilities of the estimation of the movement of
muscles has been reported to be similar to that of muscle contracting muscle in human elbow flexors using X-ray
fibers (Wilkie, 1950), but the similarity is controversial if photography or needles inserted into the muscles,
one considers the multiple factors lying between muscle indicating the biceps muscle shorten or is lengthened in
fibers and a joint: from observations at the joint, one a phase corresponding to the flexion and extension of
cannot get information on how much muscle shortening elbow joint. Some more recent papers (Henriksson-
or lengthening occurs during joint actions. Especially, in Larsen et ul., 1992; Kawakami, 1993; Kuno and
pennate muscles in which fascicles are arranged diago- Fukunaga, 1995; Rutherford and Jones, 1992) have
nally to the line of pull of the muscle (Bobbert et ul., 1990; shown that fascicles and aponeurosis can be visualized in
Roy and Edgerton, 1992; Trotter, 1993), it is almost humans by means of ultrasonography and pennation
impossible to describe the behavior of a muscle-tendon angles can be measured in vim.
unit from the joint movement. In the present study, the movement of tendinous tis-
Recently, development of imaging techniques such as sues in the human tibialis anterior muscle (TA) was
MRI and ultrasonography is remarkable, making pos- measured by the use of ultrasonic apparatus with an
sible the determination of the architecture of the muscle- electronic linear array probe of 7.5 MHz wave frequency
tendon complex in humans (Henrikkson-Larsen et al., (ALOKA, SSD-2000, Jpn). The echoes from interspaces
1992: Rutherford and Jones, 1992; Kawakami et al., of the TA were sometimes imaged more clearly when the
plane of probe was changed slightly diagonally to the line
drawn with the pen, in which case the recreated image
Address correspondence to T. Fukunaga. Department of Life was used for the measurement. The experimenter visually
Sciences, University of Tokyo, 3-R-I. Komaba, Meguro, Tokyo, Japan. confirmed the echoes reflected from aponeurosis and
interspaces among fascicles in TA through a comparison of
ultrasonic measurements with direct measures (Kawakami
of (I/.. 1993). The cross point (P) between two echoes. one r adipose tissue
from deep aponeurosis and the other from fascicles. was
easily determined on the ultrasonogram (Fig. 1).
When an ankle joint was dorsi- and plantar flexed
without additional load, it was observed that the
P moved proximally during dorsiflexion and distally
during plantarflexion. Figure 2 shows an example of the
distance, D, moved by P and joint angle, 0, during dorsi-
and plantarflexion without an additional load. The dis-
placement of P studied here is considered to indicate the
excursion of the tendinous tissue in the TA during muscle
contraction. The D appeared to synchronize with the
displacement of the joint angle during dynamic actions,
indicating that the muscle-tendon complexes are stiff
relative to the applied force---fairly small in the case of
foot shaking motion without load. In the human elbow
flexor muscle, no detectable phase shift was observed
between intramuscular and joint displacements during Fig. 1. Ultrasonic image of the human lower leg. Subo~~t,~ncoua adipose
voluntary elbow flexion-extension movements with no tissue and muscle (tibialis anterior) and internal aponcurobis are 1 isua-
ized. The cross-point (P) was determined from the cchoe~ ~>rf deep
additional load (Fellows and Rack, 1987). aponeurosis and fascicles. A placement makct- was fixed IO \kln on the
During dorsiflexion the changes in 6, and D were highly TA at the mid-point of the tibia1 bone as a refcl-encc point I~J lhat doea
correlated in every subjects (1. = 0.93- 0.99) (Fig. 3). not move during contractions.
Because the TA is a bipennate muscle with its proximal
fibers attached to the tibia1 bone, it is reasonable to
assume that the proximal attachment does not move
during contraction (Fig. 4). Thus, displacement of the
central aponeurosis which is attached to tuberosity of
metatarsal in the foot, i.e. movement of P is considered to
be equivalent to the movement of the distal tendon. It
follows therefore that the slope of the regression line in
Fig. 3 (i.e. the distance moved by P per 1 rad of ankle
dorsiflexion) represents the moment arm of TA. Values i 20-
ranging from 44 to 48 mm over a motion range of
17 - 34 were determined for five subjects, which were in
good agreement with a previous report. i.e. TA moment
arm measured by MRI changed between 51 and 42 mm , I I I
0 2 4 6 8 10
depending on ankle joint angles (Rugg et al., 1990).
The tendinous movement observed in this study was Time (s)
caused by the change in length of muscle fibers. However,
the tendinous movement might include elongation of the Fig. 2. Displacement of P (D) and angle of ankle joint (0) during
dorsi- and plantar-flexion. The D was measured at every 25ms.
aponeurosis (although not a large amount). Furthermore, it Zero degree of ankle joint (8) represents at the natural position of
has been shown that the fibers do not run from the origin foot and the D represents the distance from the natural position
to insertion, but taper within fascicles (Hijikata et al., moved by P.

20? 1

I5 -
Subj. A
I Subj. B

b io 2b 0 10 20 0 10 20

8 (de@ 61 (deg) 0 (de@

Fig. 3. The relationships between D and H for three subjects. Significant positive correlation was observed
in all subjects.
Muscle architecture and function in humans

q 0.00 rad
l 0.26 rad

0 5 10 15 20

Fig. 5. Relationship between the distance (AI) moved by the P on
the aponeurosis and the static force (AF) exerted by ‘static‘ contrac-
tion of dorsiflexor at different angles of the ankle joint. 0.00 rad repres-
ents the natural position of the foot, and 0.26 and 0.52 rad represent the
positions dorsiflexed from the natural position, respectively. AF was
obtained from the ‘static’ measured torque of dorsiflexion divided by
the moment arm.

Fig. 4. Schematic illustration for measuring the movement distance of
the P and the moment arm of TA during ankle dorsiflexion. During dorsiflexion with gradually increasing force in each trial
dorsiflexion the point P on deep aponeurosis in TA moved proximally. at three ankle joint angles. The ultrasonic echo from deep
The moment arm is approximately equivalent to the distance D during aponeurosis in TA (same as the point P in Fig. 1) was
1 rad of dorstflexion. observed to move proximally during ‘static’ dorsiflexion,
which is in good agreement with our previous study
(Fukashiro et al., 1995). The distance moved by P(A I) was
1993). Elasticity of the attachments between tapering considered as the changes in tendon length. The tension
fibers might affect the tendinous movement. The present exerted by muscle contraction (AF) was calculated from
study cannot answer what amount in the tendinous the joint torque measured by a dynamometer and the
movement is muscle and what amount is tendon. In moment arm reported previously (Rugg et (ll., 1990).
addition, the present results are based on the measure- The tension (A.F))length (AI) curve during ‘static’ con-
ments of the movement of one certain point on the traction (Fig. 5) was well-fitted to quadratic regression,
aponeurosis. It has been shown in rat muscles that there which was quite similar to that of the isolated tendon
is some variability in the elasticity over the aponeurosis (Woo, 1981).
(Zuurbier et nl., 1994). Such heterogeneity may exist in The force-length curve of the human tendon can be
human muscles, in which case the movement of separate directly but noninvasively obtained by the ultrasonic
areas on the aponeurosis might not be the same. This method, and it is considered that during static muscle
uncertainty would be the subjects, who can be investi- contraction an elastic component (i.e. mainly tendinous
gated with the present method in future studies. This tissue) of the muscle-tendon complex is stretched signifi-
method would also have other applications in the field of cantly by the contraction force of the muscle.
muscle physiology and biomechanics in humans.

ACTION Most skeletal muscles run across the joints; thus, the
shortening of muscle fibers induces changes in joint
According to Hill’s classical model, the muscle-tendon angles. The muscle architecture (geometric character-
complex consists of contractile and series elastic compo- istics of fiber or tendon), therefore, has a considerable
nents (CC and SEC, respectively). The major part of SEC effect on the force-producing capacity of the muscle (Roy
is located in the tendinous tissues (Huijing, 1992). The and Edgerton, 1992; Huijing, 1992).
SEC demonstrates elastic behavior in most movements We measured the length and angle of fascicle (fiber) of
and especially when the muscle is activated and simulta- the vastus lateralis muscle and observed changes in the
neously stretched prior to concentric action (Komi, fascicle length and pennation angle during knee exten-
1984). The characteristics of SEC have been indirectly sion. In the ultrasonic image obtained from the vastus
estimated by special in vivo and in vitro methods (Huijing, lateralis muscle at 50% of the distance from the greater
1992; Poussen et nl., 1990). trochanter to the lateral epicondyle of the femur (Fig. 6)
We can observe in civo the movement of tendinous the echoes reflected from the fascicles and deep aponeur-
tissue in tibialis anterior muscle (TA) during ‘static’ con- osis can be observed. One of the fascicles was carefully
traction by means of ultrasonography. The subject lay traced from the proximal and distal ends. and the
supine on a bed and was requested to perform ‘static’ length of fascicle was measured by the use of a digital
Knee angle 15” Knee angle 50”

Fig. 6. Ultrasonic image obtained from human vastus lateralis muscle at two different joint angles during
relaxed and tensed conditions with 10% of maximal static strength. The ultrasonic transducer was placed
on the skin over the vastus lateralis muscle at 50% of the distance from the great trochanter to lateral
epicondyle of femur. The fascicle length (fl) was determined as the length of a line drawn along the
ultrasonic echo parallel to fascicles. The fascicle angle (0) was determined as angles between the echoes
obtained from fascicles and deep aponeurosis in the ultrasonic image.

curvimeter. The fascicle angles, defined as the angles 1501
I *
between the echoes of the deep aponeurosis and the
echoes from interspaces among fascicles were also meas-
ured. When the knee was extended passively from 100’
flexion (0” = full extension) without muscle contraction,
the fascicle length decreased by 18%, from 129 + 9 mm
(mean + SE.) at 100” to 107 f 8 mm at 20” (Fig. 7).
When the knee extensors contracted ‘statically’ with 10%
of their maximal voluntary strength (MVC) at different
joint angles, in which case the MVC changed due to the
----.-.- Relaxed
joint angle, the fascicle length decreased and its magni- - Tensed
tude was greater (30%) when the knee was closer to full
extension than that (5%) at the flexed positions (Fig. 7).
During ‘static’ contractions of the quadriceps muscle so!
100 80 60 40 20
a patellar tendon was oriented anteriorly at extended
knee positions (Herzog and Read, 1993) suggesting lax- Knee joint angle (de@
ity of the joint in this condition. Because the
Fig. 7. Changes in fascicle lengths at various angles of the knee joint
muscle-tendon complex consists of muscle fibers and (n = 6. mean and SE.). After measurements of the fascicle length with-
tendinous tissues, or of CC and SEC (Bobbert et al., out muscle contraction at each joint angle the subject was requested to
1990) the differences in changes in fascicle length be- perform isometric contractions of knee extensor muscles at 10% MYC
tween the relaxed and tensed conditions would be caused by using a specially designed dynamometer (MYORET, Asics, JPN) in
by the laxity of the relaxed muscle and the lengthening of which the gravitational effect was controlled and the fascicle length was
measured during contraction as well.
the SEC during contraction. Because lengthening of the
SEC is a function of tension applied to it (Bobbert et al.,
1990) the lengthening of SEC would be expected at each the slackness of the muscle-joint system when the knee is
joint angle. Larger shortening of the fascicles at the extended. The fascicles are connected to the deep apo-
extended that at flexed positions would be due to neurosis with an angle, which was defined as a fascicle
Muscle architecture and function in humans 461

“M z
- 18.
z 8- Angular velocity lOdeg/sec
"M 2v 6-
9b x
cd 14-

100 80 60 40 20

Knee joint angle (deg) 01
100 80 60 40 20
Fig. 8. Changes in fascicle angles as a function of knee angles (n = 6, Knee joint angle (deg)
mean and S.E.). Significantly higher fascicle angles in tensed than in
relaxed conditions were observed at the extended positions (i.e. knee Fig. 9. Velocity of shortening of the fascicle in relation to knee joint
angle = 20 ). angles (n = 6. mean and SE.). The fascicle velocity was calculated from
changes of the fascicle length traveled in 10 of the joint when the knee
was extended ‘isokinetically’ with an angular velocity of 10 s-’ and
angle (or pennation angle). The fascicle angle at the with a tension of about 10% MVC by an isokinetic dynamometer.
relaxed condition increased from 14 to 17” with knee
extension (Fig. 8). Larger fascicle angles were observed in
tensed than in relaxed conditions at each joint angle and with knee extension, e.g. much lower MVC (81 N m) at
greater differences between the two conditions were ob- knee extended position (20”), was observed, compared to
served when the knee was in extended positions. The knee flexed positions (244 N m at 60” and 213 N m at
pennation angle of vastus lateralis muscle has been re- 100”).
ported to be 5520” obtained from cadavers (Yamaguchi
et al., 1990) and 6 - 27” in living humans (Henriksson- PENNATION ANGLES IN HYPERTROPHIED MUSCLES
Larsen et ul., 1992; Rutherford and Jones, 1992).
These are in good agreement with our measurements. As Morphologically, skeletal muscles are roughly divided
the force applied to the tendon by the contraction of into two types, parallel fiber muscles in which fibers line
muscle fibers is less than the sum of the forces of the almost parallel to the line of action of the muscle and
individual fibers, i.e. the tendon force is reduced by a fac- pennate muscles in which fibers insert into the tendon at
tor of cos0 (0 = pennation angle), the larger the penna- an angle to the line of action of the muscle (pennation
tion or fascicle angles, the more disadvantageous the angle) (Jones et al., 1989; Hijikata et al., 1993). The
force development would be expected (Gans and Gaunt, pennation angle (fascicle angle) in the human triceps
1991; Roy and Edgerton, 1992; Kawakami et al., 1993). brachii muscle was measured as 10 - 60” for many differ-
Increase of the fascicle angle at the extended positions, ent age groups (aged 10-60yr) by means of the ultrasonic
therefore, implies a mechanical disadvantage in the trans- method. Figure 10 shows the relationship between the
mission of force. fascicle angle and the muscle thickness for the triceps
In previous studies the ‘isokinetic’ contraction has brachii muscle with significant correlation coefficients.
been defined as joint action at a constant angular velocity which agrees with a previous study (Kawakami et al..
throughout the range of motion (Wickiewicz et al., 1984). 1993). These would imply that muscle hypertrophy might
When the knee was extended with a given angular velo- accompany an increase in fiber angles. Maxwell et al.
city (i.e. ‘isokinetic’ action), the shortening velocity of (1974) predicted that for the muscle having constant
fascicle increased when the knee was in extended posi- muscle length, fiber length, and fiber numbers, hyper-
tions (Fig. 9) i.e. with ‘isokinetic’ extension of the knee trophy (i.e. increase in the diameter of fibers) must accom-
with 10’~si during the whole range of motion the fas- pany increases in pennation angles and muscle thickness.
cicle velocity was 4 mm s- ’ at flexed positions (100-60”) The physiological cross-sectional area (PCSA) of
and increased linearly up to double this (8 mm s-i) near muscle, which is defined as the total area of fiber in
the knee extension. This would suggest that when study- parallel and then represents the force potential produced
ing the functional characteristics of muscle fiber from by muscle, is calculated by
knee joint actions, care has to be taken as to the hetero- PCSA = (MV/FL)cos 8.
geneity of the shortening velocity of muscle fibers during
isokinetic muscle actions, especially when the knee is where MV is muscle volume and FL is muscle-fiber
close to the extended positions. length. The cosine of the pennation angle 8 normalizes
Considering the smaller force production at shorter fiber angulation to the line of action of the muscle. If
muscle lengths and at higher contraction velocities esti- muscle hypertrophy accompanied the increase in
mated from the force-length and forceevelocity relation- fiber pennation angles, then this change would be disad-
ships, and the lower efficiency of force transmission at vantageous for the force development. However, an in-
larger angles of pennation, the work performance at the crease in pennation angles would cause more contractile
tendon of vastus lateralis muscle is sequentially reduced material to be attached to the tendon. which would
Friedrich, J. A. and Brand. R. A. (1990) ivlusclc ar~hllccturc 11, iltc
human lower limb. J. Biur?rrc,hrrnirs 23, Y I 95.
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