Neil D. Reeves and Marco V.

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J Appl Physiol 95:1090-1096, 2003. First published May 9, 2003; doi:10.1152/japplphysiol.01046.2002

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J Appl Physiol 95: 1090–1096, 2003.
First published May 9, 2003; 10.1152/japplphysiol.01046.2002.
Behavior of human muscle fascicles during shortening
and lengthening contractions in vivo
Neil D. Reeves and Marco V. Narici
Centre for Biophysical and Clinical Research into Human Movement, Manchester
Metropolitan University, Alsager Campus, Cheshire, United Kingdom ST7 2HL
Submitted 14 November 2002; accepted in final form 2 May 2003
Reeves, Neil D., and Marco V. Narici. Behavior of
human muscle fascicles during shortening and lengthening
contractions in vivo. J Appl Physiol 95: 1090–1096, 2003. First
published May 9, 2003; 10.1152/japplphysiol.01046.2002.—
The aim of the present study was to investigate the behavior
of human muscle fascicles during dynamic contractions.
Eight subjects performed maximal isometric dorsiflexion con-
tractions at six ankle joint angles and maximal isokinetic
concentric and eccentric contractions at five angular veloci-
ties. Tibialis anterior muscle architecture was measured in
vivo by use of B-mode ultrasonography. During maximal
isometric contraction, fascicle length was shorter and penna-
tion angle larger compared with values at rest (P ⬍ 0.01).
During isokinetic concentric contractions from 0 to 4.36
rad/s, fascicle length measured at a constant ankle joint
angle increased curvilinearly from 49.5 to 69.7 mm (41%; P ⬍
0.01), whereas pennation angle decreased curvilinearly from
14.8 to 9.8° (34%; P ⬍ 0.01). During eccentric muscle actions,
fascicles contracted quasi-isometrically, independent of an-
gular velocity. The behavior of muscle fascicles during short-
ening contractions was believed to reflect the degree of
stretch applied to the series elastic component, which de-
creases with increasing contraction velocity. The quasi-iso-
metric behavior of fascicles during eccentric muscle actions
suggests that the series elastic component acts as a mechan-
ical buffer during active lengthening.
isokinetic dynamometry; muscle contraction; muscle archi-
tecture; ultrasonography
THE ARCHITECTURE OF A SKELETAL muscle is an important
determinant of its functional characteristics (13). Hu-
man muscle architecture may be studied noninvasively
in vivo both at rest and during muscle contraction, by
using real-time ultrasonography (15, 20, 22). Indeed,
several investigators (9, 24, 27) have demonstrated
that during isometric contractions muscle architecture
undergoes remarkable changes. However, very few
studies (10, 17) have explored the changes in muscle
architecture occurring in dynamic contractions. This is
despite the fact that most contractions performed in
daily living are dynamic. In humans, the fascicles of
the gastrocnemius muscle have been observed to con-
tract quasi-isometrically during the support phase of
walking, whereas the muscle-tendon complex length-
ens (10). During the eccentric phase of walking in the
Address for reprint requests and other correspondence: N. D.
Reeves, Centre for Biophysical and Clinical Research into Human
Movement, Manchester Metropolitan Univ., Alsager Campus, UK
ST7 2HL (E-mail: n.reeves@mmu.ac.uk).
1090 8750-7587/03 $5.00 Copyright © 2003 the American Physiological Society
cat, while the muscle-tendon complex lengthens, the
fibers actually shorten, suggesting that the length
change is almost entirely accounted for by the compli-
ance of the tendon (14).
Wickiewicz et al. (31) used the architectural fea-
tures obtained from cadavers in an earlier study (32)
to estimate the in vivo maximum shortening velocity
of muscle fibers from contractions performed by
healthy subjects. However, because of the changes
Downloaded from jap.physiology.org on April 23, 2010
occurring in muscle tissue during the fixation pro-
cess, measurements obtained from cadavers should
not be used to predict the behavior of muscle fibers in
vivo. The dynamic behavior of muscle has been stud-
ied in vivo by using sinusoidal oscillations during
submaximal contractions (3) and has been shown to
fit well to the force-velocity relationship predicted by
Hill’s hyperbola (28). The first study that investi-
gated changes in human muscle architecture mea-
sured in vivo during shortening contractions was
performed by Ichinose et al. (17). It was found that
the degree of shortening of muscle fascicles de-
creased as contraction velocity increased. However,
the above study presents two limitations. The first
was that of having investigated only a limited range
of shortening velocities (30 and 150°/s), with a peak
velocity that represents only 20% of the estimated
maximal shortening velocity for this muscle group,
knee extensors (see Ref. 31). The second limitation
was that of having investigated changes in muscle
architecture only in shortening contractions but not
in lengthening contractions. Hence the purpose of
the present study was to extend these measurements
also to lengthening contractions, investigating
changes in fascicle lengths and pennation angles
over a greater range of shortening and lengthening
angular velocities with the aim of comparing the
behavior of fascicles during both shortening and
lengthening contractions. The hypothesis of the
present study was that changes in fascicle length
would reflect the degree of stretch of the series elas-
tic component (SEC), which comprises the intra- and
extramuscular tendon tissue as well as that residing
within the cross bridges, and that this would be
dependent on the velocity of contraction.
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby
marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
http://www.jap.org
 BEHAVIOR OF MUSCLE FASCICLES IN DYNAMIC CONTRACTIONS
METHODS
Subjects. Eight subjects (4 men and 4 women, mean ⫾ SD
age, height, and body mass of 25.1 ⫾ 2.6 yr, 175 ⫾ 7.4 cm, and
70.3 ⫾ 9.5 kg, respectively) gave their written, informed
consent to participate in this study, after the ethics commit-
tee of the Centre for Biophysical and Clinical Research into
Human Movement at the Manchester Metropolitan Univer-
sity had approved the procedures involved. This sample size
was selected on the basis of a power analysis performed
previously with repeated measures of fascicle length, penna-
tion angle, and isokinetic torque. All procedures complied
with the Declaration of Helsinki.
Torque measurements. The force-velocity features of the
dorsiflexor muscle group [tibialis anterior (TA) muscle] were
investigated by measuring the torque developed during max-
imal voluntary contraction (MVC) performed on an isokinetic
dynamometer (Cybex NORM, Ronkonkoma, NY). Subjects
lay in the supine position on the bench with the right knee
joint securely fixed at an angle of 1.57 rad (90°) to prevent
movement of the tibia with respect to the center of rotation of
the talocrural joint. The right foot was tightly strapped to a
footplate; all measurements were performed on the right leg.
Subjects had previously attended the laboratory on at least
one occasion to become familiarized with the procedures of
the investigation. The anatomical zero of the foot was defined
as a 1.57-rad angle between the coronal plane of the tibia and
the footplate. The range of motion was from full plantarflex-
ion to full dorsiflexion. Maximal isometric dorsiflexion torque
was measured at ankle joint angles of ⫹0.52, ⫹0.35, ⫹0.17, 0,
⫺0.17, and ⫺0.35 rad (⫹30, ⫹20, ⫹10, 0, ⫺10, and ⫺20°,
respectively). Two maximal contractions were performed at
each joint angle, separated by 60 s of rest between contrac-
tions. Contractions were held until the experimenter ob-
served a plateau in torque, displayed on the screen of a
computer (Apple Macintosh, G4, Cupertino, CA) interfaced
with an acquisition system (Acknowledge, Biopac Systems,
Santa Barbara, CA) used for analog-to-digital conversion.
This time period was ⬃3–5 s. Maximal isokinetic concentric
and eccentric dorsiflexion contractions were performed at
angular velocities of 0.87 (50), 1.75 (100), 2.62 (150), 3.49
(200), and 4.36 rad/s (250°/s). A set of five concentric and five
eccentric maximal contractions was performed at each angu-
lar velocity. Contractions were performed in cycles, with a
concentric contraction being immediately preceded by an
eccentric contraction. An isometric phase lasting ⬃100 ms
preceded each eccentric contraction, ensuring that the mus-
cle underwent a period of isometric preloading, thereby
maintaining a constant preactivation level. Pilot work indi-
cated that this phase of isometric contraction, preceded by
maximal concentric contraction, was sufficient to produce an
isometric fascicle length before the eccentric action. A rest
period of 180 s separated each set of contractions. During all
contractions, torque, ankle joint angle, TA muscle electro-
myographic (EMG) activity, and angular velocity were sam-
pled simultaneously by the acquisition system at a frequency
of 2,000 Hz and were saved for subsequent analysis.
Isokinetic torque was analyzed at a position corresponding
to an ankle joint angle of 0.14 rad (8°) for both concentric and
eccentric contractions. The rationale for this procedure was
justified by the observation that the isovelocity phase of the
contraction decreased and occupied a narrower portion, to-
ward the midrange of joint motion with increasing angular
velocity. The ankle joint angle of 0.14 rad was selected as a
position to read torque, because it fell within the isovelocity
phase of both concentric and eccentric contractions for all
angular velocities. If this specific angle did not lie within the
J Appl Physiol • VOL 95 • SEPTEMBER 2003 •
1091
isovelocity phase for a certain subject, the closest angle
corresponding to an isovelocity phase was selected; in any
case this angle did not deviate more than ⫾0.02 rad from the
ankle joint angle of 0.14 rad. The highest isoangular torque
from each of the five concentric and eccentric contractions at
each angular velocity was selected.
The TA moment arm was assumed to represent the com-
mon moment arm of the dorsiflexors, and this was estimated
at 0.14 rad of ankle joint angle from the data of Rugg et al.
(29). Rugg et al. measured the TA moment arm during
contraction, from sagittal-plane magnetic resonance imaging
scans. Force (N) of the dorsiflexor muscle group was calcu-
lated from the following equation
F d ⫽ T/MA
where Fd is the force generated by the dorsiflexor muscle
group, T is the joint torque, and MA is the TA moment arm
at 0.14 rad of ankle joint angle (29). The peak of the two
isometric contractions at each ankle joint angle was selected.
The isometric force at 0.14 rad was estimated from the
torque-ankle joint angle data by fitting the experimental
points with a line of best fit.
Ultrasonography. The architectural features of the TA
Downloaded from jap.physiology.org on April 23, 2010
muscle: pennation angle, fascicle length, and the distance
between aponeuroses (Fig. 1) were assessed from images
obtained using real-time B-mode ultrasonography (ATL-HDI
3000, Bothwell, WA). After identification and marking of the
proximal and distal insertions of the muscle, a 7.5-MHz
linear-array probe with a 38-mm scanning length was posi-
tioned perpendicular to the dermal surface along the midsag-
ittal plane of the TA muscle at the site corresponding to the
thickest portion of the muscle, identified by ultrasound. This
site was clearly marked to provide a standardized measure-
ment site and ensure that measurements at all velocities
were taken from the same external site. The probe was
coated with a water-soluble transmission gel to provide
acoustic contact without depressing the dermal surface. Ac-
curacy of the ultrasound method in measuring muscle archi-
tectural features has been previously demonstrated to show
good agreement with direct anatomical measurement on a
cadaver (27).
Images were obtained at rest and during maximal isomet-
ric contraction at ankle joint angles of ⫹0.52 to ⫺0.35 rad in
0.17-rad increments. Images were obtained during maximal
isokinetic concentric and eccentric contractions at 0.87, 1.75,
2.62, 3.49, and 4.36 rad/s. Images were recorded onto video-
tape at 50 Hz for subsequent analysis. At rest and during
contraction, the probe was firmly held in place at the mea-
surement site by the experimenter. Ultrasound images were
Fig. 1. Sagittal plane ultrasound scan of the tibialis anterior muscle
showing the architectural features of fascicle length (Lf), pennation
angle (␪), and the distance between superficial and central tendon
aponeuroses (t).
www.jap.org
1092 BEHAVIOR OF MUSCLE FASCICLES IN DYNAMIC CONTRACTIONS
taken with adjusted depth and focus to optimize image qual-
ity and sampling frequency. Sampling frequency was main-
tained at or above 28 Hz. Acquired isometric images were
analyzed at the time point at which peak torque was gener-
ated. Acquired isokinetic concentric and eccentric contraction
images were analyzed at the time point corresponding to 0.14
rad of ankle joint angle. The image corresponding to the
highest concentric and eccentric force at 0.14 rad of ankle
joint angle for each angular velocity was analyzed. An exter-
nal voltage (10-V) trigger was used to synchronize the ultra-
sound with the acquisition system. The delta time was mea-
sured from the point of application of the external trigger to
the desired torque or ankle joint angle displayed on the
acquisition system. To locate the corresponding ultrasound
image, this time period was then applied to the ultrasound
sequence, starting from the point of application of the exter-
nal trigger.
Measurements of fascicle length, pennation angle, and
distance between aponeuroses were performed by using dig-
itizing software (NIH Image, version 1.61, National Insti-
tutes of Health, Bethesda, MD). Pennation angle was defined
as the angle created by the echoes from the fascicles and their
insertion into the aponeurosis. This was measured at the
superficial and central aponeuroses, and the two values were
then averaged. Measurements of t, defined as the distance
between the superficial and central aponeuroses, were made
on either side of the image and then averaged (Fig. 1). One
end of the fascicle generally extended off the acquired ultra-
sound image. The visible part of the fascicle was measured by
using digitizing software and, by assuming a linear continu-
ation, trigonometry was used to estimate the part of the
fascicle that was not visible. To estimate the order of error
associated with this method of determining fascicle length,
additional measurements were taken in a subsample of sub-
jects (n ⫽ 6). A maximal isometric contraction was performed
and maintained for 4–5 s, during which the ultrasound probe
was moved along the midsagittal plane of the muscle, over a
series of external markers fixed on the skin with surgical
tape. The ultrasound image was reconstructed and the entire
length of fascicles identified. The actual fascicle length was
measured and compared with the estimated fascicle length
determined when using the available scan window of 38 mm.
These measurements indicated that the order of error asso-
ciated with estimating fascicle length was 2.4%. In the event
of fascicles inserting curvilinearly into the aponeurosis, pen-
nation angle was measured by using an approach previously
applied for the triceps surae muscle group (24). Muscle ar-
chitecture was analyzed from the superficial half of the
bipennate TA only, on the basis of reports that the architec-
tural features are not significantly different between the two
parts of the muscle at rest in any joint position or during
isometric contraction (23).
Measurement of electromyographic activity. Electromyo-
graphic activity was assessed from the TA muscle. Two
self-adhesive Ag-AgCl electrodes 10 mm in diameter (Neuro-
line, Medicotest, Rugmarken, Denmark) were placed in a
bipolar configuration with a constant interelectrode distance
of 20 mm at a site corresponding to the proximal third of the
muscle (34), with the reference electrode placed on the lateral
tibial condyle. In an attempt to minimize cross-talk from
adjacent muscles, electrodes were placed along the midsag-
ittal plane of the muscle, guided by axial-plane ultrasound
scanning. To reduce skin impedance below 5,000 ⍀ , elec-
trode placement was preceded by shaving, skin abrasion, and
cleansing with an alcohol-based solution. Sampled at 2,000
Hz by the acquisition system, the raw EMG signal was
preamplified and filtered by using high- and low-pass filters
J Appl Physiol • VOL 95 • SEPTEMBER 2003 •
set at 10 and 500 Hz, respectively. The EMG activity was
measured over a 30-ms time period corresponding to 0.14 rad
of ankle joint angle for both concentric and eccentric contrac-
tions. During an isometric contraction performed at 0.17 rad,
the EMG activity was measured over a 30-ms time period
corresponding to maximal torque. Measurements were per-
formed taking into account the electromechanical delay, and
the raw signal was then rectified, integrated, and normalized
for a 1-s time period.
Statistical analysis. Repeated-measures 2 ⫻ 6 factorial
analysis of variance (ANOVA) was used to test for any dif-
ferences in pennation angle, fascicle length, distance be-
tween aponeuroses of the TA muscle as a result of changes in
ankle joint angle (⫹0.52 to ⫺0.35 rad), and contraction state
(rest; isometric MVC). Repeated-measures 2 ⫻ 6 factorial
ANOVA was used to test for any differences in pennation
angle, fascicle length, distance between aponeuroses of the
TA muscle as a result of changes in angular velocity (0 to 4.36
rad/s), and contraction type (concentric or eccentric). Re-
peated-measures 2 ⫻ 6 factorial ANOVA was applied to test
for any differences in the integrated EMG activity of the TA
muscle as a result of changes in angular velocity (0 to 4.36
rad/s) and contraction type (concentric or eccentric). Where
Downloaded from jap.physiology.org on April 23, 2010
necessary, post hoc analysis was performed by using
Scheffé’s procedure. Significance was accepted at P ⬍ 0.05,
and values presented are means ⫾ SD.
RESULTS
Effect of ankle joint angle and isometric contraction
on fascicle length, pennation angle, and distance be-
tween aponeuroses. Fascicle length (mean of resting
and contracted fascicle length) at ⫹0.52 rad of ankle
joint angle (80.4 ⫾ 2.4 mm) was significantly greater
than fascicle length at every other ankle joint angle,
with the exception of ⫹0.35 rad (P ⬍ 0.01). Fascicle
length averaged across all ankle joint angles during
maximal isometric contraction (53.8 ⫾ 2.9 mm) was
significantly shorter compared with that at rest (71.9 ⫾
1.9 mm; P ⬍ 0.01; Fig. 2A).
Pennation angles (mean of resting and contracted
pennation angles) at ⫹0.52 rad of ankle joint angle
(8.5 ⫾ 0.5°) were significantly smaller compared with
pennation angles at every other ankle joint angle,
except ⫹0.35 rad (P ⬍ 0.01). Pennation angles (mean
across all ankle joint angles) were significantly greater
during maximal isometric contraction (13.9 ⫾ 0.7°)
compared with those in the relaxed state (9.6 ⫾ 0.5°;
P ⬍ 0.01). A significant interaction indicated that pen-
nation angle at every given ankle joint angle, with the
exception of ⫹0.52 rad, was significantly greater dur-
ing isometric contraction compared with that at rest
(P ⬍ 0.01; Fig. 2B).
Changes in ankle joint angle from ⫹0.52 to ⫺0.35°
and the transition from rest to isometric MVC did not
result in significant changes in muscle thickness.
Effect of angular velocity and contraction type on
fascicle length, pennation angle, and distance between
aponeuroses. Fascicle length at a constant ankle joint
angle (0.14 rad) was significantly greater during con-
centric contraction at angular velocities of 3.49 (68.2 ⫾
5.9 mm, P ⬍ 0.01) and 4.36 rad/s (69.7 ⫾ 5.1 mm, P ⬍
0.01) compared with that during isometric contraction
(0 rad/s; 49.5 ⫾ 3 mm). Furthermore, fascicle length
www.jap.org
 BEHAVIOR OF MUSCLE FASCICLES IN DYNAMIC CONTRACTIONS 1093

0.3 mm) compared with during concentric contraction

(12.2 ⫾ 0.4 mm) at a constant ankle joint angle. The
distance between aponeuroses did not change signifi-
cantly as a function of angular velocity.
Force-velocity features of the dorsiflexor muscle
group. Force-velocity characteristics of the dorsiflexor
muscle group are displayed in Fig. 4. The peak isoan-
gular force of the dorsiflexors produced during eccen-
tric contractions (1,548.3 ⫾ 384 N) was 1.27 times
greater than the force produced during isometric con-
traction (1,218.5 ⫾ 293.1 N). Because the highest
tested angular velocity was 4.36 rad/s, which corre-
sponds to ⬃54% of the maximum shortening velocity of
the dorsiflexor muscle group (31), the data points were
deliberately not fitted with a predicted curve such as
Hill’s equation, because this would have required the
measurement of force-velocity values up to zero load.
Nevertheless, the data points at the highest two veloc-
ities (3.49 and 4.36 rad/s) seem clearly above the force
values that would be expected from a hyperbolic data
distribution passing through all the positive force-ve-

Downloaded from jap.physiology.org on April 23, 2010

locity data points. Possible reasons for this phenome-

Fig. 2. Tibialis anterior muscle fascicle length (A) and pennation

angle (B) as a function of changes in ankle joint angle at rest and
during maximal isometric contraction. Values presented are
means ⫾ SD (n ⫽ 8). * Significant difference (P ⬍ 0.01) between rest
and isometric contraction.

during concentric contraction at 0.87 rad/s (54.1 ⫾ 3.7

mm) was significantly shorter compared with that at
4.36 rad/s (Fig. 3A). Fascicle length measured at a
constant joint angle during eccentric contraction was
independent of angular velocity and was not signifi-
cantly different from fascicle length during isometric
contraction (Fig. 3A).
At a constant ankle joint position, pennation angles
during isometric contraction (0 rad/s; 14.8 ⫾ 0.8°) were
significantly greater compared with pennation angles
during concentric contractions at 1.75 (11.8 ⫾ 0.8°),
2.62 (11 ⫾ 0.8°; P ⬍ 0.01), 3.49 (10.2 ⫾ 0.6°; P ⬍ 0.01),
and 4.36 rad/s (9.8 ⫾ 0.9°; P ⬍ 0.01). Pennation angles
during eccentric contraction at all angular velocities
except 4.36 rad/s (11.8 ⫾ 0.6°) were significantly
smaller compared with those during isometric contrac-
tion (0 rad/s). Pennation angles did not change signif-
icantly as a function of angular velocity during eccen-
tric contraction; however, during concentric contrac-
tion pennation angles at 3.49 and 4.36 rad/s were
significantly less than those at 0.87 rad/s (13.3 ⫾ 0.8°; Fig. 3. Tibialis anterior muscle fascicle length (A) and pennation
Fig. 3B). angle (B) at 0.14 rad of ankle joint angle during concentric and
eccentric contractions (n ⫽ 8). Values presented are means ⫾ SD. *
Averaged over all angular velocities, eccentric con- and ** Significant difference (P ⬍ 0.05 and P ⬍ 0.01, respectively)
tractions resulted in a significantly greater distance from 0 rad/s. *** Significant difference (P ⬍ 0.01) from 0 rad/s and
between superficial and central aponeuroses (12.7 ⫾ 0.87 rad/s.

J Appl Physiol • VOL 95 • SEPTEMBER 2003 • www.jap.org

1094 BEHAVIOR OF MUSCLE FASCICLES IN DYNAMIC CONTRACTIONS
Fig. 4. Mean ⫾ SD isoangular force-velocity characteristics of the
dorsiflexor muscle group (n ⫽ 8).
non are suggested in the DISCUSSION. There were no
significant differences in the integrated EMG activity
of the TA muscle over the tested angular velocities
during either concentric (ranging from 2.24⫺01 ⫾
2.38⫺02 to 2.64⫺01 ⫾ 5.78⫺02 mV 䡠 s; P ⬎ 0.05) or eccen-
tric (ranging from 2.58⫺01 ⫾ 3.66⫺02 to 2.88⫺01 ⫾
3.19⫺02 mV 䡠 s; P ⬎ 0.05) contractions. There were also
no significant differences in the integrated EMG activ-
ity between concentric and eccentric contractions at
any angular velocity (P ⬎ 0.05).
DISCUSSION
The main findings of the present study were 1) at a
constant ankle joint angle, fascicle length and penna-
tion angle changed significantly as a function of short-
ening velocity; 2) fascicle length was greater at the
higher compared with the lower shortening velocity;
and 3) during eccentric muscle actions, fascicles be-
haved quasi-isometrically. Each of these findings will
be discussed in detail in the sections below.
TA muscle architecture at rest and during isometric
contraction. Fascicle length at rest was found to be
dependent on ankle joint angle, decreasing by 38%
with passive movement from full plantarflexion to full
dorsiflexion (Fig. 2A), accompanied by a 64% increase
in pennation angle (Fig. 2B). Fascicle length was
shorter and pennation angle greater during maximal
isometric contraction compared with that at rest. This
has been observed previously (9, 24, 27) in other mus-
cles and is due to the fascicles shortening at the ex-
pense of the SEC (19). Pennation angle of the TA
muscle during isometric contraction was greater than
at rest at every joint angle except ⫹0.52 rad (Fig. 2B).
The magnitude of the difference between rest and
isometric contraction was greater closer to full dorsi-
flexion (⫺0.35 rad). A similar pattern has been ob-
served in the vastus lateralis muscle (9) and is likely
due to the low passive tension of the slack muscle-
tendon complex. This concept is supported by the 166%
increase in pennation angle of the slack-fibered bra-
J Appl Physiol • VOL
chialis muscle in the transition from rest to maximal
isometric contraction (16). In agreement with findings
in the gastrocnemius medialis (GM) muscle (27), the
transition from rest to maximal isometric contraction,
in conjunction with changes in joint angle, had no
effect on the distance between the superficial and cen-
tral aponeuroses in the TA muscle.
Force-velocity features of the dorsiflexors. Concentric
force at the faster angular velocities appeared to be
higher than might be expected and seems to deviate
from the typical hyperbolic relation. A possible expla-
nation is that the concentric contractions may have
been potentiated by the immediately preceding eccen-
tric contraction, via the storage and subsequent release
of elastic energy (e.g., Ref. 2). Indeed, this has been
demonstrated to occur in the knee extensors, where the
performance of a prior eccentric contraction enhanced
the subsequent concentric torque beyond that using a
prior isometric contraction (8). Dorsiflexion force is
produced by the combined effects of four muscles: TA,
extensor digitorum longus, extensor hallucis longus,
Downloaded from jap.physiology.org on April 23, 2010
and peroneus tertius (30). The TA muscle was consid-
ered to be the major contributor to dorsiflexion torque
because of its relative physiological cross-sectional area
composing ⬃60% of the entire dorsiflexor volume (11, 12).
It has not yet been possible to directly measure in vivo
the force exerted by one of these synergist muscles, and a
number of assumptions must be made when calculating
the force exerted by this muscle group. The generated
joint moment was divided by the moment arm at 0.14 rad
of ankle joint angle, taken from the data of Rugg et al.
(29) during contraction, to provide an estimate of the
combined dorsiflexor muscle group force. This is as-
suming that the TA moment arm represents the com-
mon moment arm for the entire dorsiflexor muscle
group. The force presented is assuming no coactivation
of plantarflexors, which would subtract from the gross
force produced by the dorsiflexor muscle group. Antag-
onist integrated electromyographic (iEMG) activity of
the soleus muscle during maximal isometric dorsiflex-
ion was identified to be ⬍3% of the iEMG activity
produced during maximal isometric plantarflexion
(26). By assuming a linear iEMG-MVC relationship, it
was estimated the antagonist soleus iEMG signal
would result in an opposing moment of 1–6 Nm during
maximal isometric dorsiflexion.
Changes in muscle architecture during shortening
contractions. At a constant ankle joint angle, TA mus-
cle fascicle length increased curvilinearly (from 49.5 to
69.7 mm) during concentric contractions of increasing
angular velocity from 0 to 4.36 rad/s (Fig. 3A). These
results agree with findings in the vastus lateralis mus-
cle, showing that during concentric contraction the
extent of fascicle shortening is greater at a lower com-
pared with a higher angular velocity (17). In the
present study, fascicles were shorter by 41% during
contraction at 0 rad/s compared with those during
concentric contraction at 4.36 rad/s. An equivalent
increase in angular velocity during concentric contrac-
tion resulted in a concomitant 34% decrease in penna-
tion angle (Fig. 3B).
95 • SEPTEMBER 2003 • www.jap.org
 BEHAVIOR OF MUSCLE FASCICLES IN DYNAMIC CONTRACTIONS
The mechanism responsible for the observed changes
in fascicle length and pennation angle as a function of
shortening velocity is most likely due to the compliance
of the SEC. The SEC can only be stretched by applying
a force, either passive (changes observed at rest as a
function of ankle joint angle) or active, and the greater
the force, the greater the extension (33). During iso-
metric contraction, the force is greater compared with
during any concentric contraction; therefore shorten-
ing of fascicles, stretching of the SEC, and pennation
angles are all at their greatest. As the angular velocity
increases during concentric contraction, the muscle
produces less force, which results in a reduced short-
ening of the contractile element. As fascicle shortening
becomes less pronounced, a smaller proportion of the
central aponeurosis is pulled proximally, which leads
to smaller pennation angles during faster shortening
velocities. Evidence in support of this concept comes
from ramp isometric contractions in which greater
proximal displacement of the central aponeurosis (25),
greater fascicle shortening, and increasing pennation
angles (24, 27) occur with increments in force from rest
up to isometric MVC. The decreasing pennation angles
during concentric contraction of increasing angular
velocity observed in the present study are advanta-
geous for reducing the loss of force transmission to the
tendon. Torque is often read at a constant joint angle
because this is thought to reflect a constant muscle
length and an underlying assumption is that this rep-
resents a constant fiber length. The present results
demonstrate that a constant fiber length cannot be
assumed from the same joint angle during concentric
contractions of different angular velocities. Caution
must be emphasized when interpreting the results of
the present study at the higher angular velocities.
Because the duration of each contraction was reduced
at the faster angular velocities, the number of ultra-
sound frames available for analysis decreased. This is
a constraint of the ultrasound equipment; however, an
ideal situation would be to increase scanning frequency
in proportion to the reduction in contraction duration,
to allow the same number of ultrasound frames to be
available for each contraction.
Changes in muscle architecture during lengthening
contractions. During eccentric muscle actions, the TA
muscle fascicles contracted quasi-isometrically. Penna-
tion angles during eccentric contractions were reduced
compared with those during isometric contraction. Both
fascicle length and pennation angle were independent of
angular velocity during eccentric contractions (Fig. 3, A
and B, respectively). The quasi-isometric behavior of fas-
cicles during eccentric muscle actions reveals an impor-
tant role for the SEC in acting as a mechanical buffer
during this type of contraction. This may be an important
factor for preventing injury to muscle fibers during rapid,
high-force eccentric contractions. Because most of the
elongation appears to occur at the expense of the tendon,
this has important implications for energy saving during
locomotion. During ground impact, energy is stored in
lengthening tendons as strain energy, which is then re-
leased during the subsequent tendon recoil, permitting
J Appl Physiol • VOL
1095
metabolic energy saving (2). In agreement with the find-
ings of the present study, fascicles of the GM muscle have
been identified to contract quasi-isometrically during the
eccentric support phase of walking (10). It has been
shown by Kawakami et al. (21) that, during the eccentric
phase of a countermovement jump, the GM muscle fas-
cicles contracted isometrically, whereas the tendon is
suggested to have lengthened, thus storing elastic energy
that resulted in a force enhancement on plantarflexion
above that found in the same action performed with no
countermovement. Cat muscle fibers have been identified
to actually shorten as the muscle-tendon unit continues
to lengthen during the eccentric phase of gait (14). In
contrast to the findings of the present study, vastus
lateralis muscle fascicles have been reported to initially
contract isometrically, but then to lengthen during the
subsequent phase of an eccentric muscle action (18).
These contrasting findings, however, might represent
differences between the muscles and joint systems stud-
ied. The biochemical fiber type composition of the TA
muscle is thought to be relatively unimportant in ex-
Downloaded from jap.physiology.org on April 23, 2010
plaining the results of the present study, given that
mathematical modeling has revealed a dominance of ar-
chitectural over fiber-type effects in determining muscle
function (1). Changing the level of preactivation in eccen-
tric contractions has been shown to affect not only the
force produced but also the length of fascicles (18). In
vitro studies on isolated fibers suggest that the develop-
ment of an isometric tension is necessary before any
change in length, to ensure full preactivation (4–6). It is
clear, therefore, that the preactivation status of the mus-
cle is an important factor influencing both force and the
behavior of fascicles during the subsequent eccentric con-
traction. In the present study, the eccentric contraction
was preceded by a maximal concentric contraction but
more importantly by an isometric phase, which ensured
that the preactivation level was maximal and further-
more that it remained constant across angular velocities.
The finding that both force and iEMG activity of the TA
muscle remained relatively constant across eccentric an-
gular velocities adds further support to this point.
Changes in muscle thickness with shortening and
lengthening contractions. The distance between aponeu-
roses (averaged over all angular velocities) at a constant
ankle joint angle was significantly greater during eccen-
tric compared with during concentric contraction. The
smaller distance between aponeuroses during concentric
contractions may be a consequence of the smaller penna-
tion angles and greater fascicle lengths at higher angular
velocities, creating an elongated muscle. Elastic deforma-
tion of a constant volume can only occur if more than one
side is elastic (7); therefore, if the muscle becomes longer
it also becomes thinner. Greater muscle length and a
reduced muscle thickness at the same ankle joint angle
during concentric contractions of increasing angular ve-
locity may therefore explain the smaller distance be-
tween the aponeuroses compared with during eccentric
contractions. Because the TA muscle does not act solely
in a sagittal plane, this may result in scanning the mus-
cle from a slightly different orientation, resulting in the
appearance of an increased distance between aponeuro-
95 • SEPTEMBER 2003 • www.jap.org
1096 BEHAVIOR OF MUSCLE FASCICLES IN DYNAMIC CONTRACTIONS
ses. However, great care was taken to scan the muscle
along the sagittal plane of the fascicles so that in each
image the entire visible length of the fascicles could be
tracked.
In conclusion, the present study has demonstrated that
at a constant ankle joint position fascicle length of the TA
muscle increases curvilinearly during concentric contrac-
tions of increasing angular velocity, with a concomitant
curvilinear decrease in pennation angle. These architec-
tural features appear to be modified during shortening
contractions, according to the force being applied to ex-
tend the SEC. The TA muscle fascicles were observed to
contract quasi-isometrically during eccentric muscle ac-
tions, independent of angular velocity. Pennation angles
during eccentric contractions were smaller compared
with those during isometric contraction but were inde-
pendent of angular velocity. The present study shows
that inferences regarding fascicle length during dynamic
contractions of different angular velocities cannot be as-
sumed solely from joint angle.
We express appreciation to Panorea Politi for help with the testing
in this study.
DISCLOSURES
This study was partly supported by Italian Space Agency (ASI)
funds.
REFERENCES
1. Burkholder TJ, Fingado B, Baron S, and Lieber RL. Rela-
tionship between muscle fiber types and sizes and muscle archi-
tectural properties in the mouse hindlimb. J Morphol 221: 177–
190, 1994.
2. Cavagna GA, Heglund NC, and Taylor CR. Mechanical work
in terrestrial locomotion: two basic mechanisms for minimizing
energy expenditure. Am J Physiol Regul Integr Comp Physiol
233: R243–R261, 1977.
3. Desplantez A and Goubel F. In vivo force-velocity relation of
human muscle: a modelling from sinusoidal oscillation behav-
iour. J Biomech 35: 1565–1573, 2002.
4. Edman KA, Elzinga G, and Noble MI. Enhancement of me-
chanical performance by stretch during tetanic contractions of
vertebrate skeletal muscle fibres. J Physiol 281: 139–155, 1978.
5. Edman KA. The velocity of unloaded shortening and its relation
to sarcomere length and isometric force in vertebrate muscle
fibres. J Physiol 291: 143–159, 1979.
6. Edman KA, Elzinga G, and Noble MI. Further characteriza-
tion of the enhancement of force by stretch during activity in
single muscle fibres of the frog. J Physiol 280: 35P–36P, 1978.
7. Ettema GJC and Huijing PA. Architecture and elastic prop-
erties of the series elastic element of muscle-tendon complex. In:
Multiple Muscle Systems: Biomechanics and Movement Organi-
sation, edited by Winters JM and Woo SL-Y. New York: Spinger-
Verlag, 1990.
8. Finni T, Ikegawa S, and Komi PV. Concentric force enhance-
ment during human movement. Acta Physiol Scand 173: 369–
377, 2001.
9. Fukunaga T, Ichinose Y, Ito M, Kawakami Y, and
Fukashiro S. Determination of fascicle length and pennation in
a contracting human muscle in vivo. J Appl Physiol 82: 354–358,
1997.
10. Fukunaga T, Kubo K, Kawakami Y, Fukashiro S, Kanehisa
H, and Maganaris CN. In vivo behaviour of human muscle
tendon during walking. Proc R Soc Lond B Biol Sci 268: 229–
233, 2001.
11. Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Day MK,
Lee PL, Kwong-Fu H, and Edgerton VR. Physiological cross-
sectional area of human leg muscles based on magnetic reso-
nance imaging. J Orthop Res 10: 928–934, 1992.
J Appl Physiol • VOL 95 • SEPTEMBER 2003 •
12. Fukunaga T, Roy RR, Shellock FG, Hodgson JA, and Ed-
gerton VR. Specific tension of human plantar flexors and dor-
siflexors. J Appl Physiol 80: 158–165, 1996.
13. Gans C and Bock WJ. The functional significance of muscle
architecture—a theoretical analysis. Ergeb Anat Entwicklungs-
gesch 38: 115–142, 1965.
14. Griffiths RI. Shortening of muscle fibres during stretch of the
active cat medial gastrocnemius muscle: the role of tendon com-
pliance. J Physiol 436: 219–236, 1991.
15. Henriksson-Larsen K, Wretling ML, Lorentzon R, and
Oberg L. Do muscle fibre size and fibre angulation correlate in
pennated human muscles? Eur J Appl Physiol 64: 68–72, 1992.
16. Herbert RD and Gandevia SC. Changes in pennation with
joint angle and muscle torque: in vivo measurements in human
brachialis muscle. J Physiol 484: 523–532, 1995.
17. Ichinose Y, Kawakami Y, Ito M, Kanehisa H, and Fuku-
naga T. In vivo estimation of contraction velocity of human
vastus lateralis muscle during “isokinetic” action. J Appl Physiol
88: 851–856, 2000.
18. Ikegawa S, Finni T, and Komi PV. Effect of pre-activation
level on the force and length of muscle in eccentric actions. In:
Proceedings of the 5th Annual Congress of the European College
of Sport Science, edited by Avela J, Komi PV and Komulainen J.
Jyvaskyla, Finland: Gummerus Kirjapaino Oy, 2000, p. 342.
19. Jewell BR and Wilkie DR. An analysis of the mechanical
Downloaded from jap.physiology.org on April 23, 2010
components in frog’s striated muscle. J Physiol 143: 515–540,
1958.
20. Kawakami Y, Abe T, and Fukunaga T. Muscle-fiber penna-
tion angles are greater in hypertrophied than in normal muscles.
J Appl Physiol 74: 2740–2744, 1993.
21. Kawakami Y, Muraoka T, Ito S, Kanehisa H, and Fuku-
naga T. In vivo muscle fibre behaviour during counter-move-
ment exercise in humans reveals a significant role for tendon
elasticity. J Physiol 540: 635–646, 2002.
22. Kuno S and Fukunaga T. Measurement of muscle fibre dis-
placement during contraction by real-time ultrasonography in
humans. Eur J Appl Physiol 70: 45–48, 1995.
23. Maganaris CN and Baltzopoulos V. Predictability of in vivo
changes in pennation angle of human tibialis anterior muscle
from rest to maximum isometric dorsiflexion. Eur J Appl Physiol
79: 294–297, 1999.
24. Maganaris CN, Baltzopoulos V, and Sargeant AJ. In vivo
measurements of the triceps surae complex architecture in man:
implications for muscle function. J Physiol 512: 603–614, 1998.
25. Maganaris CN and Paul JP. Load-elongation characteristics
of in vivo human tendon and aponeurosis. J Exp Biol 203:
751–756, 2000.
26. Maganaris CN, Baltzopoulos V, and Sargeant AJ. Differ-
ences in human antagonistic ankle dorsiflexor coactivation be-
tween legs; can they explain the moment deficit in the weaker
plantarflexor leg? Exp Physiol 83: 843–855, 1998.
27. Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, and
Cerretelli P. In vivo human gastrocnemius architecture with
changing joint angle at rest and during graded isometric con-
traction. J Physiol 496: 287–297, 1996.
28. Rack PM. The behaviour of a mammalian muscle during sinu-
soidal stretching. J Physiol 183: 1–14, 1966.
29. Rugg SG, Gregor RJ, Mandelbaum BR, and Chiu L. In vivo
moment arm calculations at the ankle using magnetic resonance
imaging (MRI). J Biomech 23: 495–501, 1990.
30. Thompson CW and Floyd RT. Manual of Structural Kinesiol-
ogy. Dubuque, IA: WCB/McGraw-Hill, 1998.
31. Wickiewicz TL, Roy RR, Powell PL, Perrine JJ, and Ed-
gerton VR. Muscle architecture and force-velocity relationships
in humans. J Appl Physiol 57: 435–443, 1984.
32. Wickiewicz TL, Roy RR, Powell PL, and Edgerton VR.
Muscle architecture of the human lower limb. Clin Orthop:
275–283, 1983.
33. Wilkie DR. Muscle. London: Edward Arnold, 1968.
34. Zipp P. Recommendations for the standardization of lead posi-
tions in surface electromyography. Eur J Appl Physiol 50: 41–54,
1982.
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