BJMB
Brazilian Journal of Motor Behavior
Research Articles
!
Fontana, Herzog
2023
VOL.17
N.5
238 of 245
Fascicle shortening upon activation in voluntary human muscle contractions
HEILIANE DE BRITO FONTANA
1,2
| WALTER HERZOG
2
1
Morphological Sciences Department, Federal University of Santa Catarina, Florianopolis, SC, Brazil
2
Human Performance Laboratory, University of Calgary, Calgary, Canada
Correspondence to: Heiliane de Brito Fontana.
email: heiliane.fontana@ufsc.br
https://doi.org/10.20338/bjmb.v17i5.380
HIGHLIGHTS
• VL fascicle shortening as a function of activation/force
depends crucially on muscle length.
• Fascicle shortening results from a compromise between
the force generating potential of the muscle and muscle
elasticity at different lengths.
• Fascicle kinematics cannot easily be estimated from
joint angle and activation.
ABBREVIATIONS
EMG Electromyography
MTU Muscle tendon unit
MVC Maximal voluntary contraction
RMS Root mean square
VL Vastus lateralis
PUBLICATION DATA
Received 25 07 2023
Accepted 29 09 2023
Published 30 09 2023
BACKGROUND: The dependence of fascicle length on complex interactions with joint angle
and force challenges the interpretation of in vivo joint mechanics, muscle mechanical
properties, contractile behavior, and muscle function.
AIM: The purpose of this study was to determine the complex interaction between muscle
activation, joint angle, and fascicle length for isometric contractions of the human vastus
lateralis muscle (VL).
METHOD: Knee extensor torques, joint angles, EMG activation, and fascicle lengths were
determined in nine healthy subjects during maximal and submaximal isometric contractions.
RESULTS: Fascicle shortening during isometric contractions depended on muscle-tendon
unit length/joint angle and activation, reaching a maximum between angles where VL had its
maximum force potential and minimum resistance to fascicle shortening. Maximal fascicle
shortening shifted to shorter muscle-tendon unit lengths with decreasing activation.
CONCLUSION: Fascicle shortening upon activation depends crucially on the force generating
potential and stiffness of the muscle and can reach 30% of the resting fascicle length. Not
accounting for the complex interactions between muscle length, force potential, muscle
structure, and muscle stiffness has led to erroneous interpretations of the function and
properties of healthy and diseased muscles.
KEYWORDS: Series elasticity | Muscle properties | Isometric contraction | Force-length |
Force-velocity | In vivo muscle function | Muscle work
INTRODUCTION
Muscle tendon unit (MTU) length changes can be derived easily from joint angular excursion, if the instantaneous moment arm
is known
1
. In contrast, length changes of fascicles and fibers depend heavily on complex interactions between muscle architecture,
activation, and the force-dependent elongation of series elastic elements
2–6
. Muscle structure, such as the pennation angle and fascicle
length, change during activation and force production, even when the contraction is “isometric” on the MTU level
7
.
This dependence of fascicle length on complex interactions with several factors challenges the interpretation of in vivo joint
mechanics, muscle mechanical properties, contractile behavior, and muscle function. One could make an argument that contraction types
– concentric, eccentric and isometric - should be defined on the contractile element (fibre/fascicle) level since it is the contractile
element’s conditions (length, rate of change in length, and history of length changes) that affect the basic muscle properties (force-length
relationship
8
, force-velocity relationship
9
, and history-dependent relationships
10
).
A further complication in understanding fascicle mechanics during voluntary contractions is that activation, muscle length/joint
angle, and series elasticity interact and affect fascicle lengths in a complex way. There are at least two factors that need to be considered
when determining fascicle mechanics from joint kinematics: (i) the force potential of muscles, and therefore the capacity to stretch series
elastic elements, depends on the joint angle
11–13
, and (ii) the passive resistance to fascicle shortening also depends on joint configuration
because of differences in stiffness and slackness of elastic elements across the operating range of the muscle
14–16
.
However, despite the obvious importance of knowing fascicle, and thus contractile element lengths, little systematic work has
been done to determine the interactions between muscle lengths/joint angle, force potential, muscle structure, and muscle stiffness that
affect fascicle shortening properties and in vivo behavior.
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
De Brito Fontana,
Herzog
2023
VOL.17
N.5
239 of 245
Research Articles
The purpose of this study was to determine the interaction between EMG activation, joint angle, and fascicle length for in vivo
isometric contractions of the human vastus lateralis muscle (VL). We hypothesized that a given level of activation produces different
amounts of fascicle shortening depending on knee joint angle, and that the amount of fascicle shortening is greatest in the mid-range of
knee motion, somewhere between the joint angles where VL force is greatest and resistance to fascicle shortening is smallest.
METHODS
Nine subjects (7 male and 2 female) took part in this study. Subjects gave written, informed consent to participate in this
research, and all procedures were approved by the University of Calgary’s Conjoint Health Research Ethics Board. The subjects were
recreational athletes participating in sports such as running, swimming or soccer. Mean±SD age, height and weight were 27±3 years,
1.76±0.13 m and 69±15 kg, respectively. The maximal and submaximal fascicle force-length relationships obtained from this study have
been published previously
11
.
Knee extensor torques and knee joint angles were measured on a Biodex II dynamometer (Biodex Medical Systems, Inc.,
Shirley, NY). Subjects were seated with the back supported and the hip joint flexed at 80˚. Straps across the shoulders, waist and thigh
were used to stabilize subjects and isolate the action of the knee extensor muscles. The lower limb was positioned until the knee joint
rotational axis was aligned with the axis of the dynamometer arm throughout the entire range of motion. Full knee extension was defined
as 180 degrees. The tibia was strapped to the dynamometer arm 3 cm proximal to the lateral malleolus.
Surface EMG was recorded from VL using bipolar electrodes (Norotrode 20™, inter electrode spacing 22 mm). The skin was
shaved and cleaned with alcohol before placing the electrodes approximately two-thirds along a line from the anterior superior iliac spine
to the proximal end of the patella. A ground electrode was placed on the tibial tuberosity. Skin impedance was checked and pronounced
acceptable once it was less than 5 kΩ. EMG, torque and joint position were recorded at 1000 Hz using the Windaq data acquisition
system (Dataq Instruments, Akron, OH).
VL fascicles were imaged at 37-49 Hz using a 12.5-MHz linear array ultrasound probe (50mm, Philips Envisor, Philips
Healthcare, Eindhoven, The Netherlands). The ultrasound probe was attached to the skin on the lateral mid-thigh region using a custom-
built holder and was supported by the examiner during testing. Probe orientation and location were adjusted until the best image of VL
fascicles was obtained. An external function generator (B-K Precision 3010, Dynascan Corp., Chicago, IL) was used for synchronization
of all signals.
Knee joint angle, VL EMG activity, and VL mid-portion fascicle lengths were obtained continuously. The ultrasound images
were also used to determine the distance between the deep and superficial aponeuroses and the angle pennation using freely available
software (MicroDicom version 0.7.8). When fascicles were not visible along their entire lengths, fascicle lengths (Fl) were calculated using
standard trigonometry
11
. Fascicles were assumed to be straight lines and an error of 2-7% has been ascribed to this assumption
17–21
.
Subjects executed a standard warm up consisting of ten submaximal knee extension and flexion repetitions. For the actual
testing, subjects performed two maximum isometric knee extensor contractions at ten different knee angles (from 80° to 170° at 10°
increments) in a randomized order, and the trial with the greater torque was used for analysis. Subjects were asked to build up to the
maximal torque over 5 seconds and then hold the maximal torque for another 2 seconds. Verbal encouragement and visual feedback of
the knee extensor torque were provided during all contractions. A rest period of at least 2 min was strictly enforced and was extended
upon a subject’s request.
Knee angle, EMG, fascicle length, and torque were exported to Microsoft Office Excel (Microsoft Corp. Redmond, WA) and
analyzed using Matlab (Math-Works, Natick, MA). Root mean square values (RMS) of the EMG signal were calculated (100 ms window)
throughout the entire contraction. Patellar tendon moment arms were calculated using the regression equation defined by Herzog and
Read
22
. Knee extensor force was calculated by dividing torque by the patellar tendon moment arm. VL force was approximated by
multiplying the total knee extensor force by 0.34
23
.
Fascicle lengths at 0 to 100% of maximum activation (in 10% increments, normalized to the maximum EMG at each knee
angle), and at 10, 20, and 30% of the maximum force at optimal length were determined at all knee angles. Mean fascicle shortening as a
function of activation and force was then calculated across all joint angles.
The interaction between activation and joint angle on fascicle lengths were analyzed based on a repeated measures ANOVA
comparing fascicle shortening (passive – active) across the 10 different angles (α=0.05). The effect of activation was further analyzed
using regression analyses relating fascicle lengths and activation at long (80˚ knee angle), mid-range (130˚), and short muscle lengths
(170˚).
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
De Brito Fontana,
Herzog
2023
VOL.17
N.5
240 of 245
Research Articles
RESULTS
Mean VL fascicle lengths ranged from 13.5±1.2 cm for passive VL at its longest position to 6.3±0.7 cm at maximum activation
and its shortest position. VL maximal force production varied from approximately 523 N at 170° of knee extension to an optimal force
production of 1588 N at 100° of knee extension. For contractions producing the same level of force, fascicle shortening was greater at
more extended knee positions, and consequently shorter VL MTU, compared to more flexed knee positions and longer muscle lengths.
The solid lines in Figure 1 show the mean values for fascicle shortening at 10% and 30% of MVC at the optimal knee joint angle. The
dashed line shows the maximum VL force angle curve shape.
The effect of activation on fascicle length (passive – active) was significantly different across joint angles (F = 2.651; p = 0.048).
For a given activation, fascicle shortening was greatest in the mid-range, decreasing towards the flexed and extended knee joint angles
(Figure 1, columns).
Figure 1. Fascicle shortening at different levels of activation and different knee joint angles (180° =full knee extension = shortest VL length). Fascicle shortening was
greatest in the mid-range of knee joint angles because of the interaction between muscle force generating potential at the different joint angles/MTU lengths (illustrated by
the VL force angle relationship - dashed line) and the decrease in resistance to fascicle shortening at more extended knee angles/short MTU Lengths (as illustrated by the
increase in fascicle shortening for a given amount of force: solid lines, triangles = 30% of MVC force and squares = 10% of MVC force). In addition, fascicle shortening for
10% increments in activation were greater at low compared to high levels of activation, especially at the more extended knee positions/short MTU lengths. Values are
means across subjects and error bars represent standard errors of the mean for the total fascicle shortening distances for the full activation conditions.
Fascicle lengths decreased at all joint angles as activation increased. Since the effect of activation on fascicle shortening was
shown to depend on joint angle, regression analyses of activation-dependent absolute fascicle lengths were performed separately at an
intermediate length (knee angle of 130°) and at the longest (80°) and shortest VL lengths (170°) (Table 1).
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
De Brito Fontana,
Herzog
2023
VOL.17
N.5
241 of 245
Research Articles
Table 1. Summary results of stepwise multiple regression analysis with normalized activation (0-100%) as a factor determining absolute fascicle length
in cm for VL at an intermediate (130°), the longest (80°), and the shortest VL length (170°). ∆Predicted refers to maximum and minimum predicted
values of fascicle length during isometric contractions at each angle. The constant value indicates the predicted values of VL fascicle length in the
passive state.
Factor
80° KNEE ANGLE
130° KNEE ANGLE
170° KNEE ANGLE
R
2
B(SE)
β
R
2
B(SE)
β
R
2
B(SE)
Β
Constant
12.7
(0.2) cm
10.1
(0.3) cm
8.4
(0.2) cm
activation
0.16
-0.016
(0.004)
-0.392
*
0.27
-0.028
(0.005)
-0.517
*
0.41
-0.046
(0.010)
-1.330
*
activation
2
non-significant p = 0.333
non-significant p = 0.084
0.45
2.36E-4
(9.3E-5)
0.715
*
∆Predicted
[12.7 cm to 11.1 cm]
13% of max. shortening
[10.1 cm to 7.3 cm]
28% of max. shortening
[8.4 cm to 6.2 cm]
26% of max. shortening
*
p<0.05 SE = standard error
From Table 1 the following equations can be used to relate activation and fascicle length (cm) at 80°, 130°, and 170° degrees,
respectively.
!
!
!
A negative linear correlation was observed between activation and fascicle shortening at a knee angle of 80˚ and 130˚ with
16% and 27% of the absolute fascicle length variability explained by changes in activation (equation I, p <0.001, equation II, p<0.001).
For the most extended knee position, a quadratic relationship was obtained, indicating that changes in fascicle lengths upon activation
were greatest for the lowest level of activation (from 0-10% of activation), and then decreased continuously with increasing activation. At
this angle, 41% of the total variability in fascicle length was explained by changes in activation (equation III, p = 0.013).
DISCUSSION
Fascicle lengths and fascicle length changes in an activated muscle at a given joint angle/MTU length depend primarily on the
force produced by fascicles and the resistance to fascicle shortening. We analyzed this relationship systematically for VL based on
measurements of fascicle length and fascicle length change for the entire range of activation and for the physiologically relevant MTU
lengths/joint angles. We also quantified the amount of fascicle shortening for a given absolute force across joint angles to determine the
resistance to fascicle shortening – a measure of elastic element stiffness – as a function of muscle length.
𝐼)#𝐹𝑙
𝑎𝑡 #80°
= −0.016#
(
%𝐸𝑀𝐺
𝑚𝑎𝑥
)
+ 12.67
𝐼𝐼)#𝐹𝑙
𝑎𝑡 #130°
= −0.028#
(
%𝐸𝑀𝐺
𝑚𝑎𝑥
)
+ 10.10
𝐼𝐼𝐼 )#𝐹𝑙
𝑎𝑡 #170°
= 2.36 × 10
−4
(
%𝐸𝑀𝐺
𝑚𝑎𝑥
)
2
− 0.046 ×
(
%𝐸𝑀𝐺
𝑚𝑎𝑥
)
+ 8.44
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
De Brito Fontana,
Herzog
2023
VOL.17
N.5
242 of 245
Research Articles
Resistance to fascicle shortening is caused by muscle elastic elements that become stiffer with increasing MTU lengths.
Therefore, for a given amount of force, one would expect fascicle shortening to be greatest at the shortest MTU length where resistance
is lowest. This result was indeed obtained, with fascicle shortening for a force corresponding to 10% and 30% of the maximal isometric
force at optimal length being 1.3±0.5 and 2.5±1.2 cm respectively at the shortest MTU lengths (Figure 1) and 0.3±0.3 and 0.7±0.6 cm,
respectively at the longest (80˚) MTU length.
Fascicle force depends primarily on activation and on the length of the fascicle in accordance with the force-length relationship.
For VL, the force generating potential (for maximal activation) reaches its maximum at knee angles of 100-110˚ (de Brito Fontana and
Herzog
11
and Figure 1; 180 = full extension). Resistance to fascicle shortening increases continuously with VL elongation, therefore
fascicle shortening upon full activation can be expected to be greatest somewhere between i) the knee angles where VL reaches its
maximum force (100-110˚) and ii) the knee angles where resistance to fascicle shortening is smallest (170˚, Figure 1).
Indeed, fascicle shortening from the passive to the fully activated VL is greatest (2.9-3.0 cm) at knee angles ranging from 130-
150˚ (Figure 1). At the longest VL length, fascicle shortening is a mere 1.5 cm because resistance to shortening is highest and the
maximal VL force is only about 80% of its maximum at optimal length. At the shortest VL lengths, despite resistance to fascicle
shortening being lowest, fascicle shortening is only 2.3cm because VL force is a mere 26% of the maximal force at optimal length. For
optimal conditions, fascicles can shorten by nearly 30% of their resting length during an isometric contraction. Contractions at a knee
angle of 130˚ appear to provide maximal muscle elastic element excursion, while at 100˚ - angle at which maximum force generating
potential is achieved, the elastic elements are likely strained maximally. Maximizing the straining and sliding mechanisms that occur at
the different structural levels of tendons during isometric contractions might be of interest in muscle rehabilitation to prevent the formation
of connective tissue adhesions that are related to injury, aging, and age related diseases
24–27
.
Our results demonstrate that resistance to fascicle shortening in voluntary contractions does not only increase with increasing
muscle length (Figure 1), but also increases with muscle force at a given MTU length/knee joint angle (Table 1 and equation III). The
shortening of fascicles for 10% increments in activation is greatest when the passive muscle is activated to 10% of its maximum (orange
columns height, bottom, Figure 1), and smallest from 90% to 100% of its maximum (pink columns height, top, Figure 1). For example, at
a knee angle of 150˚, fascicle shortening is 9 mm from passive to 10% activation, and then decreases for each 10% increment in
activation until it becomes 1 mm when activation increases from 90 to 100% (Figure 1).
This non-linear effect of activation on fascicle length, observed primarily at the more extended knee positions, may result from
two factors i) a non-linear relationship between activation and force production and ii) a decrease in compliance of the muscle as force
increases. Increases in activation from 0-10% results in a greater increase in force than increases in activation from 90-100%
11
. This
activation-force relationship tends to reduce the amount of shortening at activation levels close to maximum. However, changes in
muscle compliance also play a role. This effect is observed when comparing fascicle shortening at constant force levels. For example, at
a knee angle of 150 degrees, an increase in 10% in force from the passive condition led to 11 mm of fascicle shortening, while an
increase from 20 to 30% of maximum force resulted in 6 mm of shortening only. This change in compliance was observed for short VL
lengths corresponding to knee angles ranging from 130˚ to full extension. For longer VL lengths, elastic element compliance was
constant for forces from 0 to 30% of the maximal force (Figure 1), suggesting that series elastic elements are taught at these knee
positions and have entered the linear region of the force-elongation curve
28
.
The complex interaction between joint angle, activation and fascicle length has not always been considered when determining
the contractile properties and functions of healthy and diseased muscles (e.g.
29–31
). The force-length and force-velocity relationships are
arguably the most important mechanical properties of skeletal muscles, and the key determinants of in vivo human muscle function. Both
these properties depend crucially on the instantaneous length and velocity of the contractile elements which can be approximated by the
instantaneous fibre/fascicle length and velocity
8,9
. Often, these instantaneous fibre/fascicle contractile conditions are represented by the
joint angle or MTU length and velocity, despite strong evidence that this can lead to vast errors (e.g.
11,19,32,33
). This manner of estimating
fascicle lengths may be a key reason why force predictions based on musculoskeletal models often fail to provide accurate results when
compared to actual muscle force measurements in animal models
34–36
.
The term “isometric”, used for contractions in which the MTU length is kept constant, cannot be assumed to reflect the
contractile status of VL fascicles/fibres, as fibres under these conditions can shorten by as much as 30% of their passive length. The
analysis of fascicle length during contractions in humans is typically performed using ultrasound imaging, since other medical imaging
techniques (such as magnetic resonance imaging and computed tomography) cannot be used to measure dynamic changes in muscle
architecture during contraction. Our findings are in agreement with the earliest ultrasound studies in the triceps surae muscles
37,38
and
vastus lateralis
39
, that demonstrated substantial shortening during maximal isometric contractions. They are also in agreement with a
more recent systematic analysis on the tibialis anterior muscle, which showed that fascicle shortening during maximal contractions was
greatest at an angle (0 degrees of ankle plantarflexion) that allowed the muscle to work on the ascending limb of the force-length
relationship, where series elastic resistance is small. In the current study, we observed a similar behavior: maximal fascicle shortening
occurred at a knee angle more extended (muscle shorter) than the optimal angle (MTU length) for force production: However, by
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
De Brito Fontana,
Herzog
2023
VOL.17
N.5
243 of 245
Research Articles
exploring a wide range of muscle lengths on the ascending limb of the force-length relationship, we observed that maximal fascicle
shortening occurred not at the shortest muscle length but was greatest in the mid-range (28% of fascicle shortening at a knee angle of
130°) and decreased towards more flexed (13% at 80°) and extended knee joint angles (26% at 170°).
The complexity of the relationship between fascicle length and muscle compliance discussed above for the vastus lateralis
muscle increases dramatically when considering dynamic contractions
19,32,40
. In general, the relative velocity of fibre/fascicle shortening
can be much greater when force increases compared to when force decreases during isokinetic testing. In the human VL, fascicle
shortening velocities can exceed that of the MTU when force is increasing, and can be as low as 20% of the MTU shortening velocity
when force is decreasing
32
. Future work should concentrate on investigating the interplay between muscle architecture, muscle
compliance, and the dynamics of fascicles during contractions at various shortening and lengthening velocities. Exploring the concept of
muscle gearing
6
can aid in differentiating between the effects of series elasticity within the tendon and the complex dynamics of the
muscle belly on fascicle length. Conducting such studies in animal models that permit the measurement of individual muscles forces
would also offer valuable insights into how muscles work and generate force when activated within a synergistic group
41
.
The non-invasive investigation of muscle mechanics using the described setup has limitations that need to be kept in mind
when interpreting our results
42,43
. We assumed that VL’s relative force contribution to the total quadriceps force is constant. Also,
antagonistic activation was not accounted for in the calculation of VL force. Although these factors might affect the magnitude, we would
not expect them to affect the shape of the VL force-angle curve substantially, which is a main determinant of the fascicle shortening
features discussed in this study. Fascicle shortening occurs in a 3D manner
44,45
. Even though the absolute values of fascicle shortening
must be considered with this limitation in mind, we do not expect them to affect the fundamental results of this study, or the effect
expressed in the regression equations.
CONCLUSION
We conclude from the results of this study that VL fascicle shortening as a function of activation/force depends crucially on
muscle length and is not maximal at the angle where maximum force is achieved. Rather, the amount of fascicle shortening results from
a compromise between the force generating potential of the muscle and the resistance to shortening imposed by muscle elasticity at
different lengths. Consequently, force cannot easily be estimated from fascicle kinematics, and fascicle lengths should not be derived
from passive measurements and muscle lengths alone.
REFERENCES
1. Grieve DW, Pheasant S, Cavanagh PR. Prediction of gastrocnemius length from knee and ankle joint posture Vol 2a. In: Assmussen E,
Jorgensen K, eds. International Series on Biomechanics,. University Park Press; 1978:405-412.
2. Griffiths RI. Ultrasound transit time gives direct measurement of muscle fibre length in vivo. J Neurosci Methods. 1987;21:159-165.
doi:10.1016/0165-0270(87)90113-0
3. Fukunaga T, Kubo K, Kawakami Y, Fukashiro S, Kanehisa H, Maganaris CN. In vivo behaviour of human muscle tendon during walking. Proc
R Soc B Biol Sci. 2001;268(May 2000):229-233. doi:10.1098/rspb.2000.1361
4. Finni T. Structural and functional features of human muscle-tendon unit. Scand J Med Sci Sports. 2006;16(3):147-158. doi:10.1111/j.1600-
0838.2005.00494.x
5. Kawakami Y, Muraoka T, Ito S, Kanehisa H, Fukunaga T. In vivo muscle fibre behaviour during counter-movement exercise in humans
reveals a significant role for tendon elasticity. J Physiol. 2002;540(2):635-646. doi:10.1113/jphysiol.2001.013459
6. Azizi E, Brainerd EL, Roberts TJ. Variable gearing in pennate muscles. Proc Natl Acad Sci U S A. 2008;105(5):1745-1750.
doi:10.1073/pnas.0709212105
7. Ito M, Kawakami Y, Ichinose Y, Fukashiro S, Fukunaga T. Nonisometric behavior of fascicles during isometric contractions of a human
muscle. J Appl Physiol. 1998;85(4):1230-1235. Accessed May 18, 2017. http://www.ncbi.nlm.nih.gov/pubmed/9760310
8. Gordon AM, Huxley AF, Julian FJ. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol.
1966;184(1):170-192. doi:5921536
9. Hill a. VA. The Heat of Shortening and the Dynamic Constants of Muscle. Proc R Soc B Biol Sci. 1938;126(843):136-195.
doi:10.1098/rspb.1938.0050
10. Abbott BC, Aubert XM. The force exerted by active striated muscle during and after change of length. J Physiol. 1952;117(1):77-86. Accessed
June 28, 2017. http://www.ncbi.nlm.nih.gov/pubmed/14946730
11. de Brito Fontana H, Herzog W. Vastus lateralis maximum force-generating potential occurs at optimal fascicle length regardless of activation
level. Eur J Appl Physiol. 2016;116(6). doi:10.1007/s00421-016-3381-3
12. Kulig K, Andrews J, Hay J. Human strength curves. Exerc Sport Sci Rev. 1984;12(1):417-466. Accessed March 31, 2015.
http://journals.lww.com/acsm-essr/Abstract/1984/01000/Human_Strength_Curves.14.aspx
13. Ichinose Y, Kawakami Y, Ito M, Fukunaga T. Estimation of Active Force-Length Characteristics of Human VL muscle. Acta Anat (Basel).
1997;159:78-83.
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
De Brito Fontana,
Herzog
2023
VOL.17
N.5
244 of 245
Research Articles
14. Kawakami Y, Ichinose Y, Fukunaga T. Architectural and functional features of human triceps surae muscles during contraction. J Appl
Physiol. 1998;85:398-404.
15. Vaz MA, de la Rocha Freitas C, Leonard T, et al. The force-length relationship of the cat soleus muscle. Muscles Ligaments Tendons J.
2012;2(2):79-84. Accessed February 28, 2015.
http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3666510&tool=pmcentrez&rendertype=abstract
16. O’Brien T, Reeves N, Baltzopoulos V. Mechanical properties of the patellar tendon in adults and children. J. Published online 2010. Accessed
June 13, 2017. http://www.sciencedirect.com/science/article/pii/S0021929009006770
17. Ando R, Taniguchi K, Saito A, Fujimiya M, Katayose M, Akima H. Validity of fascicle length estimation in the vastus lateralis and vastus
intermedius using ultrasonography. J Electromyogr Kinesiol. 2014;24(2):214-220. doi:10.1016/j.jelekin.2014.01.003
18. Earp JE, Newton RU, Cormie P, Blazevich AJ. The influence of loading intensity on muscle-tendon unit behavior during maximal knee
extensor stretch shortening cycle exercise. Eur J Appl Physiol. 2014;114:59-69. doi:10.1007/s00421-013-2744-2
19. Finni T, Ikegawa S, Lepola V, Komi PV V. Comparison of force-velocity relationships of vastus lateralis muscle in isokinetic and in stretch-
shortening cycle exercises. Acta Physiol Scand. 2003;177(4):483-491. doi:10.1046/j.1365-201X.2003.01069.x
20. Ishikawa M, Finni T, Komi P V. Behaviour of vastus lateralis muscle-tendon during high intensity SSC exercises in vivo. Acta Physiol Scand.
2003;178:205-213. doi:10.1046/j.1365-201X.2003.01149.x
21. Kwah LK, Pinto RZ, Diong J, Herbert RD. Reliability and validity of ultrasound measurements of muscle fascicle length and pennation in
humans: a systematic review. J Appl Physiol. 2013;114:761-769. doi:10.1152/japplphysiol.01430.2011
22. Herzog W, Read LJ. Lines of action and moment arms of the major force-carrying structures crossing the human knee joint. J Anat.
1993;182(2):213-230. Accessed November 4, 2015.
http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1259832&tool=pmcentrez&rendertype=abstract
23. Akima H, Kuno S, Fukunaga T, Katsuta S. Architectural properties and specific tension of human knee extensor and flexor muscles based on
magnetic resonance imaging. Japanese J Phys Fit Sport Med. 1995;44(2). doi:10.7600/jspfsm1949.44.267
24. Sharma P, Maffulli N. Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact. 2006;6(2):181-190.
Accessed June 29, 2017.
https://www.researchgate.net/profile/Nicola_Maffulli/publication/6935766_Biology_of_tendon_injury_Healing_modeling_and_remodeling/links/0deec5210
64a90f144000000.pdf
25. Li Y, Fessel G, Georgiadis M, Snedeker JG. Advanced glycation end-products diminish tendon collagen fiber sliding. Matrix Biol. 2013;32(3-
4):169-177. doi:10.1016/j.matbio.2013.01.003
26. James R, Kesturu G, Balian G, Chhabra AB. Tendon: Biology, Biomechanics, Repair, Growth Factors, and Evolving Treatment Options. J
Hand Surg Am. 2008;33(1):102-112. doi:10.1016/j.jhsa.2007.09.007
27. Ahmad CS, Kwak SD, Ateshian GA, Warden WH, Steadman JR, Mow VC. Effects of Patellar Tendon Adhesion to the Anterior Tibia on Knee
Mechanics. Am J Sports Med. 2016;26(5):715-724. doi:10.1177/03635465980260051901
28. Fukutani A, Misaki J, Isaka T. Relationship between joint torque and muscle fascicle shortening at various joint angles and intensities in the
plantar flexors. Sci Rep. 2017;7(1):290. doi:10.1038/s41598-017-00485-1
29. Arnold AS, Liu MQ, Schwartz MH, ?unpuu S, Dias LS, Delp SL. Do the hamstrings operate at increased muscle?tendon lengths and
velocities after surgical lengthening? J Biomech. 2006;39(8):1498-1506. doi:10.1016/j.jbiomech.2005.03.026
30. Austin N, Nilwik R, Herzog W. In vivo operational fascicle lengths of vastus lateralis during sub-maximal and maximal cycling. J Biomech.
2010;43(12):2394-2399. doi:10.1016/j.jbiomech.2010.04.016
31. Rack PM, Westbury DR. The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J Physiol. 1969;204(2):443-
460. Accessed February 28, 2015. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1351563&tool=pmcentrez&rendertype=abstract
32. de Brito Fontana H, Roesler H, Herzog W. In vivo vastus lateralis force–velocity relationship at the fascicle and muscle tendon unit level. J
Electromyogr Kinesiol. 2014;24(6):934-940. doi:10.1016/j.jelekin.2014.06.010
33. Hauraix H, Nordez A, Dorel S. Shortening behavior of the different components of muscle-tendon unit during isokinetic plantar flexions. J Appl
Physiol. 2013;115(7):1015-1024. doi:10.1152/japplphysiol.00247.2013
34. Herzog W, Leonard TRR. Validation of optimization models that estimate the forces exerted by synergistic muscles. J Biomech. 1991;24:31-
39. doi:10.1016/0021-9290(91)90375-W
35. Prilutsky BI, Herzog W, Allinger TL. Force-sharing between cat soleus and gastrocnemius muscles during walking: explanations based on
electrical activity, properties, and kinematics. J Biomech. 1994;27(10):1223-1235. Accessed July 21, 2017.
http://www.ncbi.nlm.nih.gov/pubmed/7962010
36. Herzog W, Ait-Haddou R. Coordination of One- and Two-Joint Muscles during Voluntary Movement: Theoretical and Experimental
Considerations. Motor Control. 2000;4(1):68-74. doi:10.1123/mcj.4.1.68
37. Narici M V., Binzoni T, Hiltbrand E, Fasel J, Terrier F, Cerretelli P. In vivo human gastrocnemius architecture with changing joint angle at rest
and during graded isometric contraction. J Physiol. 1996;496 ( Pt 1(Pt 1):287-297. doi:10.1113/JPHYSIOL.1996.SP021685
38. Maganaris C. In vivo measurements of the triceps surae complex architecture in man: implications for muscle function. J …. Published online
1998. Accessed January 20, 2016. http://onlinelibrary.wiley.com/doi/10.1111/j.1469-7793.1998.603be.x/full
39. Fukunaga T, Ichinose Y, Ito M, Kawakami Y, Fukashiro S. Determination of fascicle length and pennation in a contracting human muscle in
vivo. J Appl …. 1997;82(1):354-358. Accessed February 26, 2015. http://jap.physiology.org/content/82/1/354.short
40. Nikolaidou ME, Marzilger R, Bohm S, Mersmann F, Arampatzis A. Operating length and velocity of human M. vastus lateralis fascicles during
vertical jumping. R Soc Open Sci. 2017;4(5):1-15. doi:10.1098/RSOS.170185
41. Finni T, de Brito Fontana H, Maas H. Force transmission and interactions between synergistic muscles. J Biomech. 2023;152:111575.
doi:10.1016/j.jbiomech.2023.111575
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
De Brito Fontana,
Herzog
2023
VOL.17
N.5
245 of 245
Research Articles
42. de Brito Fontana H, Han S won, Sawatsky A, Herzog W. The mechanics of agonistic muscles. J Biomech. 2018;79(0):15-20.
doi:10.1016/j.jbiomech.2018.07.007
43. Roberts TJ, Dick TJM. What good is a measure of muscle length? The how and why of direct measurements of skeletal muscle motion. J
Biomech. 2023;157:111709. doi:10.1016/J.JBIOMECH.2023.111709
44. Raiteri BJ, Cresswell AG, Lichtwark GA. Three-dimensional geometrical changes of the human tibialis anterior muscle and its central
aponeurosis measured with three-dimensional ultrasound during isometric contractions. PeerJ. 2016;4:e2260. doi:10.7717/peerj.2260
45. Herbert RD, Héroux ME, Diong J, Bilston LE, Gandevia SC, Lichtwark GA. Changes in the length and three-dimensional orientation of muscle
fascicles and aponeuroses with passive length changes in human gastrocnemius muscles. J Physiol. 2015;593(2):441-455.
doi:10.1113/jphysiol.2014.279166
ACKNOWLEDGMENTS
NSERC of Canada, The Killam Memorial Chair, the Canada Research Chair Programme. CAPES Ministry of Education in Brazil
Citation: de Brito Fontana H, Herzog W. (2023).!Fascicle shortening upon activation in voluntary human muscle contractions. Brazilian Journal of Motor Behavior,
17(5):238-245.
Editor-in-chief: Dr Fabio Augusto Barbieri - São Paulo State University (UNESP), Bauru, SP, Brazil. !
Associate editors: Dr José Angelo Barela - São Paulo State University (UNESP), Rio Claro, SP, Brazil; Dr Natalia Madalena Rinaldi - Federal University of Espírito Santo
(UFES), Vitória, ES, Brazil; Dr Renato de Moraes – University of São Paulo (USP), Ribeirão Preto, SP, Brazil.!
Copyright:© 2023 Fontana and Herzog and BJMB. This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No
Derivatives 4.0 International License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: CAPES Ministry of Education in Brazil
Competing interests: The authors have declared that no competing interests exist.
DOI:!https://doi.org/10.20338/bjmb.v17i5.380