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Clinical Anatomy 16:215–223 (2003

)

ORIGINAL COMMUNICATION

Force-Length Characteristics of the In Vivo Human
Gastrocnemius Muscle
CONSTANTINOS N. MAGANARIS*
Centre for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, Alsager, United Kingdom

In this study, the force-length characteristics of the in vivo medial (GM) and lateral (GL)
heads of the human gastrocnemius muscle were estimated from measurements in eight
healthy male subjects. This involved: 1) dynamometry-based measurements of the moment
generated during maximal isometric plantar flexion; 2) ultrasound-based measurements of
fascicular length and pennation angle; and 3) ultrasound-based calculations of moment arm
lengths. All measurements were taken over the ankle angle range from 20° of dorsiflexion to
30° of plantar flexion. Tendon forces were calculated by dividing the moments recorded by
the muscle moment arm lengths, and fascicular forces were calculated by dividing the tendon
forces estimated by the cosine of pennation angle. In the transition from 30° of plantar flexion
to 20° of dorsiflexion, the GM muscle fascicular length and force increased linearly from 24
to 39 mm and from 222 to 931 N, respectively. Over the same ankle angle range, the GL
muscle fascicular length and force increased linearly from 30 to 47 mm and from 139 to 393
N, respectively. Estimates of the sarcomeric lengths corresponding to the fascicular lengths
measured indicated that the two muscles operated in the range 1.4 –2.2 ␮m, below the optimal
length region for force generation according to the cross-bridge mechanism of contraction.
These results indicate that the force–length relation of the in vivo human gastrocnemius
muscle is limited to the ascending limb of the bell-shaped force–length curve obtained from
experiments on isolated material. Clin. Anat. 16:215–223, 2003. © 2003 Wiley-Liss, Inc.

Key words: ultrasound; length-tension; muscle contraction; moment arm; sar-
comere

INTRODUCTION mechanical behavior of a pennate structure to that of
a parallel-fiber structure (Herzog and ter Keurs,
The classic experiments by Gordon et al. (1966)
1988a,b; Herzog et al., 1991). The assumptions in both
showed that the force–length relation of isolated mus-
cle fibers approximated a bell-shaped pattern. The approaches, however, are clearly unrealistic. The ar-
level of contractile force elicited was related to the chitecture of a muscle changes during contraction due
extent of myofilament overlap in the sarcomere, a to a stretch in the serial tendons and aponeuroses
relationship that gave support to the cross-bridge the- (Narici et al., 1996; Kawakami et al., 1998; Maganaris
ory of contraction introduced by Huxley (1957). et al., 1998; Martin et al., 2001) and the fascicles in a
As opposed to isolated fiber experiments, the op- pennate muscle shorten upon contraction less than
erating length range of muscle fibers under in vivo those in a parallel fiber muscle (for review see Gans,
conditions is confined by the anatomical constraints of 1982). Thus, the force–length relations reported
the skeleton and the architectural features of the mus-
cle. Due to lack of technology for measuring muscular *Correspondence to: Constantinos N. Maganaris, Centre for Bio-
architecture in vivo, determining the force–length physical and Clinical Research into Human Movement, Manches-
characteristics of an intact muscle has necessitated ter Metropolitan University, Alsager ST7 2HL, UK.
either presuming that cadaver-based measurements of E-mail: C.N.Maganaris@mmu.ac.uk
fascicular length and pennation angle are representa- Received 23 November 2001; Revised 19 April 2002
tive of those during muscle contraction (Cutts, 1988) Published online in Wiley InterScience (www.interscience.wiley.
or neglecting pennation effects and approximating the com). DOI 10.1002/ca.10064

© 2003 Wiley-Liss, Inc.
216 Maganaris

should be viewed with caution when referring to in ittal plane. In vitro and in vivo experiments have
vivo muscle function. shown that the lateral side of the tibiotalar joint axis
Ultrasonography, however, has recently made it points downwards and posteriorly by 10° relative to
possible to measure in vivo muscular architecture with the medial side (Isman and Inman, 1969; van den
high accuracy and reproducibility (Narici et al., 1996; Bogert et al., 1994). This geometric arrangement re-
Kawakami et al., 1998; Maganaris et al., 1998). We sults in a triplanar orientation in the moment pro-
used ultrasonography and dynamometry to estimate duced about the tibiotalar joint; however, ankle mo-
the force–length characteristics of the intact human ment measurements in the sagittal plane include only
gastrocnemius muscle. the cosine component of this moment. Trigonometry-
based calculations using the above axis angle values
indicate that the measurable component of moment
MATERIALS AND METHODS accounts for 97% of the entire moment vector. Thus,
Experimental Design the present MVC moment measurements were con-
sidered to be valid.
The force–length relation of the gastrocnemius
muscle of the right limb was examined in eight Measurements of Fascicular Length and
healthy male volunteers (age, 22 ⫾ 2 years; height, Pennation Angle
173 ⫾ 3 cm; and body mass, 75 ⫾ 3 kg; mean ⫾ SD)
with approval from the institutional ethics committee. Fascicular lengths and pennation angles were mea-
Measurements were taken at ankle angles of ⫺20° sured in vivo from sonographs taken during MVCs
(dorsiflexion direction), ⫺10°, 0° (the sole of the foot elicited at the knee extension angle (Narici et al.,
at right angles to the longitudinal axis of the tibia), 1996; Kawakami et al., 1998; Maganaris et al., 1998;
⫹10° (plantar flexion direction), ⫹20°, and ⫹30°. All Martin et al., 2001). A linear-array, 7.5 MHz, B-mode
subjects could passively rotate the foot from ⫹30 to ultrasound probe (Esaote Biomedica, Florence, Italy),
⫺10°, but a slight force was applied externally to bring with width and depth resolutions of 1 mm and 0.62
the foot to ⫺20°. At each ankle angle studied, the mm, respectively, was coated with transmission gel
following parameters were either measured or calcu- and placed over the midlongitudinal axes of the me-
lated: 1) the moment elicited upon isometric plantar dial (GM) and lateral (GL) heads of the gastrocnemius
flexion maximal voluntary contraction (MVC); 2) the muscle, 5 cm above (first and third MVCs) and 5 cm
gastrocnemius muscle fascicular length and pennation below (second and fourth MVCs) the midlength of the
angle; and 3) the gastrocnemius muscle moment arm muscle belly during MVC (Fig. 1). The architecture of
length. the two muscle heads in the above regions has been
shown to be representative of that along and across the
Measurement of MVC Moment muscle belly (Narici et al., 1996; Maganaris et al.,
1998). In the muscle scans recorded, fascicular, inter-
MVC contractions were elicited in the prone posi-
fascicular, and aponeurotic echoes were identified.
tion on the bench of an isokinetic dynamometer (Lido
The criterion adopted for ensuring that the scanning
Active, Loredan Biomedical, Davis, CA). The pivot
point of the dynamometer lever was aligned with the plane coincided with the plane in which the fascicles
lateral malleoli and the foot was firmly secured at the lay was that the echo of the entire fascicular path
dynamometer footplate with Velcro straps. Measure- could be seen in the scans (Narici et al., 1996;
ments were taken after compensating for gravitational Kawakami et al., 1998; Maganaris et al., 1998). This
and passive moments about the ankle. After a warm- criterion was met in most of the scans taken with the
ing up protocol consisting of three submaximal con- scanning head placed in the midsagittal plane of the
tractions, the subjects generated four MVCs with the muscle. If, however, this probe position generated
knee fully extended (0°) and two MVCs with the knee echoes in only a part of the fascicular path, the probe
flexed at 120°. MVCs were elicited randomly for knee was oriented manually to a plane that included the
and ankle angles, and were separated by a 2-min rest. entire length of the fascicles. In each scan, the length
Measurements were repeated until obtaining the of one to three fascicles was digitized using comput-
MVC moments established in a familiarization trial erized image analysis (NIH Image, National Institute
(⫾5%) 2 to 3 days earlier. of Health, Bethesda, MD), taking into account any
Conventional dynamometers record moments in visible curvature along the fascicular path. Pennation
only one plane in each test. In the present experi- angle measurements were taken at the fascicular in-
ment, moment measurements were taken in the sag- sertions in the deep aponeurosis (Fig. 2).
In Vivo Force–Length Characteristics 217

medial and lateral borders of each muscle in each scan
were marked on the skin to identify the midlongitu-
dinal axis of the muscle, which was also drawn on the
skin. The probe was positioned in the sagittal plane
along the midlongitudinal axis of each muscle to lo-
cate the exact position of the myotendinous junction.
The probe was oriented in a plane reflecting clear
echoes and secured with adhesive tape on the skin.
Scans were first recorded having the ankle plantar
flexed by 5° more than the angle at which the moment
arm length was to be obtained (Figs. 2, 3A). The same
procedure was repeated with the ankle plantar flexed
by 5° less, compared to the angle at which the mo-
ment arm length was to be obtained. The displace-
ment dx of the tendon endpoint in each myotendi-
nous junction over the 10°-rotation (d␪) was then
digitized in the scans taken. The absence of medio-
lateral shifts in the gastrocnemius muscle during plan-
tar flexion-dorsiflexion rotation (Fukunaga et al.,
2001) indicates that all dx measurements in each mus-
cle were taken in a single muscular section. The
moment arm lengths of the GM and GL muscles were
calculated from the ratios dx/d␪ (d␪ in rad).
Data Analysis
The moment-producing potential of the gastrocne-
mius muscle at each ankle angle was estimated by
subtracting the MVC moment at the knee flexion
angle from that at the knee extension angle. For each
knee angle, the MVC that generated the highest mo-
Fig. 1. Schematic representation of the ultrasound scanning sites.
The muscle belly shown refers to either of the two muscles examined ment was considered. The above calculation assumes
in the right limb as seen from the back. that at any given ankle angle: 1) the gastrocnemius
muscle is fully active during an MVC with the knee
extended; 2) the biarticular gastrocnemius musculo-
Calculation of the Moment Arm Length tendon unit is slack at a knee flexion angle of 120° and
Moment arm lengths were obtained using the ex- thus it transmits upon MVC negligible contractile
cursion method (An et al., 1984), adapted under in forces to the calcaneus; and 3) the moment produced
vivo conditions as described by Ito et al. (2000) and by other muscles crossing the ankle joint is the same
Maganaris (2000). This method necessitates identify- between MVCs generated at knee angles of 0 and
ing a reference landmark along the action line of the 120°. The validity of the first assumption could be
muscle and measuring displacement of the landmark tested by superimposing electrical current upon the
over a given rotation in the joint that the muscle MVCs carried out, referred to as the “twitch superim-
spans. Because the action lines of the GM and GL position technique” (Belanger and McComas, 1981;
muscles do not coincide and the axis of rotation in the Allen et al., 1995). Unfortunately, we found the appli-
tibiotalar joint is not perpendicular to the sagittal cation of this method in the experimental trial imprac-
plane, separate measurements were taken to quantify tical: placement of stimulating electrodes over the
the displacements of the reference landmarks in the muscle prohibited muscle scanning, and placement of
two muscles. The reference landmark in each muscle stimulating electrodes over the tibial nerve in the
was the end point of the echo generated by the ten- popliteal fossa proved to be ineffective at the knee
don in the distal myotendinous junction of the mus- flexion angle due to loose contact between the elec-
cle. To locate the myotendinous junction, five axial- trodes and the skin. However, to assess whether our
plane sonographs were recorded (with the scanning subjects were capable of activating fully the gastroc-
probe described above) along the central portion of nemius muscle upon volition, the twitch superimpo-
the GM and GL muscle bellies at 2-cm intervals. The sition technique was applied in the familiarization
218 Maganaris

Fig. 2. Left: Typical sonographs 5 cm above the midlength of the medial head of the gastrocnemius muscle; GL, lateral head of the
GM (top) and GL (bottom) muscle bellies at an ankle angle of ⫺20°. gastrocnemius muscle; SOL, soleus muscle; FHL, flexor hallucis lon-
The horizontal white striations are aponeurotic echoes, the oblique gus muscle. Right: Typical sonographs over the medial head of the
white striations are interfascicular echoes, and the oblique black stri- gastrocnemius myotendinous junction at ankle angles of ⫺5° (top) and
ations are fascicular echoes. The superimposed white line at the top ⫹5° (bottom). M, muscle; DA, deep aponeurosis; MTJ, myotendinous
indicates the path of a fascicle between the superficial and deep junction; T, tendon. Note the negligible angulation between the ori-
aponeuroses. ␾, the angle of pennation; SF, subcutaneous fat; GM, entations of the deep aponeurosis and tendon.

trial. For these measurements, twitch doublets of tendon force in a recent study (Arndt et al., 1998);
150 –175 V were applied to the GM and GL muscles however, these measurements were taken in only one
through two self-adhesive rubber electrodes of dimen- subject. More importantly, the authors assumed that
sions 7.5 ⫻ 12.5 cm. Our pilot measurements showed the length of the Achilles tendon moment arm does
no evidence of incomplete motor unit activation dur- not change as a function of muscle-tendon length and
ing MVC. The validity of the second assumption is contraction-state, which later proved to be incorrect
supported by previous EMG-based studies (Hof and (Maganaris et al., 1998).
van den Berg, 1977; Gravel et al., 1987) and by recent The moment contribution of the GM and GL mus-
results showing that knee flexion above 115° yields no cles to the entire gastrocnemius muscle moment was
measurable decrease in the moment generated during obtained from the relative physiological cross-sec-
plantar flexion contraction (Maganaris, 2001). The tional areas of the GM and GL muscles to that of the
third assumption has been discussed in detail by Her- entire gastrocnemius muscle: 70 and 30%, respec-
zog and ter Keurs (1988a) and Herzog et al. (1991): tively (Huijing, 1985; Fukunaga et al., 1992). Tendon
because all the synergists and antagonists of the gas- forces in each muscle were calculated by dividing the
trocnemius muscle span the ankle joint only, their estimated moment by the moment arm length of the
moment contribution to the net MVC moment at any muscle (Fig. 3B). Fascicular forces were estimated by
given ankle angle would not differ between knee representing the muscle as a parallelogram with apo-
angles. This view has been challenged by moment neuroses and tendons operating over the same line
calculations from in vivo measurements of Achilles (Gans, 1982; Cutts, 1988; Narici et al., 1996;
In Vivo Force–Length Characteristics 219

Kawakami et al., 1998; Maganaris et al., 1998). The
fascicular force elicited upon contraction was there-
fore obtained by dividing the tendon force by the
cosine of pennation angle (Fig. 3B). The selection of
the above model as opposed to that developed by
Huijing and Woittiez (1985) was based on visual in-
spection of the aponeuroses and tendons in the scans
taken over the myotendinous junction region (Fig. 2).
Nevertheless, it should be recognized that although
simple unipennate muscle models (with or without an
angle between the tendons and the aponeuroses) are
computationally efficient for estimating changes in
forces when altering muscle length, they are mechan-
ically unstable. Modelling mechanically stable archi-
tectures requires detailed information about the arcs
over which the fascicles and the tendinous sheets
operate (Van Leeuwen and Spoor, 1992), which can-
not be obtained in vivo at present.
Direct measurements on cadaveric human muscles
have previously shown that ultrasonography provides
valid measurements of fascicular length and penna-
tion angle (Kawakami et al., 1993; Narici et al., 1996).
Inter- and intraobserver variations of the scanning
procedures and image analyses involved have been
confirmed to be less than 8% (Maganaris et al., 1998;
Ito et al., 2000; Maganaris, 2000, 2001). In the present
study, all scan morphometrics were carried out three
times and mean values were used for further analysis.
In each muscle, average values of pennation angle
across all fascicles traced and both muscular regions
scanned were considered in the analysis.

RESULTS
Tables 1 and 2 show the measured and calculated
values of the parameters examined. The following
observations can be made from the data shown:

1. The MVC moment at the knee extension angle
Fig. 3. A: Illustration of the method used to estimate moment
was higher by 57– 65% than that at the knee
arm lengths. The lower extremity model shown refers to either of the flexion angle. This difference is in line with
two muscles examined for estimating the moment arm length at the previous results (Sale et al., 1982; Kawakami et
ankle angle of 0° (the sole of the foot at right angles to the longitudinal al., 2000a) and reflects the ineffectiveness of the
axis of the tibia). The excursion dx of the myotendinous junction gastrocnemius musculotendon unit to transmit
(MTJ) in the transition from ⫹5° (top) to ⫺5° (bottom) was measured
in the ultrasound scans taken. This excursion was then divided by the
contractile forces and generate calcaneal dis-
10° (0.175 rad) ankle rotation carried out to obtain the moment arm placements at knee angles above 90° (Hof and
length of the muscle. B: Functional line diagram of the musculoskel- van den Berg, 1977; Gravel et al., 1987; Maga-
etal model used to calculate forces at the ankle angle of 0°. The model naris, 2001).
shown refers to either of the two muscles examined. An MVC gener- 2. Both muscles exhibited similar architectural fea-
ates the fascicular force vector F1, part of which (F2) is transmitted
along the tendon to produce a plantar flexion moment M about the
tures between the two regions scanned, in agree-
ankle. According to the moment equilibrium equation, F2 ⫽ M 䡠 t⫺ 1, ment with previous studies reporting a uniform
where t is the moment arm length of the muscle estimated as shown in geometry along the muscle belly (Narici et al.,
the above panel. According to the vectorial analysis of forces, F1 ⫽ 1996; Maganaris et al., 1998).
F2 䡠 cos⫺1␾, where ␾ is the pennation angle of the muscle. 3. The two muscles exhibited similar patterns of
220 Maganaris

TABLE 1. Parameters Measured as a Function of Ankle Angle*

Ankle angle (degrees)
Dorsiflexion 7 Plantar flexion
⫺20 ⫺10 0 ⫹10 ⫹20 ⫹30
MVC moment at knee extension (Nm) 201 ⫾ 17 191 ⫾ 17 172 ⫾ 15 157 ⫾ 13 117 ⫾ 11 86 ⫾ 8
MVC moment at knee flexion (Nm) 124 ⫾ 11 117 ⫾ 11 109 ⫾ 9 99 ⫾ 8 73 ⫾ 6 52 ⫾ 4
GM muscle fascicular length A (mm) 39 ⫾ 6 34 ⫾ 5 33 ⫾ 5 29 ⫾ 4 28 ⫾ 4 25 ⫾ 3
GM muscle fascicular length B (mm) 39 ⫾ 6 36 ⫾ 5 31 ⫾ 4 30 ⫾ 4 25 ⫾ 4 24 ⫾ 4
GL muscle fascicular length A (mm) 46 ⫾ 7 45 ⫾ 7 41 ⫾ 6 38 ⫾ 5 32 ⫾ 4 28 ⫾ 4
GL muscle fascicular length B (mm) 47 ⫾ 8 44 ⫾ 7 39 ⫾ 6 34 ⫾ 6 33 ⫾ 5 32 ⫾ 4
GM muscle pennation angle A (deg) 30 ⫾ 4 36 ⫾ 5 41 ⫾ 5 45 ⫾ 6 48 ⫾ 7 50 ⫾ 7
GM muscle pennation angle B (deg) 32 ⫾ 5 36 ⫾ 5 43 ⫾ 6 43 ⫾ 6 48 ⫾ 6 53 ⫾ 7
GL muscle pennation angle A (deg) 20 ⫾ 3 24 ⫾ 3 27 ⫾ 4 29 ⫾ 5 31 ⫾ 5 32 ⫾ 5
GL muscle pennation angle B (deg) 22 ⫾ 3 25 ⫾ 4 27 ⫾ 5 30 ⫾ 5 30 ⫾ 5 33 ⫾ 5

*MVC, maximum voluntary contraction; GM and GL, medial and lateral heads of the gastrocnemius muscle, respectively; A and B, 5 cm
above and 5 cm below the midlength of the muscle belly, respectively. Fascicular lengths and pennation angles are average values from
one to three fascicles. Values are mean ⫾ SD (n ⫽ 8).

changes in any given parameter examined as a cles, but the normalized force–length curves were
function of ankle angle, not surprising given that very similar (Fig. 4B), thus indicating that the two
both muscles are anatomic subunits of the same muscles operated over similar relative length regions.
actuator (the gastrocnemius muscle).
4. Neither muscle exerted its maximal force at the
DISCUSSION
ankle angle of 0°, in contrast with the general
notion that skeletal muscles generate maximal Determination of force-length characteristics in in-
forces at neutral anatomical positions (see also tact human muscles has often been attempted; how-
Lieber et al., 1994). ever, the following unrealistic assumptions have been
made: 1) the architecture of cadaveric muscles repre-
The observed changes in all parameters examined sents muscular architecture during contraction (Cutts,
as a function of ankle angle agree with several previ- 1988); 2) pennate muscles behave mechanically like
ous studies (Sale et al., 1982; Rugg et al., 1990; Herzog parallel fiber muscles (Herzog and ter Keurs, 1988b;
et al., 1991; Narici et al., 1996; Kawakami et al., 1998; Herzog et al., 1991); 3) antagonist muscles are inactive
Maganaris et al., 1998, 2000). during contraction (Ichinose et al., 1997); and 4) the
As shown in Figure 4A, the contractile force of each operating range of a muscle during submaximal and
muscle increased as a function of fascicular length. In maximal contractions is the same (Leedham and
either muscle, fitting the force–length data with linear Dowling, 1995). In the present experiment, these lim-
models produced R2 ⬎ 0.98. No further improvement itations have been eliminated. An additional advan-
in R2 (P ⬎ 0.05; Student’s t-test) was obtained by tage of the present methodology is that it allows esti-
fitting the data using second and third order polyno- mates to be derived of the theoretical operating range
mials. The starting point and the slope of the force– of the average sarcomere. Dividing the GM and GL
length relation were different between the two mus- fascicular lengths in the present study by 17,600 and

TABLE 2. Parameters Calculated as a Function of Ankle Angle*

Ankle angle (degrees)
Dorsiflexion 7 Plantar flexion
⫺20 ⫺10 0 ⫹10 ⫹20 ⫹30
GM muscle muscle moment (Nm) 54 ⫾ 4 52 ⫾ 4 44 ⫾ 4 41 ⫾ 3 31 ⫾ 3 23 ⫾ 2
GL muscle moment (Nm) 23 ⫾ 2 22 ⫾ 2 19 ⫾ 2 17 ⫾ 2 13 ⫾ 2 11 ⫾ 1
GM muscle moment arm length (mm) 51 ⫾ 4 54 ⫾ 4 60 ⫾ 4 63 ⫾ 4 68 ⫾ 4 70 ⫾ 4
GL muscle moment arm length (mm) 55 ⫾ 4 58 ⫾ 4 62 ⫾ 4 64 ⫾ 4 67 ⫾ 4 69 ⫾ 4
GM tendon force (N) 1055 ⫾ 82 960 ⫾ 73 731 ⫾ 57 650 ⫾ 45 455 ⫾ 35 327 ⫾ 29
GL tendon force (N) 416 ⫾ 35 379 ⫾ 31 306 ⫾ 24 265 ⫾ 20 194 ⫾ 15 160 ⫾ 13
GM fascicular force (N) 931 ⫾ 95 810 ⫾ 79 577 ⫾ 52 500 ⫾ 48 331 ⫾ 35 222 ⫾ 20
GL fascicular force (N) 393 ⫾ 42 350 ⫾ 38 278 ⫾ 26 235 ⫾ 23 171 ⫾ 18 139 ⫾ 15

*GM and GL, medial and lateral heads of the gastrocnemius muscle, respectively. Values are mean ⫾ SD (n ⫽ 8).
In Vivo Force–Length Characteristics 221

man, ⬃25° (Sammarco et al., 1973; Nigg et al., 1992).
It must be emphasized, however, that the above cal-
culations assume that the lengths of a fascicle and the
fibers contained in it coincide. Indeed, there is evi-
dence from staining-based studies on the number and
position of motor end-plates in cadaveric specimens
that the gastrocnemius muscle fibers span the entire
fascicular length (Kawakami et al., 2000b).
The fascicular force–length relation and the theo-
retical sarcomeric operating range obtained indicate
that the gastrocnemius muscle has more in-series sar-
comeres than those required to generate maximal ac-
tivation forces at optimal lengths. This finding, how-
ever, should not be taken to imply that physiological
function is associated with operation of the gastrocne-
mius muscle outside its plateau region. Physiological
functioning requires generating smaller muscular
forces than those produced during maximal isometric
contraction, thus resulting in less myofilament overlap
and longer sarcomeric lengths. During locomotion, for
example, the human gastrocnemius muscle contracts
near-isometrically, close to its theoretical optimal
length (sarcomeric operating range: 2.75–2.92 ␮m;
Fukunaga et al., 2001). This propels the body ahead at
minimal metabolic cost. Similar results have been
reported from sarcomeric length measurements dur-
ing physiological movement in several other species
(Burkholder and Lieber, 2001). Numerous experi-
ments have shown that the number of serial sarco-
meres is highly adaptable to changes in muscle length
(Tabary et al., 1972; Williams and Goldspink, 1973;
Herring et al., 1984; Williams, 1990). For many mus-
cles, the muscle length that dictates sarcomere num-
ber seems to be the length corresponding to maximal
Fig. 4. A: Fascicular force-length relations of the GM and GL isometric force (Herring et al., 1984; Williams, 1990).
muscles. The linear models used to fit the data in each muscle are also The above experiments on sarcomeric length, how-
shown. Data are mean ⫾ SD (n ⫽ 8). B: Normalized fascicular ever, indicate that in some muscles adjustments in
force–length relations of the GM and GL muscles. Average values
from all eight subjects are presented.
sarcomeric number may be made to optimize habitual
function rather than maximize contractile force gen-
eration (see also Herring et al., 1984).
21,300 in-series sarcomeres, respectively (Huijing, The present results are of clinical relevance. Infor-
1985), indicated that the average sarcomere operated mation about force–length properties of in vivo mus-
at between 1.4 and 2.2 ␮m. The optimal sarcomeric cles is important in surgical procedures involving ten-
length region of 2.6 –2.8 ␮m (Walker and Schrodt, don transfer/lengthening (Delp et al., 1995; Loren et
1974; Lieber et al., 1994) would be obtained at fascic- al., 1996). Laser diffraction has allowed direct length
ular length regions between 46 and 49 mm in the GM measurements to be taken in sarcomeres of the af-
muscle and between 55 and 60 mm in the GL muscle. fected muscle (Lieber and Friden, 1998); however,
Extrapolating the fascicular length–ankle angle rela- this intraoperative method is highly invasive, thus
tions in the present experiment (GM muscle: y ⫽ impractical for measuring sarcomeric length in a
⫺3.4x ⫹ 110.4, R2 ⫽ 0.99; GL muscle: y ⫽ ⫺2.859x ⫹ healthy muscle. Therefore, providing reference values
114.61, R2 ⫽ 0.99) indicated that the above fascicular according to which corrective operation would be
lengths would be reached over the ankle angle range planned may not be always feasible. Moreover, laser
between ⫺43° and ⫺57°. These angles far exceed the diffraction necessitates making appropriate correc-
physiological end-range dorsiflexion ankle angle in tions in the length measurements taken to account for
222 Maganaris

the stretch of the series elastic component during Gordon AM, Huxley AF, Julian FJ. 1966. The variation in
contraction (Lieber et al., 1994). The present meth- isometric tension with sarcomere length in vertebrate mus-
odology allows noninvasive measurements to be taken cle fibers. J Physiol 184:170 –192.
Gravel D, Arsenault AB, Lambert J. 1987. Soleus-gastrocne-
in a healthy muscle during contraction, e.g., in the mius synergies in controlled contractions produced around
contralateral unaffected limb of a patient. From these the ankle and knee joints: an EMG study. Electromyogr
measurements, the length-range over which the mus- Clin Neurophysiol 27:405– 413.
cle develops force can be determined and guide the Herring SW, Grimm AF, Grimm BR. 1984. Regulation of
decision making of tendon transfer in the affected sarcomere number in skeletal muscle: a comparison of hy-
limb. If, for example, a muscle operates during con- potheses. Muscle Nerve 7:161–173.
Herzog W, Read LJ, ter Keurs HEDJ. 1991. Experimental
traction in the ascending limb of the force–length
determination of force-length relations of intact human gas-
relation as shown here, lengthening the in-series ten- trocnemius muscles. Clin Biomech 6:230 –238.
don or transferring its insertion proximally will result Herzog W, ter Keurs HEDJ. 1988a. A method for the determi-
in shifting the operating length of the sarcomeres nation of the force-length relation of selected in vivo human
further away from the optimal range for force gener- skeletal muscles. Pflugers Arch 411:637– 641.
ation. In cases where it is anatomically possible, the Herzog W, ter Keurs HEDJ. 1988b. Force-length relation of in
resultant reduction in contractile force could be com- vivo human rectus femoris muscle. Pflugers Arch 411:642–
647.
pensated for by an increase in the force moment arm
Hof AL, van den Berg JW. 1977. Linearity between the
length by inserting the tendon at a site allowing op- weighted sum of the EMGs of the human triceps surae and
eration over a greater distance from the center of the total torque. J Biomech 10:529 –539.
rotation in the joint spanned. This would not only Huijing PA. 1985. Architecture of the human gastrocnemius
achieve the desired range of movement in the joint muscle and some functional consequences. Acta Anat
but also approximate the moment-producing potential (Basel)123:101–107.
of the contralateral healthy muscle. Huijing PA, Woittiez RD. 1985. Notes on planimetric and
three-dimensional muscle models. Neth J Zool 35:521–525.
Huxley AF. 1957. Muscle structure and theories of contraction.
Prog Biophys Chem 7:255–318.
REFERENCES Ichinose Y, Kawakami Y, Ito M, Fukunaga T. 1997. Estimation
of active force-length characteristics of human vastus late-
Allen GM, Gandevia SC, McKenzie DK. 1995. Reliability of ralis muscle. Acta Anat (Basel) 159:78 – 83.
measurements of muscle strength and voluntary activation Isman RE, Inman VT. 1969. Anthropometric studies of the
using twitch interpolation. Muscle Nerve 18:593– 600. human foot and ankle. Bull Prosthet Res 10/11:97–129.
An KN, Takahashi K, Harrigan TP, Chao EY. 1984. Determi- Ito M, Akima H, Fukunaga T. 2000. In vivo moment arm
nation of muscle orientations and moment arms. J Biomech determination using B-mode ultrasonography. J Biomech
Eng 106:280 –282. 33:215–218.
Arndt AN, Komi PV, Bruggemann GP, Lukkariniemi J. 1998. Kawakami Y, Abe T, Fukunaga T. 1993. Muscle-fiber penna-
Individual muscle contributions to the in vivo Achilles ten- tion angles are greater in hypertrophied than in normal
don force. Clin Biomech 13:532–541. muscles. J Appl Physiol 74:2740 –2744.
Belanger AY, McComas AJ. 1981. Extent of motor unit activa- Kawakami Y, Amemiya K, Kanehisa H, Ikegawa S, Fukunaga
tion during effort. J Appl Physiol 51:1131–1135. T. 2000a. Fatigue responses of human triceps surae muscles
Burkholder TJ, Lieber RL. 2001. Sarcomere length operating during repetitive maximal isometric contractions. J Appl
range of vertebrate muscles during movement. J Exp Biol Physiol 88:1969 –1975.
204:1529 –1536. Kawakami Y, Kumagai K, Huijing PA, Hijakata T, Fukunaga
Cutts A. 1988. The range of sarcomere lengths in the muscles T. 2000b. The length-force characteristics of human gas-
of the human lower limb. J Anat 160:79 – 88. trocnemius and soleus muscles in vivo. In: Herzog W, edi-
Delp SL, Statler K, Carroll NC. 1995. Preserving plantar flex- tor. Skeletal muscle mechanics: from mechanisms to func-
ion strength after surgical treatment for contracture of the tion. Chichester: John Wiley & Sons Ltd. p 327–341.
triceps surae: a computer simulation study. J Orthop Res Kawakami Y, Ichinose Y, Fukunaga T. 1998. Architectural and
13:96 –104. functional features of human triceps surae muscles during
Fukunaga T, Kubo K, Kawakami Y, Fukashiro S, Kanehisha H, contraction. J Appl Physiol 85:398 – 404.
Maganaris CN. 2001. In vivo behaviour of human muscle Leedham JS, Dowling JJ. 1995. Force-length, torque-angle and
tendon during walking. Proc R Soc Lond B Biol Sci 268: EMG-joint angle relationships of the human in vivo biceps
229 –233. brachii. Eur J Appl Physiol 70:421– 426.
Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Day MK, Lieber RL, Friden J. 1998. Musculoskeletal balance of the
Lee PL, Kwong-Fu H, Edgerton VR. 1992. Physiological human wrist elucidated using intraoperative laser diffrac-
cross-sectional area of human leg muscles based on mag- tion. J Electromyogr Kinesiol 8:93–100.
netic resonance imaging. J Orthop Res 10:926 –934. Lieber RL, Loren GJ, Friden J. 1994. In vivo measurement of
Gans C. 1982. Fiber architecture and muscle function. Exerc human wrist extensor muscle sarcomere length changes.
Sport Sci Rev 10:160 –207. J Neurophysiol 71:874 – 881.
In Vivo Force–Length Characteristics 223

Loren GJ, Shoemaker SD, Burkholder TJ, Jacobson MD, Fri- Rugg SG, Gregor RJ, Mandelbaum BR, Chiu L. 1990. In vivo
den J, Lieber RL. 1996. Human wrist motors: biomechani- moment arm calculations at the ankle using magnetic reso-
cal design and application to tendon transfers. J Biomech nance imaging (MRI). J Biomech 23:495–501.
29:331–342. Sale D, Quinlan J, Marsh E, McComas AJ, Belanger AY. 1982.
Maganaris CN. 2000. In vivo measurement-based estimations Influence of joint position on ankle plantar flexion in hu-
of the moment arm in the human tibialis anterior muscle- mans. J Appl Physiol 52:1636 –1642.
tendon unit. J Biomech 33:375–379. Sammarco GJ, Burstein AH, Frankel VH. 1973. Biomechanics
Maganaris CN. 2001. Force-length characteristics of in vivo of the ankle: a kinematic study. Orthop Clin North Am
human skeletal muscle. Acta Physiol Scand 172:279 –285. 4:75–96.
Maganaris CN, Baltzopoulos V, Sargeant AJ. 1998. In vivo Tabary JC, Tabary C, Tardieu C, Tardieu G, Goldspink G.
measurements of the triceps surae complex architecture in 1972. Physiological and structural changes in the cat’s soleus
man: implications for muscle function. J Physiol 512:603– muscle due to immobilization at different lengths by plaster
casts. J Physiol 224:231–244.
614.
van den Bogert AJ, Smith GD, Nigg BM. 1994. In vivo deter-
Maganaris CN, Baltzopoulos V, Sargeant AJ. 2000. In vivo
mination of the anatomical axes of the ankle joint complex:
measurement-based estimations of the human Achilles ten-
an optimization approach. J Biomech 27:1477–1488.
don moment arm. Eur J Appl Physiol 83:363–369. Van Leeuwen JL, Spoor CW. 1992. Modelling mechanically
Martin DC, Medri MK, Chow RS, Oxorn V, Leekam RN, Agur stable muscle architectures. Philos Trans R Soc Lond B Biol
AM, McKee NH. 2001. Comparing human skeletal muscle Sci 336:275–292.
architectural parameters of cadavers with in vivo ultrasono- Walker SM, Schrodt GR. 1974. I segment lengths and thin
graphic measurements. J Anat 199:429 – 434. filament periods in skeletal muscle fibers of the Rhesus
Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, Cerre- monkey and the human. Anat Rec 178:63– 81.
telli P. 1996. In vivo human gastrocnemius architecture with Williams PE, Goldspink G. 1973. The effect of immobilization
changing joint angle at rest and during graded isometric on the longitudinal growth of striated muscle fibers. J Anat
contraction. J Physiol 496:287–297. 116:45–55.
Nigg BM, Fisher V, Allinger TL, Ronsky JR, Engsberg JR. Williams PE. 1990. Use of intermittent stretch in the preven-
1992. Range of motion of the foot as a function of age. Foot tion of serial sarcomere loss in immobilized muscle. Ann
Ankle 13:336 –343. Rheum Dis 49:316 –317.