Download Differential muscle function between muscle synergists: long and

J Appl Physiol 105: 1262–1273, 2008.
First published July 24, 2008; doi:10.1152/japplphysiol.01316.2007.
Differential muscle function between muscle synergists: long and lateral
heads of the triceps in jumping and landing goats (Capra hircus)
Andrew M. Carroll,1 David V. Lee,2 and Andrew A. Biewener1
1
Concord Field Station, Harvard University, Bedford, Massachusetts; 2School of Life Sciences, University of Nevada, Las
Vegas, Nevada
Submitted 12 December 2007; accepted in final form 23 July 2008
multiple muscles may power rotation at a
given joint. One way to make sense of this redundancy is to
investigate how anatomical differences among synergistic
muscles lead to different patterns of muscular strain, force, and
work (e.g., Ref. 35). Understanding how these differences may
lead to functional differences is critical to interpreting neural
control strategies (47) and to analyzing the biomechanical
ramifications of musculoskeletal physiology and form (21).
One way synergist muscles may differ is in the number of
joints they cross (8). Here we investigate in vivo muscle strain
and inverse dynamic estimates of muscle work and stress to
understand how biarticular and monoarticular synergists of the
goat (Capra hircus) triceps brachii might differ in their function across differing locomotor tasks.
The functional repertoires available to biarticular muscle
have been extensively discussed and modeled (reviewed in
Refs. 25, 44). A biarticular muscle may shorten and produce
positive work—simultaneously at each of the joints it crosses
(13). Alternatively, a biarticular muscle may lengthen at one
joint while shortening at the common joint, reducing strain
rates relative to its monoarticular synergist, thus allowing it to
generate greater force (44, 36). If the relative joint rotations are
sufficient, the biarticular muscle may also contract isometrically, transmitting energy from one joint to another, without
the muscle itself doing any work. More generally, it has been
proposed that biarticular muscles are responsible for controlling joint moments while monoarticular muscles are responsible for powering joint rotation (44). Finally, if no rotation
occurs at the second joint, a biarticular muscle may not differ
in its function from its monoarticular synergist. This might be
especially true when the moment arm across one of the joints
is small (10).
The wealth of prediction about how biarticular muscles may
function relative to their monoarticular agonists has motivated
several empirical comparisons of function in mono- and biarticular muscles of the hindlimb triceps surae (e.g., Refs. 25,
35). However, to our knowledge, only two comparisons of
directly measured muscle fascicle strain in monoarticular/
biarticular synergists have been published (23, 43), which were
based on ultrasound studies of the human monoarticular soleus
compared with the biarticular medial gastrocnemius (MG).
Both studies found differing functional patterns between the
two muscles. The soleus was observed to follow the kinematics
of the ankle, stretching and shortening with ankle movement in
both walking (23) and landing prior to a drop jump (43), in a
pattern similar to other monoarticular muscles (15, 22). In
contrast, the MG showed isometric strain patterns during
walking (23) and fascicle shortening in low-intensity drop
jumps, but stretching in high-intensity drop jumps (43). Reduced strain and strain rates during walking in the human MG
are consistent with the predictions of isometric function that
may arise from a biarticular muscle that transfers energy
between joints but does little or no work itself. Such behavior
has also been observed in vivo for the biarticular lateral
gastrocnemius in various animals during running and hopping
(e.g., Refs. 2, 39).
The paucity of empirical comparisons of biarticular and
monoarticular muscle strain and work production, however,
may limit or bias our understanding of the range of functional
differences between biarticular and monoarticular synergists.
A main goal of this study, therefore, is to augment these studies
of the hindlimb triceps surae with an analogous forelimb
Address for reprint requests and other correspondence: A. M. Carroll,
Biology Department, University of Evansville, Evansville, IN (e-mail: ac204
@evansville.edu).
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.
biarticular; fascicle strain; muscle work
IN VERTEBRATE LIMBS,
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Carroll AM, Lee DV, Biewener AA. Differential muscle function between muscle synergists: long and lateral heads of the
triceps in jumping and landing goats (Capra hircus). J Appl
Physiol 105: 1262–1273, 2008. First published July 24, 2008;
doi:10.1152/japplphysiol.01316.2007.—We investigate how the biarticular long head and monoarticular lateral head of the triceps brachii
function in goats (Capra hircus) during jumping and landing. Elbow
moment and work were measured from high-speed video and ground
reaction force (GRF) recordings. Muscle activation and strain were
measured via electromyography and sonomicrometry, and muscle
stress was estimated from elbow moment and by partitioning stress
based on its relative strain rate. Elbow joint and muscle function were
compared among three types of limb usage: jump take-off (lead limb),
the step prior to jump take-off (lag limb), and landing. We predicted
that the strain and work patterns in the monoarticular lateral head
would follow the kinematics and work of the elbow more closely than
would those of the biarticular long head. In general this prediction was
supported. For instance, the lateral head stretched (5 ⫾ 2%; mean ⫾
SE) in the lead and lag limbs to absorb work during elbow flexion and
joint work absorption, while the long head shortened (⫺7 ⫾ 1%) to
produce work. During elbow extension, both muscles shortened by
similar amounts (⫺10 ⫾ 2% long; ⫺13 ⫾ 4% lateral) in the lead limb
to produce work. Both triceps heads functioned similarly in landing,
stretching (13 ⫾ 3% in the long head and 19 ⫾ 5% in the lateral) to
absorb energy. In general, the long head functioned to produce power
at the shoulder and elbow, while the lateral head functioned to resist
elbow flexion and absorb work, demonstrating that functional diversification can arise between mono- and biarticular muscle agonists
operating at the same joint.
MUSCLE FUNCTION IN MONO- AND BIARTICULAR MUSCLES
muscle synergist pair, by comparing the biarticular long head
of the triceps brachii (TrLONG) and monoarticular lateral head
(TrLAT). Muscle activation, strain, stress, and work patterns are
compared between the muscle heads during upward and downward jumps in goats (Capra hircus). The forelimb was also
chosen because it is involved in landing from downward jumps
as well as powering upward jumps and would therefore be
expected to display a broad range of joint and muscle function.
We hypothesize that strain and work patterns of the monoarticular TrLAT, like those of the soleus in humans (23), will
follow the kinematics of the elbow joint more closely than the
biarticular TrLONG. Specifically, we predict that shoulder flexion during upward jumps (3) might allow the long head to
shorten despite elbow flexion in the early periods of stance.
However, similar to the human soleus and MG during highintensity landings (43), we predict that the TrLONG and TrLAT
would both function to absorb energy when goats land from a
downward jump.
Animals. Four goats (25, 28, 42, and 45 kg) were used in the study
as a minimum but sufficient sample size for statistical significance
(based on previous studies, e.g., Ref. 15). Animals were housed
outdoors in fields at the Concord Field Station, Bedford, MA, and
experiments were conducted in accordance with Harvard Institutional
Animal Use and Care Committee guidelines and U. S. Department of
Agriculture regulations. Over a period of 2–3 wk goats were trained
to jump onto and off of a wooden platform that measured 1.0 m high
for the three larger goats and 0.82 m for the 25-kg goat (1.0 ⫻ 0.3 m
top surface) until jumps were made smoothly and without hesitation.
Anatomy. The long head (TrLONG) and the lateral head (TrLAT) of
the triceps both insert on the olecranon process of the ulna (Fig. 1;
Ref. 9). A much smaller monoarticular medial head is also present; its
Fig. 1. Anatomy of the goat (Capra hircus) triceps brachii. The biarticular
long head (TrLONG) and monoarticular lateral head (TrLAT) both insert on the
olecranon process of the ulna. The TrLONG originates on the scapula, whereas
the TrLAT originates on the humerus. Symbols indicate the location of sonometric crystals and electromyographic (EMG) electrodes for 3 of 4 goats used
in this study (Table 3). In the fourth goat, 1 set of crystals was used to record
from the midbelly of the long head, rather than 2 sets (anterior and posterior)
as in the other goats.
J Appl Physiol • VOL
mass and cross-sectional area were grouped with that of the lateral
head for the purposes of this study. The lateral and medial triceps
heads originate from the humerus, while the long head originates from
the distal-most third of the ventrocaudal margin of the scapula. A
much smaller tensor fascia antebrachii (9) also runs from the scapula
to the olecranon, and its mass and cross-sectional area were grouped
with that of the long head. The TrLAT was found to be smaller than the
TrLONG, averaging 53% of the mass and 39% of the physiological
cross-sectional area (PCSA) of the TrLONG. Architecturally, the TrLAT
contains parallel fascicles that run the extent of its length (ranging
from an average of 6.0 cm in a 25-kg goat to 8.0 cm in a 45-kg goat).
The TrLONG also contains long fascicles of similar length (average:
6.5 cm in a 25-kg goat to 8 cm in a 45-kg goat), but is slightly
unipinnate (15 ⫾ 4°).
Surgery. Prior to surgery, animals were starved for 1 day. Goats
were induced for intubation with 8 mg/kg ketamine and 0.05 mg/kg
xylazine administered into the jugular vein. Following intubation,
goats were maintained in a surgical plane of anesthesia with 2– 4%
isoflurane by volume, administered via inspired oxygen. The skin of
the lateral, proximal forelimb was sterilized. Under aseptic conditions,
an incision was made superficial to the long and lateral triceps muscle
bodies, and their fascicles were exposed by separation of overlying
fascia. 2-mm sonometric crystals (Sonometrics, London, ON, Canada)
and bipolar electromyography (EMG) electrodes, fashioned from
twisted strands of 0.102 mm Teflon-coated silver wire (California
Fine Wire, Grover Beach, CA) with a 3– 4 mm dipole distance (28)
were soaked overnight in a sterilizing solution (Nolvasan Solution,
Aveco, Fort Dodge, IA). A 2-cm incision was made in the neck of the
animal and a subcutaneous channel was hollowed between this incision and the incision over the triceps. Sonometric crystals and electrodes were passed from the neck to the forelimb incision, leaving
their connectors outside the smaller neck incision. Sonometric crystals
were inserted into the muscle, and fascicles were gently sutured over
the crystal with 4 – 0 silk. Care was taken to insert each pair of
sonometric crystals along the fascicle axis 10 –14 mm apart. In the
long head, this meant implanting the distal crystal slightly deeper than
the proximal due to the muscle’s slight fascicle pinnation. EMG
electrodes were inserted immediately lateral to those fascicles containing crystals via an 18.5-gauge hypodermic needle and were
secured to the fascicles with 4 – 0 silk suture. The connectors were
then sutured to the skin of the neck with sterile 0 surgical wire. Both
incisions were closed with 3– 0 vicryl suture, and the goats were
allowed to recover overnight. Every 12 h between surgery and death
animals were given a nonsteroidal anti-inflammation agent (Flunixin
1 mg/kg) and a broad spectrum antibiotic (Polyflex, Wyeth, Madison,
NJ). Data collection took place within 1–2 days following surgery. All
animals were killed following data collection with 120 mg/kg of
commercial pentobarbital sodium solution injected into the jugular
vein. No animal showed signs of infection or lameness prior to death.
Joint kinematics. The hoof and the skin overlying the metacarpophalangeal, wrist, and shoulder joints and the scapular spine (at its
most proximal palpable extent) were marked with nontoxic white
paint. Jumps and landings were digitally recorded at 250 Hz using a
Redlake PCI-500 video system (Redlake, Morgan Hill, CA). Joint
locations were digitized using a custom auto-tracking digitization
program in MatLab (v. 6.5; The MathWorks, Natick, MA) written by
T. L. Hedrick, UNC, Chapel Hill, NC (http://www.unc.edu/
⬃thedrick/software1.html). Digitized data were filtered at 35 Hz with
a fourth-order recursive (zero lag) Butterworth filter and used to
determine hoof position, limb segment position, and elbow and
shoulder angles for each sequence. The camera was controlled by an
analog trigger, and the voltage signal from this trigger was used to
synchronize camera recordings with EMG, sonomicrometry, and
forceplate recordings. As opposed to the definition for humans (Moore
and Agar, 34a), shoulder flexion is this study is defined as closing of
the caudal (posterior) angle between the humerus and scapula in the
sagittal plane.
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METHODS
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MUSCLE FUNCTION IN MONO- AND BIARTICULAR MUSCLES
55 kg; Lee et al., 2008 27a) and scaled to the size of the goats used in
the current study.
Elbow work was measured as the numerical integration of elbow
moment and elbow angle change over the period of interest. Elbow
work was normalized by the combined mass of the TrLONG and TrLAT
heads measured post mortem. Muscle work was measured as the
numerical integration of muscle fascicle shortening and estimated
force (calculated as described below) and was normalized by the mass
of each muscle.
Muscle stress. Muscle stress was estimated from extensor moments
acting across the elbow joint by assuming that the triceps are the only
muscles capable of extending the elbow:
M elbow ⫽ ␴LONG PCSALONG rLONG 共␪兲 ⫹ ␴LAT PCSALAT rLAT共␪兲
where Melbow is the moment at the elbow, ␴MUS is the stress produced
by each muscle as a function of time, PCSAMUS is the physiological
cross-sectional area of each muscle (measured post mortem), and
rMUS(␪) is the moment arm of each muscle as a function of elbow
angle (␪).
Because this equation cannot be solved for muscle stress, it was
necessary to make further assumptions to estimate the stress acting in
each of the muscles. Therefore, muscle stress was assigned based on
the estimated capacity of each muscle to generate force as a function
of its shortening velocity (18). This was done by calculating a single
common stress ␴ˆ , which was distributed to each muscle according to
a weighting factor, kMUS, based on the relative estimated force for
each muscle. For example the weighting factor for the TrLAT was:
k LAT ⫽
F⬘LAT
F⬘LONG ⫹ F⬘LAT
(2)
where F⬘MUS is the relative force estimated for each muscle based on
instantaneous measurement of fascicle velocity (as described below).
Thus the following equation was used to solve for stress in each
individual muscle.
Fig. 2. Video frames from a goat (45 kg) showing kinematics
of the lead limb (A) and lag limb (B) of an upward jump and
the landing limb (C) of a down jump. Goats jumped off or onto
a force plate. Frames show time points of foot-on, peak elbow
flexion, and foot-off. These kinematic events defined periods
used to analyze muscle and joint function in this study.
J Appl Physiol • VOL
(1)
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EMG. EMG signals were filtered (60-Hz notch and 30- to 3,000-Hz
band pass) and amplified at 1,000⫻ with Grass P511 amplifiers
(Grass-Telefactor, West Warwick, RI). Outputs from the Grass amplifiers were digitized at 2,000 Hz through a 12-bit analog-to-digital
converter (Digidata 1200B, Axon Instruments, Union City, CA).
EMG signals were later digitally filtered with a 100- to 1,000-Hz band
pass fourth-order zero-lag Butterworth filter before analysis. Onset
and offset times were measured relative to timing of hoof contact.
Rectified EMG intensity (mV) was normalized by the largest recorded
value for each electrode over all trials.
Muscle strain. Sonometric crystals measure latency of ultrasound
to determine instantaneous muscle length. The speed of sound in
muscle was estimated to be 1,550 m/s (34). Latency of crystal
response was transduced and amplified with a Triton sonometrics
system (model 120 –1001; Triton Technology, San Diego, CA) and
digitized with the EMG signals at 2,000 Hz as described above. Due
to its filtering circuitry, there is a 5-ms delay inherent in the Triton
system that was accounted for in subsequent data analysis. Crystal
signals manually cleaned to eliminate “drop-outs,” were digitally
filtered at 30 Hz with a fourth-order recursive (zero lag) Butterworth
filter and a custom MatLab script. Crystal distances were normalized
to resting length at stance.
Elbow joint moment analysis. Elbow moments were calculated
using inverse dynamics (29). Goats jumped onto or off of one of two
forceplates (0.4 m by 0.6 m, model AMTI BP400600HF, Watertown,
MA), covered with grip tape (3M Safety-Walk Medium Duty Resilient Tread 7741), flush with ground level, and resting in a bed of sand.
Plate forces and moments were recorded using a custom LabView
program (written by D. V. Lee). The center of pressure of each plate
was calculated from these data and transformed into the camera frame
of reference using a custom MatLab script. Elbow joint moments were
estimated from ground reaction force, segment mass, translational and
rotational segment inertia, and moment of the more distal joint using
a MatLab script modified from that developed by Craig McGowan
(31). Segmental properties were determined from two goats (20 and
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MUSCLE FUNCTION IN MONO- AND BIARTICULAR MUSCLES
M elbow ⫽ ␴ˆ 关kLONG PCSALONG rLONG共␪兲 ⫹ kLAT PCSALAT rLAT共␪兲兴 (3)
with estimated individual muscle stress equal to the product of ␴ˆ (t)
and kMUS(t), and muscle force equal to the product of stress and
physiological cross sectional area of each muscle (PCSAMUS).
Relative force for each muscle was calculated to depend on muscle
velocity (strain rate) by an inverse hyperbolic relationship (19).
During shortening this relationship was described by the following
equation (32):
1 ⫺ V共t兲/ Vmax
F⬘MUS ⫽
1.5 䡠 关1 ⫺ V共t兲兴/共Vmax 䡠 k兲
(4)
F⬘MUS ⫽
1.1 䡠 V共t兲/Vmax ⫹ a/Fo 䡠 V共t兲/ Vmax ⫹ b/ Vmax
1.5 䡠 关V共t兲/Vmax ⫹ b/Vmax兴
(5)
a⬘/Fo was estimated as 0.4 (30) while b⬘/Vmax was estimated as 0.15
(27, 30).
The asymptotic force in our model is set at 1.5 times that of
isometric force. While values as high as 1.8 are often cited in in vitro
冋冉 冏
ACT
⫽ exp
F MUS
⫺abs
冏冊 册
L1.55 ⫺ 1
0.81
2.12
(6)
ACT
equals
where L is the normalized length (i.e., resting length ⫽ 1 and FMUS
ACT
a maximum of 1 at resting length). FMUS was multiplied by FMUS
to
take into account reductions in muscle force at lengths other than
resting length. Passive force was not estimated because it accounts for
⬍5% of total force up to 1.2 times muscle resting length (4), which is
near the maximum strains measured in this study.
The slight pennation angle of the TrLONG was not taken into
account. On the basis of an emperical study of the turkey lateral
gastrocnemious (1), a maximum fiber angle of ⬃20° was estimated,
which would lead to a 7% reduction in muscle force output. However,
because it is impossible to estimate actual fiber rotation in vivo it was
not incorporated into the model. EMG timing and amplitude were also
not used to estimate muscle force because of the intrinsic difficulties
in comparing EMG preparations (28) and because of the difficulty of
accurately estimating activation and deactivation force kinetics due to
lack of published data for these muscles. Instead, we assumed that
both muscles produced force when an extensor muscle moment acted
at the elbow.
Fig. 3. Mean (solid line) and standard error (dashed line) for elbow angle, elbow moment, horizontal ground reaction force (GRF), and vertical GRF for a 45-kg
goat as percent of stance. The gray area indicates stance (foot-on to foot-off) and the dashed line indicates peak elbow flexion. Forelimb use resulted in differences
in joint kinematic, force, and moment profiles. Note different scales for horizontal vs. vertical GRF.
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where F⬘MUS is normalized to a maximum eccentric force ⬃1.5 times
isometric force (see below). The normalized hill parameter, k (⫽b/
Vmax and a/Fo), was estimated as 0.20 (5, 41). Vmax was estimated as
⫺7 fiber lengths (FL/s) based on the assumption that the triceps is
composed of both type I and type II fibers with a Vmax of ⫺5 and ⫺9
FL/s, respectively [based on temperature normalized values for humans (46), horses (40), and sheep (42)].
Relative force during stretch was estimated using the following
equation (30):
and in situ literature (e.g., Ref. 24), values are frequently lower during
voluntary contractions (e.g., 1.2; Ref. 12). Asymptotic force was
assumed to be achieved at approximately ⫺1/2 Vmax as observed in
numerous studies (e.g., Refs. 4, 12, 30).
The active force-length properties of each muscle head were also
estimated based on the following equation and parameters from
Brown et al. (4):
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MUSCLE FUNCTION IN MONO- AND BIARTICULAR MUSCLES
Fig. 4. Histogram showing means (⫾SE) across the 4 individual goats for
changes in shoulder angle (A), elbow angle (B), elbow moment (C), and elbow
joint work (D). Values for the 3 patterns of limb use (lead and lag limb of up
jumps and landing from down jumps) are shown for phases of elbow flexion
and extension, and net values over the duration of stance. *Significant difference among jump types in Tukey’s Honestly Significant Difference (HSD)
post hoc tests with a starting ␣ of 0.05. Differences in limb function resulted
in significant differences among kinematic and dynamic parameters, particularly elbow work, which differed significantly over all phases for the 3
categories of forelimb usage.
J Appl Physiol • VOL
eters between the long and lateral heads were tested with a two-factor
ANOVA with muscle head and individual as factors (Table 2). ANOVA,
post hoc tests, and normality tests were run in .Jmp (SAS institute,
Cary, NC). Correlations among muscle strain and work were tested
using SigmaPlot (Systat Software, San Jose, CA), and were performed
on pooled data from all individuals.
RESULTS
Goats did not appear to favor their noninstrumented forelimb, as all but one individual used the instrumented forelimb
as the lead limb to jump up in most cases (Table 3), suggesting
that instrumentation did not alter limb usage. Regardless of
forelimb usage, all jumps began with a period of elbow flexion
(duration: lead 0.047s ⫾ 0.002 s; lag 0.078⫹0.01 s; landing
0.083 ⫾ 0.008 s, mean ⫾ SE) followed by a period of elbow
extension (duration: lead 0.067 ⫾ 0.009 s; lag 0.092⫹0.01 s;
landing 0.074 ⫾ 0.01 s; Figs. 3 and 4B). Periods of elbow
flexion and elbow extension, as well as the total period of
stance, were used to test for differences among joint parameters in all subsequent analyses (Fig. 4).
Elbow moments. During elbow flexion, no significant differences in mean elbow moment were observed among types of
forelimb usage. During elbow extension, elbow moments differed significantly among all jump types (Fig. 4C), reflecting
differences in relative limb retraction angle (Fig. 2) and GRF
magnitudes (Fig. 3).
Elbow work. Regardless of forelimb usage, the elbow experienced similar extensor moments during the flexion period
and, thus, absorbed energy (Fig. 4D). The amount of energy
absorbed during flexion, however, varied significantly with
limb usage (Fig. 4D), reflecting differences in elbow joint
angular deflection (compare Fig. 4, B and C). During elbow
extension, significant net joint work was done only during
upward jumps (46 ⫾ 9 J/kg in the lead limb and 25 ⫾ 9 J/kg
in the lag limb; Fig. 4D). No work was done during elbow
extension in downward jumps because the extensor elbow
moment fell to zero during this period (Fig. 4D). Over the
duration of stance, the elbow did net positive work in the lead
limb of an upward jump (35 ⫾ 10 J/kg) but the work done in
the in the lag limb was not significantly different from zero
(P ⬎ 0.10). In contrast, the elbow joint absorbed a great deal
of energy (⫺58 ⫾ 10 J/kg) during landing (Fig. 4D).
Muscle activity. Timing parameters did not vary with limb
usage in the TrLONG but, in the TrLAT, EMG onset was
significantly earlier when animals landed from a downward
jump. This resulted in a longer duty cycle (Fig. 5D), despite
significantly earlier offset of the TrLAT (Fig. 5C). In both
muscles, normalized EMG intensity was higher in the lead
forelimb than in the lag forelimb of an upward jump (Fig. 5A).
TrLAT EMG intensity in the lead forelimb of an upward jump
was also significantly higher than during landing from a downward jump (P ⬍ 0.05; Fig. 5A).
Muscle strain and strain rate. Muscle function parameters
were measured over stance and within stretch and shortening
periods of the TrLAT to allow comparisons between the muscle
heads (Fig. 6). In upward jumps, periods of stretch and shortening in the TrLAT were simultaneous with those defined for
the elbow joint (elbow flexion ⫽ TrLAT stretch; elbow extension ⫽ TrLAT shortening, Fig. 6; t-test: P ⬎ 0.25). The TrLONG
sometimes displayed a slight lengthening at the end of stance
(Fig. 6B), so the end of shortening in this was measured at the
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Data analysis. Goats used both forelimbs to land from downward
jumps, but only one forelimb was used during take-off in upward
jumps (Fig. 2). If the marked limb was used in take-off (being the last
forelimb to leave the ground), it was described as the “lead limb” of
an upward jump (Fig. 2). When it was used in penultimate step prior
to take-off, the marked limb was described as the “lag limb” of an
upward jump (Fig. 2). Thus we defined three distinct categories of
limb usage in this study: the lead limb of an upward jump (lead limb);
the lag limb of an upward jump (lag limb); and the marked limb of a
downward jump (landing limb). Kinematic and ground reaction force
differences appeared to justify this categorization (Figs. 3 and 4).
Consequently, all muscle and joint parameters were compared among
these categories of limb usage.
EMG, forceplate, joint, and muscle parameters were grouped
within each individual and statistics were run on the individual means
for each parameter. Differences among jump types were tested using a
two-factor ANOVA with limb usage and individual as factors (Table 1).
All data was tested for normality prior to ANOVA using a ShapiroWilk test. Tukey’s Honestly Significant Difference post hoc tests with
a starting ␣ of 0.05 were run to determine which parameters differed
over periods of stance or muscle cycle. Differences in muscle param-
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MUSCLE FUNCTION IN MONO- AND BIARTICULAR MUSCLES
Table 1. ANOVA results for limb function (lead, lag, or down jumps) effects on muscle parameters
TrLAT Shortening
TrLAT Stretch
Long head
Strain
Strain rate
Stress
Work
Lateral head
Strain
Strain rate
Stress
Work
Stance
DF
F Ratio
P
F Ratio
P
F Ratio
P
2
2
2
2
19.4
26.5
0.2
9.4
0.002
0.001
0.797
0.014
1.5
6.1
29.9
7.1
0.299
0.036
⬍0.001
0.027
33.5
45.0
2.7
10.3
⬍0.001
⬍0.001
0.1423
0.0114
2
2
2
2
11.5
4.5
17.8
10.1
0.009
0.064
0.003
0.012
5.8
2.3
6.9
2.3
0.081
0.177
0.027
0.173
11.3
8.0
30.6
12.0
0.009
0.020
⬍0.001
0.008
Biarticular long head of the triceps brachii (TrLONG) and monoarticular lateral head (TrLAT). Bold values indicate significance (P ⬍ 0.05). Differences among
types of limb function were determined by post hoc tests and are shown in Fig. 7. DF, degrees of freedom.
TrLONG showed net shortening over forelimb stance in upward
jumps regardless of limb usage (net strain: ⫺17 ⫾ 2% pooled
mean; P ⬎ 0.25) and, similar to TrLAT, underwent net stretch
when landing from a downward jump (net strain: 6 ⫾ 1%).
Muscle strain rate followed patterns of muscle strain (Fig.
7B), with the exception that strain rates during shortening were
significantly higher in the TrLONG of the lead limb during
upward jumps than during downward jumps (Fig. 7B; ⫺0.5 ⫾
0.05 vs. ⫺0.3 ⫾ 0.01 FL/s). The differences in strain rate
between muscle heads during shortening were not significant
(Table 2). When the data for lead and lag forelimbs of upward
jumps were grouped; however, the TrLONG was found to
shorten significantly more slowly than the TrLAT (⫺0.5 ⫾ 0.1
vs. ⫺1.5 ⫾ 0.2 FL/s; P ⬍ 0.05).
Muscle stress. Stresses calculated for both muscles followed
the general pattern of elbow moment (compare Figs. 4C and
7C). During the period of muscle stretch, stress in the TrLAT
did not differ significantly between the lead and lag limbs of an
upward jump (pooled mean: 258 ⫾ 27 kPa; P ⫽ 0.10), but in
downward jumps the TrLAT generated significantly less stress
in post hoc tests (Fig. 7C; 142 ⫾ 39 kPa). Over the same
period, no significant difference in muscle stress was found in
Table 2. ANOVA results for muscle head (lateral or long head) effects on muscle parameters
TrLAT Shortening
TrLAT Stretch
DF
F Ratio
P
Stance
F Ratio
P
F Ratio
P
0.4
3.1
0.9
4.44
0.565
0.176
0.407
0.125
6.1
0.6
14.2
17.3
0.091
0.507
0.033
0.025
0.1
2.0
1.7
11.8
0.782
0.256
0.284
0.041
73.1
19.0
11.0
31.5
0.003
0.022
0.045
0.011
0.9
7.5
2.6
1.6
0.418
0.070
0.208
0.297
1.4
4.4
5.8
5.7
0.326
0.126
0.094
0.090
Up Jumps
Lead limb
Strain
Strain rate
Stress
Work
Lag limb
Strain
Strain rate
Stress
Work
1
1
1
1
141
27.6
46.4
14.2
0.001
0.013
0.007
0.032
1
1
1
1
127.8
43.6
6.53
38.5
0.002
0.007
0.043
0.009
Down Jumps
Landing limb
Strain
Strain rate
Stress
Work
1
1
1
1
2.1
3.77
3.3
4.8
0.202
0.147
0.164
0.116
Bold values indicate significant difference between muscles (P ⬍ 0.05).
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nadir of its strain profile. In downward jumps, however, peak
elbow flexion occurred before peak TrLAT stretch (P ⬍ 0.05;
Fig. 6C), apparently due to the stretch of in-series compliance
in the muscle-tendon unit.
The TrLAT stretched (during elbow flexion) in upward
jumps, with significantly less stretch in lead limb than in the
lag limb (net fascicle strain: 5 ⫾ 2 vs. 14 ⫾ 4% post hoc test
with starting value of P ⬍ 0.05). Over the same period, the
TrLONG shortened by ⫺6 ⫾ 2% with no significant difference
found between the lead and lag limbs of an upward jump in
post hoc tests (Fig. 7A). In landing, both muscles stretched
simultaneously at the onset of stance (net strain: 19 ⫾ 5 and
13 ⫾ 3%; Table 2; Fig. 7A). Subsequently, during elbow
extension, the muscles shortened by a similar amount in both
the lead and lag limb of an upward jump (net strain: ⫺11 ⫾ 4%
pooled mean; P ⬎ 0.25). Over the full stance period these
patterns resulted in net TrLAT shortening in the lead limb of an
upward jump (⫺8 ⫾ 3%) but resulted in net stretching during
landing (8 ⫾ 3%). Surprisingly, the TrLAT also displayed net
stretch over the period of stance in the lag limb during jump
takeoff (5 ⫾ 2%), although the elbow underwent net extension
(comparing Fig. 4 with Fig. 7A) In contrast to the TrLAT, the
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MUSCLE FUNCTION IN MONO- AND BIARTICULAR MUSCLES
Table 3. Numbers of trials recorded for each type of jump
used in this study
Up Jumps
Goat 1 (45
Long*
Lateral
Goat 2 (42
Long
Lateral
Goat 3 (28
Long*
Lateral
Goat 4 (24
Long*
Lateral
Lead Limb
Lag Limb
Down Jumps
18
8
6
3
22
12
2
3
6
6
9
8
12
6
4
2
11
6
5
4
5
5
5
3
kg)
kg)
kg)
kg)
*Two samples were simultaneously recorded from the long head as in
Fig. 1.
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the TrLONG among the lead limb of an upward jump, lag limb
of an upward jump, or in landing from a downward jump
(pooled mean: 99 ⫾ 13 kPa). Consequently, during the period
of TrLAT stretch, stress was significantly higher in the TrLAT
than the TrLONG in the lead and lag limbs of an upward jump
(P ⬍ 0.01), but not in down jumps (P ⬎ 0.1; Fig. 7C; Table 2).
During the period in which both muscles shortened, stress in
the TrLAT was not significantly different among the lead and
lag limbs of upward jumps (pooled mean: 115 ⫾ 30 kPa; P ⬎
0.10), but was much lower in landing from a downward jump
in post hoc tests (8 ⫾ 4 kPa). Over the same period, stress in
the TrLONG was similar in the lead limb and lag limbs of an
upward jump (P ⬎ 0.25; Table 4) and again, similar to TrLAT,
much lower in landing (17 ⫾ 4 kPa; Fig. 7C). No significant
difference in TrLAT and TrLONG stress was observed during
shortening, even when data from both categories of upward
jumps were pooled (P ⬎ 0.10).
Muscle work. While being stretched, the TrLAT absorbed
more work in the lag limb (⫺34 ⫾ 5.6 J/kg) than in either the
lead limb (⫺13.0⫹3.5 J/kg) or in landing (⫺24 ⫾ 2.8 J/kg;
Fig. 7D; Table 4). Over the same period, the TrLONG shortened
to produce work in both the lead and lag limbs of an upward
jump, without significant differences among limb function
(pooled mean: 3 ⫾ 1 J/kg). In landing, however, the TrLONG
stretched and absorbed energy from a downward jump (⫺13 ⫾
4.9 J/kg; Fig. 7D; Table 4).
During the period of TrLAT shortening both muscles shortened to produce work in the lead limb (TrLONG: 10 ⫾ 3 J/kg
and TrLAT: 5 ⫾ 3 J/kg; P ⬎ 0.05). In the lag limb, positive
work was produced only by the TrLONG (5 ⫾ 1.5 J/kg), as net
work in the TrLAT was not significantly different from zero
(⫺1.5 ⫾ 1.5 J/kg; P ⬎ 0.25; Table 4). When landing from a
downward jump neither muscle produced significant work
during the period of TrLAT shortening (P ⬎ 0.1; Fig. 7D, Table
4) due to low stress calculated from the reduced elbow moment
(Fig. 4).
Despite the fact that the elbow produced positive net joint
work over stance in the lead limb, net work done by the TrLAT
was negative (⫺8 ⫾ 3.2 J/kg). TrLAT net work reflected even
greater energy absorption in the lag leg of an upward jump
(⫺35 ⫾ 7 J/kg) and in landing from a downward jump (⫺22 ⫾
3 J/kg), which were consistent in the sign, but not in the
magnitude, of elbow joint work (Fig. 4). In contrast, the
TrLONG did positive net work over stance in both the lead and
lag limbs of an upward jump (15 ⫾ 4 and 7 ⫾ 4 J/kg; Fig. 7D)
but, similar to TrLAT, absorbed energy during landing from a
downward jump (⫺13 ⫾ 5 J/kg). Hence, over the duration of
stance, net work of the TrLONG and TrLAT are opposite in sign
and significantly different during upward jumping, whereas
these muscles absorb statistically similar, negative net work
during downward jumping.
Muscle work during shortening was regressed against fascicle strain for each period of TrLAT stretching and shortening,
and over net stance, to assess the dependence of muscle work
on fascicle strain patterns over all categories of limb usage
(Fig. 8). A strong correlation indicates that fascicle strain
influences muscle energy absorption or production. During the
period of TrLAT stretch and over stance, strong correlations are
found between muscle work and muscle strain in the TrLONG
Fig. 5. Histogram showing means (⫾SE) across the 4 individual goats for
electromyogram (EMG; A) intensity, EMG onset (B), and offset times (as
percent of stance and relative to the time of foot on; C ), and EMG duty cycle
(EMG duration/stance duration; D). *Significant difference among jump types
in Tukey’s HSD post hoc tests with a starting ␣ of 0.05. In both TrLAT and
TrLONG, EMG intensity was greater in lead jumps than in lag jumps, but
intensity during landing was also greater than in the lag limb, despite a lower
elbow moment (Fig. 4B).
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MUSCLE FUNCTION IN MONO- AND BIARTICULAR MUSCLES
1269
but were lower in the TrLAT (Fig. 8). During the period defined
by TrLAT shortening, there was a weak but significant correlation in the TrLONG (r ⫽ 0.35) and no correlation in the TrLAT
(r ⬍ 0.01; P ⬎ 0.25), indicating that its work was determined
almost entirely by muscle stress.
DISCUSSION
The principal aim of this study is to understand how muscle
function in a monoarticular vs. a biarticular synergist compares
across varying locomotor tasks. This is assessed by examining
the relative relationship between muscle strain and elbow joint
kinematics and between muscle work and elbow joint work for
the monoarticular TrLAT and biarticular TrLONG of the goat
triceps brachii during jumping and landing tasks.
Fascicle strain and elbow kinematics. Our prediction that
strain patterns in the monoarticular TrLAT would follow elbow
kinematics more closely than those in the biarticular TrLONG is
generally supported. The TrLAT always stretched during elbow
flexion and shortened during elbow extension. In contrast, the
TrLONG shortened throughout stance in upward jumps (Fig. 6,
A and B). In landing from a downward jump both muscles
J Appl Physiol • VOL
stretched with elbow flexion and shortened with elbow extension (Fig. 6C ). While it is possible that these differences in
functional pattern may be due to differences in muscle-tendon
architecture between the muscle heads, we believe the most
likely explanation is that the TrLONG is biarticular and the
TrLAT is monoarticular.
Earlier studies of muscle function in the biarticular MG and
monoarticular soleus muscles of cats found very little difference in strain patterns among the muscles (e.g., Refs. 17, 35).
However, in these studies fascicle strain was estimated from
joint kinematics, which can be unreliable (2, 20). When fascicle strain in human MG and soleus fascicles was measured
directly with ultrasound during walking (23) and drop jumps
(43), strain patterns in the soleus were found to follow the
kinematics of the ankle more closely than those of the MG.
Similarly, strain in the goat TrLAT follows rotation of the elbow
more closely than that of the TrLONG.
Interestingly, this strain pattern differs from that measured in
the TrLAT of horses during trotting, which showed minimal
(⬃2%) lengthening despite elbow flexion (20). This difference
may reflect a general trend toward reduced stretch in monoar-
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Fig. 6. Mean profiles (solid lines) ⫾ standard error (dashed lines) across trials for lead limb up jump (A), lag limb up jump (B); and a forelimb landing from
a down jump (C), showing temporal patterns of shoulder angle, elbow angle, and fascicle strain and stress in the TrLONG and TrLAT muscle heads, as a percentage
of stance in a 45-kg goat. The number of trials included in each graph is given in Table 3. Gray areas indicate stance time, and dashed lines indicate peak stretch
in the TrLAT, which was concurrent with peak elbow flexion, except when the forelimb was used to land from a downward jump.
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MUSCLE FUNCTION IN MONO- AND BIARTICULAR MUSCLES
ticular muscles as animal body size increases. For instance, the
magnitude of stretch in the VL is also smaller in the horse than
in rats (14), dogs (6), or goats (15).
In downward jumps, the two goat forelimb muscles function
similarly because the TrLONG shifts from the monophasic shortening pattern required for upward jumps to a stretch-shortening
pattern resembling that observed in the TrLAT. Similarly, the
human MG exhibited net shortening over stance when
subjects landed from low-intensity drop jumps but shifted to
a stretch-shorten pattern when subjects landed from greater
drop heights (43). The stretch-shorten pattern exhibited by the
monoarticular goat TrLAT during landing from downward
jumps also parallels the pattern observed for the monoarticular
human soleus in both low- and high-intensity drop jumps (43).
Muscle work and elbow work. Consistent with our predictions, patterns of energy absorption and production of the goat
TrLAT also generally followed patterns of elbow joint work
more closely than those of the TrLONG. For instance, in the lead
limb the monoarticular TrLAT absorbed energy during elbow
flexion and produced energy during elbow extension, whereas
the biarticular TrLONG produced energy throughout stance
(Figs. 4D and 7D). A similar contrast in muscle work production was found between the two muscles in the lag limb (Table
J Appl Physiol • VOL
4). However, in downward jumps, both muscles followed the
pattern found in the elbow: stretching to absorb energy early in
stance as the elbow flexed (Fig. 7D), with neither muscle
contributing significant positive work during elbow extension.
A major result of this study that might be predicted from
force-velocity effects is that net shortening by a monoarticular
muscle may not indicate a net contribution of work across a
joint: on average, the TrLAT did not produce net work over
stance, even when there was net fascicle shortening under load,
as in the lead limb of an upward jump. Because muscles can
produce greater forces when actively stretched than when
shortening (19), the TrLAT was estimated to have absorbed
more energy while stretching than it produced during shortening in the lead limb due to this force-velocity effect (Fig. 7D).
In contrast to the TrLAT, the biarticular TrLONG shortened to
produce work throughout stance in both the lead and lag limb
of upward jumps. Thus, when work production is required of
the elbow, the biarticular TrLONG appears to contribute most of
the positive work, whereas the TrLAT predominately absorbs
energy while resisting elbow flexion.
Alternate stretch-shorten cycles, similar to that found in the
TrLAT have been interpreted as periods of work absorption and
production in other muscles, such as the vastus lateralis of rats
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Fig. 7. Histogram showing means (⫾SE) across the 4 individual
goats and 3 jump conditions for muscle strain (A), muscle strain
rate (B), mean muscle stress (C ), and muscle work (D) during
TrLAT stretch, TrLAT shortening, and over net stance. *Significant difference among jump types in Tukey’s HSD post hoc
tests with a starting ␣ of 0.05. {Significant differences between muscles with gray indicating a difference in the lag
limb, and black indicating a difference in the lead limb
(statistics given in Table 2). Parameter values shown in the
figure are also presented in Table 4. The TrLAT absorbed
substantial work as it stretched concurrent with elbow flexion
and joint work absorption. In contrast the TrLONG generated
work in both the lead and lag limb of upward jumps, but
absorbed energy in downward jumps. This shift appeared to
be mediated by changes in the relative kinematics of the elbow
and shoulder.
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MUSCLE FUNCTION IN MONO- AND BIARTICULAR MUSCLES
Table 4. Muscle parameters for the long and lateral heads of the triceps brachii of jumping goats
Strain Rate (FL s⫺1)
Strain (⌬l/lo)
Long
Lateral
Long
Work (J kg⫺1)
Stress (kPA)
Lateral
Long
Lateral
Long
Lateral
Up Jumps
Lead limb
TrLAT stretch
TrLAT shortening
Stance
Lag limb
TrLAT stretch
TrLAT shortening
Stance
⫺0.07⫾0.01
⫺0.10⫾0.02
⫺0.17⫾0.02
0.05⫾0.02
⫺0.13⫾0.04
⫺0.08⫾0.03
⫺0.47⫾0.05
⫺0.53⫾0.05
⫺0.51⫾0.05
0.89⫾0.39
⫺1.97⫾0.80
⫺0.78⫾0.30
100⫾25
99⫾16
99⫾19
259⫾44
130⫾48
185⫾42
4.7⫾1.3
10.1⫾3.0
14.8⫾4.0
⫺13.0⫾3.5
5.1⫾3.4
⫺7.8⫾3.2
⫺0.05⫾0.03
⫺0.11⫾0.04
⫺0.17⫾0.04
0.14⫾0.04
⫺0.09⫾0.03
0.05⫾0.02
⫺0.38⫾0.23
⫺0.41⫾0.12
⫺0.38⫾0.09
1.92⫾0.54
⫺1.02⫾0.46
0.35⫾0.15
101⫾13
62⫾8
76⫾6
253⫾58
99⫾38
166⫾33
1.4⫾2.6
5.3⫾1.5
6.7⫾3.9
⫺33.7⫾5.6
⫺1.5⫾1.5
⫺34.7⫾6.8
117⫾30
17⫾10
65⫾19
142⫾39
8⫾4
82⫾25
⫺14.1⫾4.9
0.8⫾0.5
⫺13.4⫾4.8
Down Jumps
Landing limb
TrLAT stretch
TrLAT shortening
Stance
0.13⫾0.03
⫺0.07⫾0.03
0.06⫾0.01
0.19⫾0.05
⫺0.11⫾0.03
0.08⫾0.03
0.73⫾0.07
⫺0.34⫾0.10
0.15⫾0.01
2.44⫾0.88
⫺1.47⫾0.41
0.54⫾0.18
⫺24⫾2.79
0.2⫾0.5
⫺21.9⫾2.6
Means ⫾ SE of 4 individual means for muscle parameters for the long and lateral heads of the triceps brachii of jumping goats.
perform less work for a given elbow extension, because the
whole muscle-tendon unit is displaced due to shoulder extension. Reduced shortening rates in the TrLONG may, therefore,
indicate power transfer from the shoulder to the elbow through
this muscle head. However, architectural differences between
the two muscles may also affect their fascicle strain behavior,
which could influence our interpretation of energy transfer via
the TrLONG.
Another way to test for energy transfer is to compare the
work done by the elbow during extension with that done by
the two muscles. In fact, In the lead leg of an upward jump the
combined work of the TrLONG and TrLAT during elbow extension was ⬃15 J/kg (Table 4), significantly less than the work
done at the elbow (⬃ 46 J/kg; P ⬍ 0.05). This strongly
indicates that power transfer occurs from shoulder extensors,
operating as antagonistics to the TrLONG, although it is also
possible that energy storage and return from elastic structures
may explain some of this difference (16). Consistent with our
interpretation, proximal to distal joint energy transfer has been
hypothesized to occur in human and animal movement (36, 37,
Fig. 8. Least-square regression correlations between
muscle work (y-axis) and fascicle strain (x-axis) for the
TrLONG and TrLAT during the phases determined by
TrLAT stretch, TrLAT shortening and net over stance for
the lead limb (F) and lag limb (E) of an up jump, and for
down jumps (red ‚). Correlations were higher in the
TrLONG overall. Correlations for both muscle heads
were lowest during elbow extension, indicating that
muscle stress most strongly determined work output
during this period. Correlations were assessed on the
basis of pooled data from all individuals. A weak
correlation between muscle work and fascicle strain
indicates that work was determined by muscle stress.
Two samples were simultaneously recorded from the
long head as in Fig. 1.
J Appl Physiol • VOL
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(14) and the iliotibialis lateralis pars postacetabularis (ILPO) of
turkeys (38). Additionally, the rat VL (14) and turkey ILPO
(38) were found to meet demands of increased joint work
production or absorption by decreasing or increasing fascicle
stretch. Likewise, the TrLAT underwent less stretch when joint
work was required in the lead limb of an upward jump and
greater stretch when more energy was absorbed across the
elbow joint as the animals landed from downward jumps.
Unlike the rat VL and turkey ILPO, however, the goat TrLAT
did not increase the magnitude of fascicle shortening to produce more work during elbow extension. Instead, work production during fascicle shortening appears to be modulated
mainly by the level of activation and stress developed in the
muscle (Fig. 8B).
Energy transfer via the biarticular TrLONG. One of the
proposed functions of biarticular muscles is to transfer power
between joints (43). The lower strain rates measured in the
TrLONG relative to the TrLAT in upward jumps, may indicate
that shoulder extension reduces the effect of elbow extension
on TrLONG fascicle strain. Thus TrLONG fascicles would need to
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MUSCLE FUNCTION IN MONO- AND BIARTICULAR MUSCLES
J Appl Physiol • VOL
muscles functioned similarly to absorb work during landing.
As this study demonstrates, empirical measurement of muscle
strain in relation to muscle and joint work output is key to
analyzing how synergist muscles function to modulate work
and force across a common joint.
ACKNOWLEDGMENTS
Pedro Ramirez maintained and helped to train the goats used in this study.
Carlos Moreno, Russell Main, Craig McGowan, Edwin Yoo, Ivo Ros, Kieth
Egan, and Trevor Higgins aided in data collection. Craig McGowan also
donated his inverse dynamics script. The comments and attention of three
anonymous reviewers were indispensable in improving this manuscript.
GRANTS
This research was supported by National Institutes of Health Grant AR047679 to A. A. Biewener.
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45). However, to our knowledge, this is the first study to use
direct measurements of in vivo fascicle strain to quantitatively
estimate the amount of energy transferred by a biarticular
muscle.
Limitations of the stress-partition model. Because joint moments alone cannot determine muscle stress when more than
one muscle crosses a joint, we used differences in relative
fascicle velocity and fascicle strain to partition stress based on
the inherent force-velocity and force-length characteristics
modeled for the two muscles (18, 19). Muscle force is also
affected by differential recruitment within a muscle. However,
this was not included in our models because EMG amplitude
provides only a rough estimation of muscle recruitment (28)
and is strongly dependent on variable contractile conditions of
the muscle, as we observed here.
Nevertheless, we observed a correspondence between muscle stress and normalized EMG intensity that provides an
independent validation of our stress-partitioning model. During
upward jumps, the goat TrLONG and TrLAT displayed a correlated increase in mean stress with increased EMG intensity in
the lead limb compared with the lag limb (Fig. 5A vs. Fig. 7C).
However, when animals landed from downward jumps, EMG
intensity of the two muscles was greater than that predicted
based on estimates of muscle stress alone. One explanation for
this discrepancy is antagonist cocontraction of elbow flexors,
which would lead to a underestimation of muscle stress in the
triceps. Antagonist cocontraction across the knee and hip has
been found within the biceps femoris and rectus femoris in
humans prior to and during landing from a downward jump
(26, 33). Similarly, antagonist cocontraction during landing in
goats might well occur to stabilize the elbow during the rapid
switch from an extensor to a flexor moment at the elbow after
landing (Fig. 3). Therefore, our estimates of energy absorption
during landing may underestimate actual energy absorption by
the triceps. Antagonist cocontraction may have also been
present during upward jumps, but it is unclear why goats would
employ such a motor pattern, as this would reduce the work
produced at the elbow and limit overall jumping performance.
Finally, our model for calculating muscle stress did not
include history-dependent effects, such as stretch-induced
force enhancement (7), which may have increased work production in the TrLAT. On the basis of the results of (11),
however, only a 12% increase in torque due to the force
enhancement following prestretch would be expected, which
would still have been insufficient for the TrLAT to produce
positive work over stance in the lead limb (values from Table
4), although it may have resulted in positive work production
in the TrLAT during extension in the lag limb.
Conclusions. The anatomical differences between the biarticular TrLONG and the monoarticular TrLAT of goats resulted in
differences in muscle function with respect to elbow joint
kinematics and work. In general, consistent with our hypothesis and as suggested previously (44), the shortening pattern
and work of the monoarticular TrLAT followed the kinematics
and work of the elbow joint more closely than the biarticular
TrLONG during the flexion and extension periods of stance.
Over the duration of stance, however, the TrLAT did not
produce significant positive net work, despite net fascicle
shortening. As a result, the TrLONG appeared to be mainly
responsible for powering upward jumps, while the TrLAT
generated force and absorbed the work of elbow flexion. Both
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