Muscle force-length dynamics during level versus incline locomotion: a comparison of in vivo performance of two guinea fowl ankle extensors
Concord Field Station, Department of Organismic and Evolutionary Biology, Harvard University, Bedford, MA 01730, USA
* Author for correspondence (e-mail: mdaley{at}oeb.harvard.edu)
Accepted 19 May 2003
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Summary |
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Key words: muscle, strain, phase, work, sonomicrometry, gastrocnemius, digital flexor, guinea fowl, Numida meleagris
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Introduction |
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These differences in mechanical roles between proximal and distal limb
muscles may relate to muscle-tendon morphology. Proximal muscles generally
have long parallel muscle fibers with little or no free tendon, suggesting the
capacity to shorten or stretch over relatively long distances, which may favor
a role in work modulation. Distal muscles tend to have short, pennate fibers
that transmit force via long free tendons, an architecture that
favors force generating capacity per unit mass, and storage and release of
elastic energy in the tendon (Ker et al.,
1988; for reviews, see
Biewener, 1998
;
Biewener and Roberts, 2000
).
Thus, a division of labor is likely to exist among limb muscles resulting from
limb and muscle-tendon morphology.
In addition to performing diverse mechanical roles in a given locomotor
task, muscles may differ in their ability to change force development and
energy output across tasks. However, few studies have investigated how muscle
performance changes to mediate behaviors with different force and energy
demands. A clear example of the capability to distinctly shift mechanical
function between tasks is demonstrated by the wild turkey Meleagris
gallopavo lateral gastrocnemius (LG), which contracts with limited length
change (strain <6%) during steady running, but provides significant
positive work during incline running by shortening substantially (strain
>10%) while generating force (Roberts
et al., 1997). In addition, external power measurements during
large accelerations in wild turkeys suggest power production by all limb
muscles, which implies that most limb muscles must be capable of such a
mechanical shift (Roberts and Scales,
2002
). Yet, in contrast to the turkey LG, in vivo
recordings of force-length behavior in the LG and plantaris of tammar
wallabies Macropus eugeni reveal that the low energy production by
these muscles does not change when the animals hop on an incline
versus a level surface (McGowan
and Biewener, 2002
). Similarly, the mallard Anas
platyrhynchos LG exhibits a limited ability to shift its mechanical
performance when ducks swim versus when moving over ground. During
both behaviors, the mallard LG shortens considerably (from 24% to 37% strain)
while producing force to do substantial work
(Biewener and Corning, 2001
).
Perhaps this is not surprising, since mallards are specialized for swimming in
addition to terrestrial locomotion. Nonetheless, given these different
findings, it remains unclear whether all limb muscles can adjust their
mechanical performance to accommodate different locomotor behaviors.
Consequently, we seek to explore this issue by examining the in
vivo force, length and muscle activity patterns of two ankle extensors of
the guinea fowl Numida meleagris; the lateral gastrocnemius (LG) and
the digital flexor to the lateral toe (DF-IV). Our general goal is to
investigate the capacity of these two muscles for modulating force and work
production to meet the mechanical demands of level versus incline
locomotion. A similar recent study of the turkey peroneus (fibularis;
Gabaldón and Roberts,
2002) has also been carried out. Guinea fowl are good runners,
known to travel 30-50 km day-1 while foraging
(Crowe, 1994
;
Forshaw, 1998
). Therefore, we
expect the LG and DF-IV to contract with little length change during level
running for greater force economy, but to shorten substantially during incline
locomotion to increase energy production, similar to the turkey LG
(Roberts et al., 1997
).
However, due to its smaller size, the guinea fowl may have a more compliant
(flexed joint) gait than the turkey
(Gatesy and Biewener, 1991
),
which could affect the contractile behavior of its limb muscles. In contrast
to turkeys and guinea fowl, mallards are specialized for swimming in addition
to terrestrial locomotion but are approximately the same size as guinea fowl.
Thus, study of the guinea fowl ankle extensors provides a comparison of two
cursorial avian species of differing size, as well as two species of similar
size but differing locomotor specialization.
Study of the guinea fowl LG and DF-IV also provides an opportunity to
compare the contractile function of two agonist limb support muscles. These
two muscles have short pennate muscle fibers and long free tendons
(Baumel, 1993), which suggest
that force economy is an important mechanical role of both (reviewed by
Biewener and Roberts, 2000
).
However, whereas the gastrocnemius crosses the knee and ankle joints, the
digital flexors cross the knee, ankle, tarso-metatarso-phalangeal (TMP) and
all distal phalangeal joints (Baumel,
1993
). Thus, the DF-IV crosses more joints and possesses a longer
free tendon than the LG (Baumel,
1993
), which may introduce greater compliance in-series with the
muscle fibers and facilitate greater elastic energy savings. Thus, although
the LG and DF-IV are architecturally similar, differences in tendon length and
the joints that each muscle crosses may lead to differences both in their
contractile function and how each is used to modulate changes in locomotor
performance. By comparing energy production and modulation between these two
muscles, we hope to gain greater insight into the relationship between
morphology and the dynamics of muscle mechanical function.
Finally, the power and work output of a muscle over a contraction cycle is
sensitive to the timing and amplitude of strain relative to force development
(e.g. Josephson and Stokes,
1989; Askew and Marsh,
1997
), which are strongly affected by the pattern of muscle
stimulation as well as the interaction between the active muscles and the load
upon which they act (see Josephson,
1999
; Marsh,
1999
). Consequently, muscle force and work output may be adjusted
by altering the timing and intensity of muscle activation, the mechanical
interaction between the limb and environment, or both
(Gillis and Biewener, 2000
).
In this study, we examine how muscle activity, force development and energy
output vary in the LG and DF-IV as a function of speed and incline. Because
peak muscle force can be expected to increase with speed due to a decrease in
duty factor (Gatesy and Biewener,
1991
), whereas net muscle work must increase with incline to
increase the potential energy (PE) of the center of mass of the body (COM), we
can also compare muscle performance as a function of speed versus
incline. To maintain force economy during level locomotion, increases in
muscle force with speed should occur with minimal increase in muscle
shortening work. During incline locomotion, net muscle work must increase. One
possible way to accomplish this is for all muscles in the limb to contribute
equally to increased energy production (i.e. changes in mass-specific work are
similar among muscles). Alternatively, certain muscles may contribute more to
work production by shortening more than others. We address these two
possibilities by comparing the mass-specific work performed by the guinea fowl
LG and DF-IV when running on the level versus an incline, relative to
the mass-specific work required to increase the PE of the COM during incline
locomotion.
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Materials and methods |
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Muscles
The two ankle extensor muscle groups of birds are the gastrocnemius, with
large lateral and medial heads and one smaller intermediate head, and the
digital flexors, which have superficial, middle and deep layers. Each digital
flexor layer has heads that insert via tendons to all four toes
(Baumel, 1993). Both muscle
groups have relatively long free tendons, allowing direct measurement of
muscle-tendon force for certain muscle components
(Fig. 1).
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Muscle activity and strain were recorded in the lateral head of the gastrocnemius (LG) and the superficial digital flexor to the lateral toe (DF-IV) by electromyography (EMG) and sonomicrometry (see below). These measurements were combined with recordings of muscle-tendon force for the common gastrocnemius tendon and the free tendon of DF-IV using tendon force buckles (Fig. 1). The DF-IV was chosen for ease of access and because its muscle belly inserts individually to a single tendon. It is impossible to relate muscle strain directly to force measurements for the other digital flexor muscle bellies because they originate and insert onto each other and have overlapping attachments to the tendons of digits II and III, making them mechanically interdependent.
Surgical procedures
The birds were anesthetized for surgery using isoflurane delivered through
a mask. After induction at 3%, the bird was prepared for sterile surgery.
During the subsequent surgical procedures anesthesia was maintained at 1-2%
isoflurane while monitoring the animal's breathing rate. Recording electrodes
and transducers were passed subcutaneously to the shank from a 1-2 cm dorsal
incision over the synsacrum. A second 4-5 cm incision was then made on the
lateral side of the left shank, overlying the division between the anterior
and posterior muscular compartments, to expose the LG and its tendon. Freeing
the lateral border of the LG provided access to the deeper DF-IV. After
exposing the DF-IV muscle and its tendon, their identity was verified by
gently pulling on the tendon to observe flexion of the lateral digit.
E-type stainless steel tendon buckle force transducers were used as
described in previous studies (Biewener et
al., 1998; Biewener and
Corning, 2001
). Because the lateral, intermediate and medial heads
of the gastrocnemius do not have separate free tendons, a buckle placed on the
common gastrocnemius tendon measured the total force exerted by all three
heads. Measurement of force from the common tendon and muscle length change
from the lateral head necessitated the assumption that all heads of the
gastrocnemius contributed equally to mass-specific work, in order to estimate
the work contributed by this muscle as a whole.
Sonomicrometry crystals (Sonometrics Inc., London, Canada) were implanted into small openings made with fine forceps within the muscle, approximately 3-4 mm deep along the axis of the fascicles. After verification of good alignment and signal quality, the crystals were secured using 5-0 silk suture to close the muscle opening. In the LG, 2.0 mm crystals were spaced approximately 10 mm apart in the middle third of the muscle belly. For the much smaller DF-IV, 1.0 mm crystals were implanted approximately 7 mm apart in the middle portion of the belly (Fig. 1).
Fine-wire (0.1 mm diameter, California Fine Wire, Inc., Grover Beach, USA) twisted, silver bipolar EMG hook electrodes (0.5 mm bared tips with 1 mm spacing) were implanted using a 23 gauge hypodermic needle immediately adjacent to each pair of sonomicrometry crystals and secured to the muscle's fascia using 5-0 silk suture. Skin incisions were sutured using 3-0 silk. The lead wires from all transducers were pre-soldered to a small epoxy-mounted, insulated connector (3xGM-6 Microtech, Inc., Boothwyn, USA). After closing the incision over the synsacrum, the connector was sutured to the skin of the back using 3-0 silk and covered with elastic surgical tape.
Each guinea fowl was allowed to recover for 24-36 h after surgery. All birds could walk and run the following day without apparent lameness. Experimental recordings took place over the subsequent 2 days. Once the experiments were completed, the guinea fowl were killed by an intravenous injection of sodium pentobarbital (100 mg kg-1).
Muscle data and video recording
In vivo recordings of muscle strain, EMG and force were made
via a lightweight 8 m shielded cable (Cooner Wire, Chatsworth, USA)
attached to the micro-connector on the bird's back. The cable connected at the
other end to a Triton 120.2 sonomicrometry amplifier (Triton Technology Inc.,
San Diego, USA), a strain gauge bridge amplifier (Vishay 2120,
Micromeasurements, Raleigh, USA), and EMG amplifiers (Grass, P-511, West
Warwick, USA). EMG signals were amplified 1000x and filtered (60 Hz
notch, 100-3000 Hzbandpass) before sampling. The outputs of these amplifiers
were sampled by an A/D converter (Axon Instruments, Union City, USA) at 2500
Hz and stored on a computer for subsequent analysis. Because the filters in
the Triton sonomicrometry unit introduced a 5 ms phase delay, all length
measurements were corrected for this offset before being related to muscle
force, EMG and limb kinematics.
Digital high-speed video was recorded in lateral view at a rate of 250 frames s-1 (Redlake Motionscope PCI 500, San Diego, USA). A post-triggered voltage pulse stopped the video recording and synchronized the video sequence to the in vivo muscle recordings of force, length and EMG activity.
Force buckle calibration
After completing all in vivo recordings, the tendon force buckles
were calibrated in situ post mortem by cutting the proximal end of
each tendon and tying it to a Kistler 9203 force transducer (Amherst, USA) 00
silk suture. The distal attachments of the tendons were left intact. Before
applying tension, the sutured end of the tendon was secured by freezing it in
a shallow dish of liquid nitrogen. Tension was applied cyclically to the
tendon until the loads exceeded the maximum output recorded in vivo
for 3-4 cycles. We obtained a dynamic calibration of each buckle using a
least-squares linear regression fit to the rise and fall of the buckle output
versus applied force measured from the force transducer. All buckle
calibration regressions yielded r2>0.992 with an
average difference in the rise and fall of force of 3±1% (mean ±
S.D.).
Morphological measurements
After the buckle calibrations were complete, we removed the buckles and
inspected the tendons to verify lack of visible damage. Each muscle was then
dissected free to confirm placement of sonomicrometry crystals and EMG
electrodes, and to obtain measurements of wet muscle mass, mean fascicle
length and pennation angle. This allowed us to calculate muscle physiological
cross-sectional area A, assuming a muscle density of 1060 kg
m-3 (Table 1). The
anatomical length L of each tendon was measured (equal to the
muscle-tendon length minus mean fascicle length), and a measured section of
free tendon was weighed to determine average tendon cross-sectional area,
assuming a density of 1120 kg m-3
(Ker, 1981). For two guinea
fowl, all hindlimb muscles were dissected and weighed (80±4 g). Using
these measurements, the total mass of the gastrocnemius and digital flexors
(24±3 g) comprised 30% of total hindlimb muscle mass.
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EMG analysis
For each stride cycle analyzed, EMG recordings were baseline-corrected to
zero offset and used to quantify onset phase, offset phase, duration and
intensity. Intensity was measured as mean spike amplitude of the rectified
signal, and reported as a fraction of the largest mean spike amplitude
recorded from each bird while it ran at the highest speed (2.0 m
s-1). The relationship between activation intensity and mechanical
force or work of a muscle is not necessarily constant because it is sensitive
to numerous factors, including force-length and force-velocity effects, and
the recent work history of the muscle (e.g. see
Josephson, 1999;
Marsh, 1999
). To investigate
whether the relationships between EMG intensity and mechanical force or work
changed from level to incline locomotion for the LG and DF-IV, we used a
two-way model I analysis of variance (ANOVA) described below.
Sonomicrometry
Sonomicrometry techniques and analysis followed those described by Biewener
and Corning (2001). Signals
were corrected for offset errors (underestimate of length) introduced by the
greater velocity of sound through the epoxy coating of each crystal compared
with the muscle. These were found to be 0.16 mm for the 1 mm crystals, and
0.82 mm for the 2 mm crystals, based on direct measurements made in a water
bath with the crystals mounted on a digital caliper. Fractional length changes
(
Lseg/Lo) of the muscle's
fascicles were calculated based on segment length changes measured between the
crystals (Lseg) relative to the resting length
(Lo), which was measured while the animal stood at rest.
As a convention, shortening strains are negative, and lengthening strains are
positive. Total fascicle length change was calculated as fractional length
multiplied by the mean fascicle length of the muscle (Lf).
Crystal alignment relative to the fascicle axis (
) was verified
post-mortem, and found to be within ±3°, indicating that
errors due to crystal misalignment, equal to (1-cos3°), were <0.01
(1%).
Measurement of overall muscle length change based on one pair of sonomicrometry crystals assumes that fractional length changes measured between the crystals are representative of the fascicle as a whole and of all fascicles within the muscle. Because both muscles under investigation in this study have relatively short muscle fascicle lengths (LG, 17.3 mm±1.2 mm; DF, 17.1 mm±5.7 mm, mean ± S.D.), segment length measurements obtained from the crystals represent a substantial portion of whole fascicle length. Although regional differences in fascicle strain within a whole muscle may exist and deserve future study, they are not examined here.
Muscle work and tendon energy recovery per stride
Changes in instantaneous muscle length determined by sonomicrometry were
differentiated to obtain muscle velocity and multiplied by instantaneous force
to calculate muscle power. For pennate muscles, length changes measured along
the fascicles overestimates whole muscle length change and thus, muscle work
and power. However, because the pennation of the muscles averaged 20° (LG)
and 21° (DF-IV) (Table 1),
the resulting overestimate in muscle length change is <6.6%
[=(1-cos)x100], and being similar for both muscles, is unlikely
to alter the interpretation of the results. Muscle power was integrated over
each stride to provide a cumulative measure of work, in which the final value
represents the net muscle work per stride. To characterize the effects of
strain, force and their relative timing on the net work produced by each
muscle, we measured the following variables for each stride, normalized as a
fraction of stride duration: time of peak force, time of peak muscle length,
the change in muscle shortening velocity during force production
(
velocity), and the phase between peak force and peak muscle length
(phase).
Elastic energy recovered from each tendon per stride was calculated based
on peak tendon stresses, assuming a tendon stiffness of 0.34 GPa
(Buchanan and Marsh, 2001) and
a hysteresis of 7% (Ker,
1981
).
Muscle work and center of mass work
To assess the shift in energy production by the muscles from level to
incline running, we compared the total energy contribution by these two
muscles as a group to the overall increase in potential energy of the animal's
COM. We estimated the total work contributed by the gastrocnemius and digital
flexors by assuming that all heads of each muscle contributed the same
mass-specific work as the single head that was measured (LG and DF-IV). The
work done during each step to increase the PE of the COM was calculated using
the high-speed video to determine the animal's stride length
(Ls). The PE increase is equal to
mgh, where m is the bird's
mass, g is the acceleration due to gravity and
h is the change in height of the body during each stride
cycle, which equals Lssin(16°).
Statistical analyses
Ten steady strides for each running condition (speed and grade) were
analyzed. Strides were considered steady if the bird maintained fore-aft
position on the treadmill belt. A three-way, mixed-model ANOVA was used to
assess the effects of incline and speed, treating individual as a random
effect and speed and incline as fixed effects. We tested whether speed and
incline had a significant effect (P<0.05) on mean muscle-tendon
force, net active muscle strain, net muscle work, EMG duration and intensity.
To account for the number of simultaneous ANOVAs performed, the significance
level for each test was adjusted using the sequential Bonferroni technique
(Rice, 1989). To assess the
effect of EMG intensity on mean force and net mechanical work within each
condition, we used a two-way model I ANOVA, treating individual and EMG
intensity as effects. To characterize the relative effects of net strain, mean
force, phase and
velocity on work, a general linear model was used that
included first order interaction effects. Student's paired t-tests
were used for all paired comparisons. Statistical tests were performed using
Systat (version 9.0 for the PC). Unless otherwise stated, average values given
in the text are means ± S.E.M.
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Results |
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In addition to operating at different muscle stresses, the two muscles exhibited different length-change patterns. The LG shortened throughout most of force production, becoming relatively isometric during the latter half of support and then stretched slightly at the end of support. In contrast, the DF-IV typically lengthened until peak force, and shortened rapidly during force decline. Although active shortening strains were similar in magnitude for the LG and DF-IV, averaging -16±2% and -12±3% of Lo, respectively, active stretch of the DF-IV averaged 11±3%, compared to only 3±1% of the LG (not shown). Thus, the average net strain over the support phase for the LG was -13±3% versus -1±6% for the DF-IV during level running at 1.3 m s-1.
Variability in strain, force and work: LG versus
DF-IV
Certain characteristics of the force-length behavior of the DFIV were
consistent across individuals; this muscle operated at higher muscle stresses
than the LG, stretched during the beginning of the support phase of the stride
and shortened during the later half of support. However, DF-IV force and
strain performance varied significantly more from stride to stride than that
of the LG (Fig. 3). The mean
coefficient of variation (CV) for muscle strain was 19% for the LG and 30% for
the DF-IV (P<0.001), and the mean CV for muscle force was 16% and
28%, respectively (P<0.001). Whereas the CV for LG muscle strain
did not significantly differ between swing and stance phases of the stride
(P=0.2450), the CV for DF-IV muscle strain significantly increased
during the support phase of the stride (P=0.0044), averaging 14%
during swing versus 46% during stance. Thus, DF-IV varied
substantially more during force development, yielding greater variation in
work production.
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The stretch-shorten pattern of the DF-IV also yielded large changes in muscle fascicle velocity during force production, which caused work production to be sensitive to the relative timing of muscle force and strain (phase). As a consequence of the greater variability in force and strain of the DF-IV compared to the LG, as well as the increased dependence of work the timing between the two, energy production by the DF-IV varied widely, both stride-to-stride and among individuals (Fig. 4), even though the DF-IV averaged little net work per stride on the level. Both intra- and inter-individual variation in energy production per stride was greater in the DFIV than in the LG (Fig. 4), and the variation in energy production by the DF-IV is greater than would be expected based on the variation in force and strain alone (Fig. 3).
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Energy production by the LG and DF-IV
Net muscle work produced per stride is the area enclosed in a work loop, a
graph of muscle force versus muscle length. To allow direct
comparison of the two differently sized muscles, we plot muscle stress (kPa)
against muscle strain (L/Lo), such that
the area enclosed in the work loop represents the volume- or mass-specific
work performed over the locomotor cycle
(Fig. 5). The timing of EMG
relative to force production did not change substantially with speed. Little
variation existed among individuals in the general shape and direction of the
work loop of the LG. This muscle often absorbed a small amount of energy
during late swing phase as the muscle was passively stretched
(Fig. 4). It then became active
just before ground contact, shortened under relatively low muscle stress for
most of the support phase of the stride, and stretched slightly near toe-off
(Fig. 5). Under all conditions
in this study, the LG generated a counter-clockwise work loop, indicating net
energy production. The LG produced 7.7±1.5 J kg-1
(56±12.2 mJ) per stride during level, intermediate speed running (1.3 m
s-1, Table 2). In
contrast to the positive work performed by the LG, the DF-IV averaged
approximately zero net work during level running
(Fig. 5). The DF-IV
demonstrated a more spring-like force-length pattern during the support phase
of the stride, becoming active just before heel-strike, stretching until
approximately peak muscle force, and subsequently shortening during force
decline (Fig. 5). Overall, the
DF-IV shortened and lengthened by similar amounts during force production, so
that work produced by this muscle averaged only -0.8±2.7 J
kg-1 (-1.9±5.3 mJ) per stride during level running at 1.3 m
s-1 (Table 2).
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Changes in muscle performance with speed
As speed increased, general patterns of muscle activation, force production
and muscle strain remained similar. However, peak force, mean force and EMG
intensity increased with speed, while EMG duration decreased, for both muscles
(Table 2). With increasing
speed, LG peak force increased significantly (P<0.0001) from
20.9±1.9 N to 33.6±3.4 N, while DF-IV peak force increased
significantly (P<0.0001) from 9.3±1.1 N to 13.6±1.4
N. Again, these forces correspond to higher peak muscle stresses for the DF-IV
(Table 2,
Fig. 6). In concordance with
the increase in force, EMG intensity increased significantly with speed for
both muscles (Table 3; LG,
P=0.0068; DF-IV, P=0.0095). In contrast, EMG duration
decreased significantly with speed for the DF-IV (P=0.0002), and
similarly for the LG, although the trend was not significant after Bonferroni
correction (Table 3).
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Net shortening strain and net muscle work per cycle (Fig. 6) also increased significantly with speed for the LG. Net active shortening by this muscle increased from 10.5±2.3% to 15.2±3.0% (P=0.0008), whereas net energy produced per stride by the LG increased from 4.5±0.9 to 11.4±2.1 J kg-1 (P=0.0001) from the slowest to the fastest speed on the level (Fig. 6). In contrast, for the DF-IV, net strain and net muscle work per stride did not differ significantly with speed (Table 3).
Tendon elastic energy storage
On a (muscle+tendon) mass-specific basis, the DF-IV recovered substantially
more strain energy from its tendon than did the LG
(Table 2,
Fig. 6). For example, during
level running at 1.3 m s-1, elastic energy recovery in the LG
tendon averaged only 2.5±0.6 J kg-1, whereas the DF-IV
tendon recovered 14.2±2.3 J kg-1. In both tendons, the
energy savings increased with speed and incline due to the significant
increase in peak muscle-tendon force under these conditions. LG tendon savings
did not exceed 5 J kg-1 and were less than half of the
mass-specific net muscle work, whereas DF-IV tendon energy recovery reached
21.1±8.8 J kg-1, greatly exceeding DF-IV muscle shortening
work (Table 2, Fig. 6). This difference in
tendon energy storage reflects the longer length and higher operating stress
of the DF-IV tendon. Given that the ratio of muscle to tendon cross-sectional
area is lower in the DF-IV than the LG
(Table 1), this difference is
not a result of the DFIV having a relatively thinner tendon.
Level versus incline locomotion
For both muscles, the net work generated per stride tended to increase when
the birds moved up a 16° incline (Figs
5,
6). However, the change in
muscle work from the level to an incline was not significant after Bonferroni
correction for the DF-IV, due to its higher stride to stride variability
(Table 3; LG,
P=0.0018; DF-IV, P=0.0380). In fact, although the DF-IV
averaged net energy production during incline running, it absorbed energy in
28% of strides on the incline (compared to 57% of strides on the level;
N=120 and 170, respectively). On average, LG net work increased by
6.5 J kg-1 and 4.3 J kg-1 at 0.7 m s-1 and
1.3 m s-1, respectively (Table
2). The increase in energy production by the LG during incline
locomotion occurred through a combination of increased mean force
(P=0.009) and net shortening strain (P=0.0035)
(Fig. 6). The DF-IV also showed
trends for increasing mean force and net shortening strain on an incline
(Table 2), with net active
shortening increasing primarily through a decrease in active stretch
(Fig. 6); however, these trends
were again not significant after Bonferonni correction
(Table 3, mean force,
P=0.0152; net strain, P=0.0289).
Relationship between EMG intensity and muscle work and force
During level locomotion, peak force showed a significant linear
relationship with EMG intensity for both muscles
(Table 4, LG,
P<0.0001; DF-IV, P=0.0041)
(Fig. 7); however, the
relationship was much stronger for the LG. Because the amplitude of EMG
activity relative to peak muscle force can be expected to differ among
individuals because of differences in electrode geometry and recording site
(see Loeb and Gans, 1986), the
slope of the relationship between EMG intensity and force (or work, see below)
also can be expected to differ among individuals. Despite such differences,
the pattern of change in EMG intensity relative to muscle force between level
and incline was consistent among the individual animals sampled. Consequently,
we report the averages of the slopes obtained among individuals for each
treatment. The average slope of the relationship (force over relative
intensity, N) was 23 N for the LG (mean r2=0.65) but only
10 N for the DF-IV (mean r2=0.33). During incline running,
LG muscle force still demonstrated a significant linear relationship with EMG
intensity, with an average slope of 34 N (mean, r2=0.58,
P<0.0001), but the DF-IV did not (P=0.6279,
Table 4,
Fig. 7).
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Similar to peak muscle force, LG muscle work (averaged across individuals) was also positively correlated with EMG intensity during both level (mean r2=0.55) and incline (mean r2=0.50) locomotion (Fig. 7, Table 4), with average slopes of 89 and 102 mJ, respectively. In contrast, DF-IV net muscle work showed no relationship with EMG intensity during level running (P=0.2991), but exhibited a small significant positive trend during incline running with an average slope of 9 mJ (mean r2=0.16, P=0.0373) (Table 4, Fig. 7).
Work output by LG and DF-IV in relation to strain, force and
phase
Because muscle work is the product of muscle force and length change, the
net work produced over the course of a stride depends on the relative timing
of these two variables. If muscle fascicle velocity is constant during force
production, the net work performed by a muscle over the course of a stride is
simply the product of mean force and net fascicle length change. However, when
fascicle velocity varies substantially during force production, the work
generated also depends on the phase relationship between length change and
force. We conducted a general linear model ANOVA to examine the effects of
these factors (mean force, net strain, phase, velocity) on the work
produced by each muscle (Table
5). This analysis revealed that net strain and mean force alone
explain 93% of variation in work for the guinea fowl LG, consistent with the
relatively constant shortening velocity exhibited by this muscle during force
production (Fig. 3). While all
factors had a statistically significant effect on LG net work
(Table 5), phase exerted only a
minor influence on work because it did not vary substantially under the
conditions in this study (Fig.
8). In contrast to the LG, net strain and mean force explained
only 37% of the variation in DF-IV work, while phase and the interaction terms
related to phase explained an additional 32%. Interactions among factors
(force, strain and phase) exhibited a larger influence on DF-IV work than LG
work (Table 5) because the
DF-IV muscle fascicles undergo a dynamic stretch-shorten cycle. Note that
although the bivariate plot of net work against net strain
(Fig. 8) suggests a positive
relationship between these two variables for the DF-IV, the effect of net
strain on work is not significant for the DF-IV once the general lineal model
accounts for interactions among variables, as reflected in the statistical
results in Table 5. Thus, the
LG and DF-IV modulate force-length mechanical performance differently: the LG
through changes in mean force and net strain, and the DF-IV through changes in
their relative timing (Fig.
8).
|
|
Muscle work and COM work
Although the LG produced greater positive energy on the incline, neither
muscle contributed energy proportional to its mass to move the bird's COM up
the incline. The increase in PE of the COM per stride was 1400 mJ at 0.7 m
s-1 and 1700 mJ at 1.3 m s-1. We compared this energy to
the total energy contributed by the gastrocnemius and digital flexors,
assuming all heads of each muscle contributed equally to mass-specific work.
During incline locomotion at 0.7 and 1.3 m s-1, the gastrocnemius
contributed 111±26 and 89±19 mJ (means ±
S.E.M.) greater average energy than during level running at the
same speeds, whereas the digital flexors contributed 38±25 and
63±16 mJ (means ± S.E.M.) greater average energy.
Therefore, together, these muscles contribute approximately 9% (1.3 m
s-1) to 11% (0.7 m s-1) of the additional energy
required for incline running. However, because they represent 30% of the total
hind limb muscle mass (see Materials and methods), they contribute only
one-third of the energy that would otherwise be expected for their mass
(Fig. 9).
|
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Discussion |
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Mechanical performance of the LG and DF-IV in relation to
muscle-tendon architecture
The mechanical performance of the guinea fowl LG and DFIV clearly differ in
a manner that is consistent with differences in their morphology. Because the
ratio of tendon to fascicle length is 10.8 in the DF-IV compared with 5.7 for
the LG, the DF-IV tendon may be expected to provide relatively greater elastic
energy savings (for a given tendon stress). Indeed, according to the model of
Ker et al. (1988), both
muscles have a muscle-tendon morphology that favors elastic energy storage
over muscular control of joint position. However, the peak muscle stresses
developed during terrestrial locomotion by the guinea fowl LG and DF-IV differ
substantially and average only 33 kPa in the LG and 116 kPa in the DF-IV.
Under these peak stresses, the guinea fowl DF-IV tendon undergoes relatively
large extensions, while the LG does not. As a result, the DF-IV contributes
more to elastic energy savings. Whereas the gastrocnemius tendon stores only
1-5 J kg-1 of energy, which amounts to 30-40% of shortening work by
the muscle, the DF-IV tendon stores 12-21 J kg-1 of elastic energy,
exceeding DF-IV shortening work by 2.2- to 2.9-fold.
Although the guinea fowl is considered a cursorial species, it also uses
its hind limbs for behaviors such as propulsion during jumping for flight
take-off and energy absorption during landing. Consequently, the low muscle
stresses in the LG and DF-IV may reflect the capacity to withstand much larger
stresses during these behaviors. The peak muscle stresses measured in the LG
are particularly low compared to those observed in other bipeds: 127 kPa in
the gastrocnemius of the running mallard
(Biewener and Corning, 2001)
and 227-262 kPa in ankle extensors of hopping wallabies
(Biewener and Baudinette,
1995
). In an early study that measured in vivo
muscle-tendon stresses, Biewener and Blickhan
(1988
) showed that the peak
ankle extensor muscle stresses developed during hopping in kangaroo rats
Dipodomys spectabilis were only one-third those experienced during
jumping: 80 versus 297 kPa. Nevertheless, LG muscle stresses are
surprisingly low compared with the stresses developed during steady locomotion
observed in running mallards and hopping wallabies. In part, this may reflect
a more limited range of performance in the case of mallards and the need to
operate at high levels of stress for effective energy savings in the case of
wallabies.
Diversity in LG force-length performance among avian bipeds
Although the pattern of LG muscle activity relative to limb movements,
force development and muscle strain observed in a variety of avian bipeds
during steady terrestrial locomotion is similar
(Jacobson and Hollyday, 1982;
Roberts et al., 1997
;
Gatesy, 1999b
;
Biewener and Corning, 2001
), LG
work performance differs substantially among mallards, turkeys and guinea
fowl, due to varying degrees of shortening during force development. Fascicle
shortening of the guinea fowl LG during force development is between that of
the turkey LG, which contracts with limited shortening (1 to 6%), and the
mallard LG, which shortens substantially (24-37%)
(Roberts et al., 1997
;
Biewener and Corning, 2001
).
The large shortening strains of the mallard LG may not be surprising given
that this bird is specialized for different locomotor modalities; however,
both turkeys and guinea fowl are cursorial ground birds, known to be capable
runners (Forshaw, 1998
). The
difference in size between the guinea fowl and turkey may account for some of
the observed difference in the contractile behavior of the LG. Smaller birds
tend to run with more crouched postures
(Gatesy and Biewener, 1991
),
which may reduce peak muscle-tendon stresses and elastic energy savings
(McMahon, 1985
;
McMahon et al., 1987
), and
therefore require greater muscular work.
Different in-series compliance of muscles among species could explain
different muscle strain amplitudes during stance, because a muscle with a more
compliant tendon might shorten more to take up the stretch of the tendon;
however, this does not appear to be the case. While tendon morphology differs
substantially between species, the stretch of the tendon relative to muscle
fiber lengths at the loads experienced during locomotion are similar. The
gastrocnemius tendon of the guinea fowl is 5.7x longer than the muscle
fascicles, while the mallard LG tendon is 1.4x longer than the muscle
fascicles (Biewener and Corning,
2001), and the compliant element of the turkey gastrocnemius
tendon is 3.2x longer than the muscle fascicles, because a large portion
of the tendon is ossified (Roberts et al.,
1997
). These ratios suggest that the guinea fowl gastrocnemius
tendon extends relatively more than the mallard and turkey tendons at a given
load. However, the loads experienced by the tendons during locomotion differ
between birds due to differences in peak muscle stress, which offsets these
differences in tendon morphology. If the Fiber Length Factor (FLF), the ratio
of muscle fiber length to tendon extension at peak load
(Ker et al., 1988
), is
calculated for each bird using the peak forces measured during terrestrial
locomotion, it is similar for the guinea fowl, turkey and mallard LG (12, 12
and 15, respectively, assuming the ratio of muscle:tendon cross-sectional area
of the turkey is similar to the guinea fowl). Thus, when differences in tendon
length and peak locomotor loads are considered simultaneously, the LG tendons
of the turkey, mallard and guinea fowl function similarly to transmit muscle
force with relatively little extension of the tendon. This suggests that
further differences may exist among these species in muscle physiology, such
as muscle contraction kinetics, that might explain the relatively greater
shortening of the mallard and guinea fowl LG compared to the turkey LG.
The similarity in LG tendon compliance relative to the peak load
experienced during locomotion results in similar elastic energy storage for
the guinea fowl and turkey LG, in spite of the large differences in muscles
stress and shortening work. As mentioned above, the guinea fowl gastrocnemius
tendon stores 1-5 J kg-1 of energy, which is 30-40% of shortening
work of the LG muscle. In comparison, the turkey gastrocnemius tendon stores
1-4 J kg-1, which is 2.5-fold greater than muscle shortening work
(Roberts et al., 1997). The
relatively low tendon compliance of the turkey gastrocnemius tendon, due to
its ossification, offsets the effect of higher muscle stresses experienced
during locomotion. If the guinea fowl gastrocnemius tendon were ossified in
proportion similar to the turkey tendon, it would be less than half as long,
and gastrocnemius elastic energy savings would be reduced to 1.7 J
kg-1 maximum. Likewise, the lower energy storage (2.5 J
kg-1) of the mallard gastrocnemius tendon can be attributed
primarily to its shorter length. It achieves half the mass-specific energy
savings of the guinea fowl tendon because it is approximately half as long (56
mm compared to 99 mm for the guinea fowl tendon)
(Biewener and Corning, 2001
).
In wallabies, which are specialized hoppers, tendon energy storage is 40-80 J
kg-1, which exceeds muscle shortening work by 20- to 36-fold
(Biewener et al., 1998
). Thus,
while the ratio of tendon energy to muscle energy is lower in the guinea fowl
LG than the turkey LG, the mass-specific energy recovered from these tendons
is comparable. The guinea fowl and turkey LG tendons recover twofold greater
energy than the tendon of the non-cursorial mallard, but much less energy than
the ankle extensors of the wallaby. Thus, the level of elastic energy savings
in the tendons of each species is consistent with differences in their
locomotor specialization.
Muscle work modulation for incline running
In addition to investigating the relationship between muscle-tendon
morphology and mechanical performance during level locomotion, we sought to
compare how the guinea fowl LG and DF-IV modulate force-length performance for
incline running. Only the LG significantly increased its net work output when
the animals moved up a 16° incline compared with on a level (4.3-6.5 J
kg-1). This increase is similar to that observed in the turkey LG
(5 J kg-1 on a 12° incline;
Roberts et al., 1997).
However, the contribution of the guinea fowl ankle extensors to the increase
in the animal's COM energy was only one-third of that expected for the
muscles' mass (Fig. 9). This
indicates that proximal limb muscles must contribute proportionately more work
for incline running. Because direct measurements of force are difficult to
obtain in proximal muscles, in vivo work has only been measured
directly in distal limb muscles. However, sonomicrometry measurements show
that proximal muscles of various species strain substantially during and
immediately following muscle activation, suggesting that they generate work or
absorb significant energy (Carrier et al.,
1998
; Gregersen et al.,
1998
; Gillis and Biewener,
2001
). In addition, the biceps femoris and vastus lateralis of
rats increase their active shortening when the animals run up an incline
compared to on the level (Gillis and
Biewener, 2002
). Measurements of joint work also suggest that
muscles at proximal joints may commonly contribute more work than those at
distal joints (Pandy et al.,
1988
; Gregersen et al.,
1998
; Belli et al.,
2002
). Taken together, these results are consistent with the view
that proximal limb muscles play a central role in modulation of limb
mechanical work.
Although the guinea fowl LG performs significantly greater work during
incline running, the qualitative shift in force-length contractile behavior is
less dramatic than in the turkey LG. Unlike the turkey LG, which shifts from
developing economic force on the level to generating work on an incline
(Roberts et al., 1997), the
guinea fowl LG functions similarly during both conditions to develop force and
generate work (Fig. 5). The
differing contractile behavior of these two muscles results primarily from
greater shortening (up to 15%) during level locomotion by the guinea fowl LG
compared with the turkey LG (1-6%: Roberts
et al., 1997
). Thus, the work loop of the guinea fowl LG maintains
a similar overall shape from level to incline locomotion, indicating little
change in the basic contractile behavior of the muscle from level to incline
locomotion. In contrast, the guinea fowl DF-IV shows a distinct shift in the
shape of its work loop from level to incline locomotion
(Fig. 5) that is qualitatively
similar to the turkey LG, even though the net work increase on the incline for
the DF-IV is not statistically significant.
Muscle activity in relation to force and work
The relatively uniform force-length contractile behavior of the guinea fowl
LG compared to the DF-IV during level and incline locomotion are also mirrored
by differences in the muscles' patterns of activation relative force and work
performance. During incline running, changes in the timing of muscle
activation relative to the limb cycle are generally small compared to the
increase in EMG intensity (Roberts et al.,
1997; Carlson-Kuhta et al.,
1998
; Gillis and Biewener,
2002
), which is typically interpreted as reflecting an increase in
muscle recruitment to meet the greater work requirements of incline
locomotion. We found that during incline locomotion, guinea fowl LG EMG
duration tended to be longer, while digital flexor-IV EMG intensity tended to
be greater (Table 2). Although
these changes were not statistically significant, they suggest different
mechanisms of neuromodulation to mediate changes in mechanical performance for
these two muscles. Furthermore, we found an interesting shift in the
relationship between EMG intensity and mechanical output of the DF-IV, but not
the LG. Because the mechanical output of a muscle is sensitive to numerous
factors, including the pattern of activation, force-length and force-velocity
effects, and the recent work history of the muscle (see
Josephson, 1999
;
Marsh, 1999
), the relationship
between EMG intensity and mechanical output (force, work) is not necessarily
constant. Yet, relative EMG intensity of the LG was strongly correlated with
both mean force and net muscle work during level and incline running, whereas
DF-IV EMG intensity was only significantly correlated with force during level
running and with net work during incline running
(Fig. 7,
Table 4). These results are
consistent with the functional shifts observed in the work loops for each
muscle discussed above. Thus, it appears that the shift in force-length
dynamics of the DF-IV from level to incline locomotion, shown by the work
loops (Fig. 5), occurs in
conjunction with a shift in the relationship between muscle recruitment and
mechanical output of this muscle.
We observed that the DF-IV, and to a lesser extent the LG, operated at a
significantly longer length at the onset of force when the animals moved on an
incline (DF-IV: 13% longer, LG: 7% longer;
Fig. 3). This is consistent
with a shift to a more crouched (flexed joint) posture on an incline
(Carlson-Kuhta et al., 1998),
which suggests that the shift in DF-IV force-length dynamics may reflect
effects associated with a postural change. By operating at a longer length, a
muscle exhibits slower force relaxation
(Josephson and Stokes, 1989
)
and achieves greater and more prolonged lengthening force enhancement
(Edman et al., 1978
), both of
which may favor increased work during the subsequent shortening phase of the
muscle's contraction cycle. Interactions between muscle force and muscle
length may play a large role in determining the mechanical performance of a
muscle that undergoes a dynamic strain cycle. Consequently, small changes in
limb mechanics, such as a change in posture from level to incline locomotion,
may result in substantial changes in muscle mechanical performance, despite
similar muscle activity patterns, as we observed for the DF-IV.
Determinants of work for the LG versus the
DF-IV
Strain cycle dynamics relative to force development also affected the
determinants of work output by these two muscles. Whereas the primary
determinants of LG work were mean force and net strain, the primary
determinant of DF-IV work was the phase relationship between force and strain
(Table 5,
Fig. 8). Because the LG
shortened at a relatively constant rate during force production
(Fig. 3), its work output
generally reflects the product of mean muscle force and net length change. In
contrast, the DF-IV underwent large changes in contractile velocity because it
was stretched and then shortened (Fig.
3). Consequently, the relative timing between force and length
change was a significant factor in its work output. This is because a given
magnitude of mean force and net length change can result in positive, zero or
negative work depending on the phase relationship between muscle force and
length. Schematically, it can be thought of as follows: if force development
and length change are symmetrical, no energy is produced or absorbed, and the
muscle-tendon system effectively operates as a simple spring
(Fig. 10A). However, if peak
force precedes peak length, energy is absorbed
(Fig. 10B); whereas, if peak
force lags behind peak length, energy is produced
(Fig. 10C). Only when a muscle
contracts with a constant velocity (whether zero or otherwise) is work
independent of the timing of force development
(Fig. 10D). In reality, the
changes in relative timing of force and length change for most muscles are
likely to be more complex than this. Even so, muscles that contract with
dynamic changes in strain pattern, such as the guinea fowl DF-IV, can be
expected to modulate work substantially through small changes in the timing of
force relative to strain.
|
Stride-to-stride variation in work by the guinea fowl DF-IV
(Fig. 4) probably results from
small changes in the timing or intensity of muscle activation with respect to
the mechanical interaction between the limb and environment, altering the
phase relationship between muscle force and strain. Interestingly,
Gabaldón and Roberts
(2002) found that the peroneus
(fibularis) muscle of the turkey uses a similar mechanism to modulate work for
running on an incline versus on a level. Their previous results,
combined with the stride-to-stride variation in work output in the guinea fowl
DF-IV observed here, demonstrate that muscles can modulate work in vivo
via the relative phase of muscle activation, length change and force.
These findings parallel in vitro work-loop studies showing that
relative phase is a critical determinant of a muscle's work output
(Josephson, 1999
).
In conclusion, the guinea fowl LG and DF-IV exhibit differing force-length dynamics during level and incline locomotion, which appear to have implications for their capacity and mechanism of work modulation and, consequently, the mechanical roles they fulfill during locomotion. While the stretch-shorten strain cycle of the DF-IV muscle may facilitate more economic force generation, it also exhibits a more limited capacity to modulate work output to increase the energy of the body COM. Furthermore, the dynamic pattern of contractile function that we observed for the guinea fowl DF-IV suggests that this muscle may be more sensitive to small changes in the mechanical interaction of the foot and digits with the ground. Although this may lead to greater variability in its work output, it may also reflect a role in mediating stability and balance during locomotion, particularly when the animal moves over more variable terrain. This is an observation that we believe warrants future investigation.
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Acknowledgments |
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