Mechanical function of two ankle extensors in wild turkeys: shifts from energy production to energy absorption during incline versus decline running
Department of Zoology, Oregon State University, 3029 Cordley Hall, Corvallis, OR 97331, USA
* Author for correspondence (e-mail: gabaldoa{at}science.oregonstate.edu)
Accepted 1 April 2004
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Summary |
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During level running at a speed of 2 m s1, the LG and PL were both active in stance but produced peak force at different times, at approximately 21% of stance duration for the LG and 70% for the PL. The LG and PL also had different length patterns in stance during level running. The LG underwent little shortening during force production, resulting in negligible net positive work (2.0±0.8 J kg1). By contrast, the PL produced force across a stretchshorten cycle in stance and did significant net positive work (4.7±1.6 J kg1). Work outputs for both the LG and PL were directly proportional to running slope. When we increased the demand for net positive work by running the turkeys on an incline, the LG and PL increased stance net positive work output in direct proportion to slope (P<0.05). Stance net positive work output increased to 7.0±1.3 J kg1 for the LG and 8.1±2.9 J kg1 for the PL on the steepest incline. Increases in stance net positive work for the LG and PL were associated with increases in net shortening strain and average shortening velocity, but average force in stance remained constant. The LG and PL muscles were also effective energy absorbers during decline running, when there is demand for net negative work on the body. During decline running at 2 m s1 on the steepest slope, the LG absorbed 4.6±2.2 J kg1 of net work in stance and the PL absorbed 2.4±0.9 J kg1 of net work. Shifts in muscle mechanical function from energy production during incline running to energy absorption during decline running were observed over a range of running speeds from 13 m s1 for both the LG and PL.
Two fundamentally different mechanisms for changing work output were apparent in the mechanical behavior of the LG and PL. The LG simply altered its length pattern; it actively shortened during incline running to produce mechanical energy and actively lengthened during decline running to absorb mechanical energy. The PL changed mechanical function by altering its length pattern and by shifting the timing of force production across its stretchshorten cycle. During incline running, the PL produced force during late stance shortening for positive work, but during decline running, the timing of force production shifted into early stance, to align with lengthening for negative work. In addition, during decline running, the PL greatly reduced or eliminated late stance shortening, thus reducing the potential for positive work.
Our results show that the changing demands for whole body work during steady speed running are met, at least in part, by an ability of single muscles to shift mechanical function from net energy production to net energy absorption.
Key words: locomotion, bird, avian, lateral gastrocnemius, peroneus longus, work, slope, wild turkey, Meleagris gallopavo
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Introduction |
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Here, we investigate whether individual muscles can perform all three
mechanical functions motor, brake and strut depending upon the
demand for locomotor work. We measured force and work output during running in
two ankle extensors, the lateral gastrocnemius and peroneus longus.
Architecturally, these muscles include features that have been suggested as
favorable for economic force production, including long tendons
(Alexander, 1974;
Biewener and Roberts, 2000
), a
short pinnate fiber architecture (Biewener
and Roberts, 2000
), and many of them cross two joints
(van Ingen Schenau, 1989
).
Some studies suggest that these features, common to the distal limb muscles in
general, may constrain them to a role as force producers, rather than work
producers. For example, Alexander
(1974
) showed that jumping dogs
increased the work output of proximal limb muscles to power jumping, but the
ankle extensors produced high forces and low work outputs independent of the
demand for work for different tasks. However, a previous study showed that the
lateral gastrocnemius muscle in running turkeys altered mechanical function
with running slope, acting as a strut during level running and as a motor when
the turkeys ran uphill (Roberts et al.,
1997
).
We hypothesized that the mechanical work output of the lateral gastrocnemius (LG) and peroneus longus (PL) muscles in wild turkeys, Meleagris gallopavo, parallels the demand for mechanical work on the body during running. This hypothesis is based on the fact that both are stance phase muscles, and thus have the potential for altering the mechanical energy of the body. Hindlimb joint excursions in wild turkeys occur largely at the knee and ankle joints during running, further suggesting that the LG (a biarticular muscle that acts as a knee flexor and ankle extensor) and PL (an ankle extensor and third toe flexor) may play an important role in modulating work output of the whole body. We ran wild turkeys on level, inclined and declined treadmills to change the demand for mechanical work. Running on level ground at steady speed involves cyclical fluctuations in the energy of the body, but the net work required in each step is negligible. Running on an incline requires net mechanical energy production (positive work) with each step to increase the potential energy of the body, whereas decline running requires energy absorption (negative work) to decrease the energy of the body. Thus, we predicted that the LG and PL would produce force near-isometrically during level running, produce net mechanical energy during incline running, and absorb net mechanical energy during decline running.
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Materials and methods |
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Surgery
Animals were induced and maintained on inhaled isoflurane anesthesia and a
sterile environment was maintained for all surgical procedures. A pair of
sonomicrometry crystals (Sonometrics, Inc., London, ON, Canada) 1 mm or 2 mm
diameter in size (we began with the 1 mm size and found that the 2 mm worked
better for eliminating level shifts) were implanted into small pockets made
with a 16-gauge hypodermic needle within each muscle, to a depth of about 3 mm
along the axis of a proximal fascicle. The crystals were aligned 812 mm
apart, secured in place with a small drop of 3 mol l1
Vet-bond glue and the wire leads were sutured to the muscle's fascia, the thin
fascia associated with the fascicles, using 6-0 silk suture. Two bipolar,
hooked electromyographic (EMG) electrodes, constructed of silver wire, with 1
mm of insulation removed from the tips, were implanted within each muscle near
the sonomicrometry crystals using a 25-gauge hypodermic needle. The leads were
sutured to the muscle's fascia using 6-0 silk suture. Two small strain gauges
(Type FLK-1-11, Tokyo Sokki Kenkyujo Co., Ltd.) were glued to the superficial
and deep aspects of the bony tendon of each muscle. The calcified tendons were
prepared for gluing by gently scraping and then defatting the surface with
chloroform. A thin layer of cyanoacrylate adhesive (Duro superglue, SUP-5;
Loctite Corp., Avon, OH, USA) was applied to each strain gauge and it was
pressed onto the tendon for 1 min for bonding. All transducer wires were
routed subcutaneously from the muscle to a small skin incision near the middle
of the synsacrum. The incision was closed and small electrical connectors
(Microtech, Inc., Boothwyn, PA, USA) were secured to the skin with 3-0 silk
suture. Animals were allowed to recover from surgery for 2448 h before
treadmill running experiments.
Running experiments
Measurements were taken as the birds ran on a level treadmill, followed by
runs on an incline (+6° and +12°) and decline (6° and
12°), at speeds of 13 m s1. Trials were
generally started at 1 m s1 and worked up to 3 m
s1 in 0.5 m s1 speed increments. Ten
seconds of data were collected for each run. Birds remained on the treadmill
at slow walking speeds between speed and slope changes and they were rested
when needed. Fascicle lengths were recorded by sonomicrometry at a frequency
of 992 Hz using the data acquisition software SonoLAB. Muscle EMG signals were
amplified 1000x using a DAM50 differential preamplifier (World Precision
Instruments, Sarasota, FL, USA) with high- and low-bandpass filters of 3 Hz
and10 kHz, respectively. The EMG signals were subsequently filtered in
software with a custom-designed FIR filter (pass band 1501000 Hz).
Tendon strain signals were amplified using a strain gauge conditioner (model
2120, Vishay Measurements Group, Raleigh, NC, USA). Data were collected at a
frequency of 4000 Hz to a Macintosh computer with a 12-bit A/D converter
(PCI-MIO-16-1, National Instruments, Austin, TX, USA) using the software
program IGOR Pro (WaveMetrics, Inc., Lake Oswego, OR, USA). High speed video
was recorded at 250 frames s1 with a Redlake Imaging
MotionScope (model 1000S; Morgan Hill, CA, USA).
In situ calibration of muscle force
Tendon strains were calibrated to muscle force in situ at the end
of running experiments. The procedure involved electrically stimulating the
muscle via the sciatic nerve while simultaneously measuring whole
muscle force and tendon strain. The birds were kept under deep anesthesia with
isoflurane gas during the experiments and body temperature was maintained at
3840°C. The sciatic nerve was isolated and severed at the proximal
end, then placed across two silver wires in a nerve cuff. Mineral oil was
poured around the nerve and the skin incision was sutured closed. The muscle
origin was fixed in place by means of two bone screws inserted into the femur
and attached to an aluminum frame. To calibrate muscle force, the tendon was
cut free at its insertion and attached to an aluminum clamp connected to a
servomotor (model 310B-LR, Aurora, Ontario, Canada), which is a calibrated
force-measuring device. The sciatic nerve was stimulated with a Grass S48
stimulator (67 V supra-maximal stimulation voltage, 100 Hz frequency,
and 250 ms train duration).
A representative calibration of muscle force for the LG in one bird is
shown in Fig. 1AC.
Superficial and deep tendon strains were averaged and muscle force, measured
using the servomotor, was plotted against average tendon strain. The period of
time when the muscle was developing force was used for calibration. The slope
of the line relating muscle force to average tendon strain was determined by
linear regression analysis. Pearson's correlation coefficient values for LG
and PL muscle calibrations were r20.96. Our
measurement of muscle force from tendon strain requires that measured strain
is due to tensile stress applied to the tendon by the muscle, rather than
tendon bending. Averaging the signals from the gauges on the superficial and
deep aspects of the tendon should cancel out any strain due to bending, as
pure bending imposes a tensile stress on one side of the tendon and a
compressive stress on the other. To determine the effectiveness of this
cancellation, we manually imposed pure bending on the tendon following the
force calibration (Fig. 1D).
Averaging the two strain signals removed approximately 90% or more of tendon
strain due to bending. Thus, even if significant bending occurs during
running, the influence of bending on our calculated force values should be
minimal.
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Data analysis and statistics
All wave analyses were performed using the software program IGOR Pro
(WaveMetrics, Inc.). Sonomicrometry signals were smoothed using the
interpolation function (smoothing spline, with a smoothing factor of 1.0 and
standard deviation of 0.010.025). Fascicle segment length (L),
the distance between the two crystals, was differentiated to calculate
instantaneous velocity. Fascicle segment length was expressed relative to the
resting segment length (Lo), which was calculated by
averaging the maximum and minimum lengths in swing. Segment velocity was also
expressed in relative units of length (L s1). To
determine muscle power, we first calculated total muscle fascicle velocity by
multiplying the fascicle segment velocity by the ratio of total fascicle
length to measured segment length. Power was calculated as the product of
muscle force and fascicle velocity, and is expressed relative to muscle mass
(W kg1). Net work (J kg1) was calculated
by integrating power over time. We focused our analysis on changes in net work
performed at each incline, because it is the net work performed by muscle that
changes the body's energy. Though elastic tendons can cycle mechanical energy
during running, they cannot perform or absorb net mechanical work,
and therefore cannot contribute to net energy changes required at different
inclines.
For each animal, 10 strides per run were averaged for analysis. We analyzed
all values (net work, average force, average velocity and net fascicle strain)
over the stance phase for the LG and PL during running at 2 m
s1. We focused on muscle function during stance, when muscle
work can act to increase or decrease the body's mechanical energy. Additional
analyses were performed over the period of force production in stance for the
LG, and over the two regions of the stretchshorten cycle in stance for
the PL. To determine the influence of running slope on the measured variables,
we used the program Systat (version 7.0 for the PC) to perform a two-way
mixed-model analysis of variance (ANOVA), with slope and individual as main
effects. The F-ratio for the main effect of slope was calculated as
the mean square for slope divided by the mean square for slop x
individual interaction term (Zar, 1997). We also performed linear regressions
on mean values, with slope as the independent variable. The criterion for
statistical significance was P0.05. Summary data are presented as
the mean ± S.E.M.
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Results |
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Muscle power and work during level running
Instantaneous muscle power outputs for the LG and PL during level running
were calculated from the force and velocity data and are shown for one bird in
Fig. 2. Positive values
represent mechanical energy production as force is produced during shortening
and negative values represent mechanical energy absorption during lengthening
contractions. The LG produced energy during late swing and in early stance.
The PL absorbed some energy in early stance and produced energy in late stance
as it actively stretchedshortened. Muscle net work
(Fig. 5) was calculated by
integrating power over time. Stance net positive work output for the LG
averaged 2.0±0.8 J kg1 at a running speed of 2 m
s1, but this value was not significantly different from a
value of zero (P>0.05). The PL had a twofold higher stance net
positive work output of 4.7±1.6 J kg1 at 2 m
s1 and work output was significantly higher than a value of
zero (P<0.05). Stance net positive work for the PL reflected the
sum of a little negative work (energy absorption) in early stance and much
higher positive work (energy production) in late stance.
Muscle net work output for the LG and PL muscles showed some individual variation between birds. Forcelength relationships for the LG and PL in three different turkeys running on level ground at a speed of 2 m s1 are shown in Fig. 3 to illustrate the range of variation between individual birds. Work loops for the LG show that some birds produced force nearly isometrically and others produced force with some shortening, resulting in individual differences in stance net work output. Work loops for the PL show that force was produced across a stretchshorten cycle for all birds during level running, but the shortening strain and/or force magnitude differed between individual birds to affect stance net work output. The brief fascicle lengthening at the start of stance indicates the small fraction of mechanical energy absorbed by the PL during lengthening in the stretchshorten cycle. The individual variation in muscle length patterns is unlikely to be due to recording from functionally different sites within the muscles. The sonomicrometry crystals were always implanted into a proximal fascicle, just above the region where the aponeurosis forms an apex. This is a reliable anatomical landmark for implanting crystals. Instead, there may be subtle differences in running kinematics that account for the variation in muscle length patterns observed in different birds.
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Muscle work output during incline and decline running
The LG and PL muscles increased stance net positive work output during
12° incline versus level running at speeds of 13 m
s1 (Fig. 4).
During 12° decline running, both muscles shifted mechanical function and
instead performed net negative work in stance
(Fig. 4). The speed of 2 m
s1 was selected for more detailed analysis of muscle
mechanical function during incline and decline running on 6° and 12°
slopes (Fig. 5). At 2 m
s1, stance net work output of the LG and PL muscles changed
significantly in relation to running slope (P<0.01, LG and
P<0.05, PL). When the birds ran on an incline, the LG and PL did
increasingly greater amounts of net positive work on steeper slopes
(Fig. 5). The LG increased net
positive work output by 3.5-fold from level to 12° incline running
(2.0±0.8 vs. 7.0±1.3 J kg1) and the
PL increased net positive work output by 1.7-fold from level to 12°
incline running (4.7±1.6 vs. 8.1±2.9 J
kg1). When the birds ran on a decline, the LG and PL did
increasingly greater amounts of net negative work on steeper slopes
(Fig. 5). On the steepest
decline of 12°, stance net negative work averaged 4.6±2.2 J
kg1 for LG and 2.4±0.9 J kg1 for
PL.
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Muscle force, velocity and strain
Muscle work is influenced by four main variables: muscle force, fascicle
strain and velocity, and the timing of force relative to the length
trajectory. We calculated all four variables to determine the mechanisms for
how the LG and PL muscles perform net positive work during incline running and
net negative work during decline running. For this analysis, we focused on the
2 m s1 values for average muscle force, net fascicle strain,
and average muscle velocity in stance (Fig.
5). Average muscle force did not change significantly with running
slope for either the LG or PL (P>0.05, LG and PL). By contrast,
net fascicle strain in stance changed significantly with the running slope
(P<0.01, LG and PL). For LG, net fascicle strain in stance,
expressed as a percentage length change relative to the resting fascicle
length, increased from 4.6±1.8% shortening during level running to
15.6±2.0% shortening during 12° incline running, and changed to a
net lengthening strain of 4.0±3.3% during 12° decline running. Net
fascicle strain for the LG during stance force production only (shown by the
open circles), was similar to net fascicle strain calculated over the entire
period of stance. Net fascicle strain in stance for the PL changed from
11.0±2.0% shortening (level running) to 19.0±3.9% shortening
(12° incline) and 7.1±1.5% lengthening (12° decline).
Associated with the changes in net fascicle strain, average muscle velocities
in stance changed significantly in relation to running slope
(P<0.01, LG and PL). The LG and PL developed positive (shortening)
velocities during incline running and negative (lengthening) velocities during
decline running.
Timing of peak force production and length pattern as mechanisms for shifting mechanical function
The LG and PL muscles used two fundamentally different mechanisms to shift
mechanical function from net energy production during incline running to net
energy absorption during decline running. Representative recordings of muscle
force and fascicle length for a turkey running on a level, inclined and
declined treadmill illustrate the different mechanisms that LG and PL muscles
used to change mechanical work output. The LG simply altered its length
pattern in early stance to change mechanical work output. To increase net
positive work output from level to incline running, the LG simply increased
shortening, and to do net negative work during decline running, the LG instead
actively lengthened. The timing of peak force production for the LG did not
change significantly in relation to running slope (P>0.05). For
all slopes, the timing of peak force production for the LG occurred in early
stance, at approximately 21% of stance duration
(Fig. 7B).
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The PL muscle changed mechanical work output by altering its length pattern and/or by shifting the timing of peak force production, depending upon the running slope. To increase net positive work output from level to incline running, the PL increased late stance shortening, while the timing of peak force production remained the same (Fig. 6). During decline running, the PL substantially reduced or eliminated late stance shortening in the stretchshorten cycle, and shifted the timing of peak force production from late stance into early stance to correlate with fascicle lengthening. The shift in timing of peak force production resulted in a marked increase in net energy absorption in early stance during decline running, as shown by the larger pulse of negative power (Fig. 6).
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The shift in timing of peak force production for the PL muscle is illustrated for one bird in Fig. 7. The LG and PL muscle force and length patterns are superimposed, showing the earlier timing of peak force production for the LG versus PL muscle during level and incline running. During decline running, the shift in timing of peak force production for the PL more closely aligns LG and PL muscle forces in early stance, and aligns high PL muscle forces with lengthening in the stretchshorten cycle, resulting in increased mechanical energy absorption.
Individual regions of the stretchshorten cycle for the PL muscle were analyzed for average force, net fascicle strain and net work output (Fig. 8). Over the stretch region of the cycle (Fig. 8A), lengthening strain increased during decline running, but only by a small amount, from 6.2±1.9%, level running, to 9.1±0.6%, 12° decline running. A major factor leading to an increase in work absorption during decline running was the threefold increase in average muscle force during muscle lengthening, reflecting the shift in timing of peak force production (Fig. 7). Muscle strain was an important determinant of muscle work output during incline running. Over the shortening region of the cycle (Fig. 8B), shortening strain increased to as much as 21.7±3.4% during 12° incline running.
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Discussion |
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Mechanical function of LG and PL muscles during level running
We predicted that stance net mechanical work output of the LG and PL
muscles would be close to zero during steady speed level running, since
negligible net work is required to move the body under these conditions. Work
output of the LG was low as predicted (2.0±0.8 J
kg1). However, work output of the PL was about 2.5-fold
higher than for the LG. Our results for the LG are consistent with previous
work showing that this ankle extensor muscle does little mechanical work
during level running (Roberts et al.,
1997). Work output for the LG was low because during most of force
production the muscle operated nearly isometrically. Isometric contractions
also characterize the function of some ankle extensor muscles, the lateral
gastrocnemius and plantaris, in tammar wallabies during steady speed hopping
on level ground (Biewener et al., 1998). It has been proposed that isometric
contractions in the leg muscles of runners and hoppers may reduce the energy
cost of locomotion (Taylor,
1985
,
1994
;
Roberts et al., 1997
).
Stretchshorten cycles can also potentially result in force production
with zero net mechanical work, depending upon the timing of force production
relative to the stretchshorten cycle, and the specific strain pattern
(rate and amount) of each segment within the cycle. We found that the turkey
PL muscle actively produced force across a stretchshorten cycle during
level running. However, net mechanical work output was positive
(4.7±1.6 J kg1) because the timing of peak force
production correlated with muscle shortening rather than lengthening, and
because shortening strain exceeded lengthening strain. Stretchshorten
cycles have also been measured by sonomicrometry in a rat knee extensor, the
vastus lateralis (Gillis and Biewener,
2002
), and a guinea fowl digital flexor
(Daley and Biewener, 2003
)
during steady speed level running. Recent work on the guinea fowl digital
flexor (DF-IV) shows that the muscle undergoes significant strain amplitudes
in the stretchshorten cycle, yet the muscle averages approximately zero
net work during level running at 1.3 m s1 because it
lengthens and shortens by similar amounts during force production
(Daley and Biewener, 2003
). In
lizards, the caudofemoralis muscle also appears to actively
stretchshorten during locomotion on level ground over a range of slow
to fast speeds (Nelson and Jayne,
2001
). Still other measurements of muscle length patterns during
level walking and running in a variety of animals indicate that some muscles
exclusively shorten when active (Ahn and
Full, 2002
; Biewener and
Corning, 2001
; Carrier et al.,
1998
; Daley and Biewener,
2003
; Gillis and Biewener,
2002
; Prilutsky et al.,
1996
), and there is at least one observation of a muscle that
exclusively lengthens (Ahn and Full,
2002
). In all, there appears to be a great diversity of length
patterns in muscles during level running. The present results demonstrate that
strain patterns can differ even among muscle agonists. The implication of this
variation in length pattern for locomotor energetics requires further
study.
The turkey LG and PL muscles have different origins and insertions that may
partly explain their different length patterns observed during level running.
The LG muscle originates on the distal end of the femur and proximal end of
the tibiotarsus, and distally has a single long tendon that joins with the
medial gastrocnemius tendon before crossing the ankle to insert on the
tarsometatarsus for ankle extension
(Raikow, 1985). The PL muscle
originates on the proximal end of the tibiotarsus and has two tendon
insertions. A short branch of the PL tendon inserts on the tibial cartilage
for ankle extension, while a longer branch inserts on the tendon of flexor
perforatus et digiti III muscle to assist in flexion of the third toe
(Raikow, 1985
). Muscle
shortening and work output of the turkey LG muscle are minimized by elastic
stretch and recoil of the tendon-aponeurosis
(Roberts et al., 1997
), and
this is probably an important mechanism influencing the PL length pattern and
mechanical work output as well. Nevertheless, our findings indicate that PL
fascicles undergo greater length changes and do more net positive work
compared to LG fascicles during level running. Mechanical work performed by
the PL in late stance may be associated with ankle extension and flexion of
the third toe to lift and reaccelerate the body at the end of each step. The
difference in timing of peak force production between the LG and PL during
level running (Fig. 2) may also
be related to the PL's function as a toe flexor in late stance.
Mechanical work during incline and decline running
By varying the slope of the running surface, we varied the demand for work,
to determine if LG and PL muscle work outputs parallel the demand for work on
the body. The major finding was that both muscles changed mechanical function
and acted as energy producing motors during incline running and as energy
absorbing brakes during decline running
(Fig. 5). The maximum capacity
of the muscles for energy production and energy absorption was not determined
in this study; work outputs at steeper slopes may be greater than measured
here. For the slopes investigated, nevertheless we found a significant linear
relationship between muscle work and running slope
(Fig. 5), which is parallel to
the demand for work on the body. This is consistent with our hypothesis that
mechanical work output of these muscles parallels the demand for work on the
body.
Changes in ankle excursion with incline (Fig. 9) illustrate how changes in muscle strain might be related to changes in joint kinematics: there was a significant positive linear relationship between running slope and ankle excursion in stance. Birds landed with the leg more extended during decline versus incline running; by contrast, they lifted the foot off the ground at the end of stance with the ankle more flexed during decline versus incline running. Thus, ankle net excursion in stance, the difference between toe-off and toe-on ankle angles, was negative for decline running, indicating net flexion, and positive for incline running, indicating net extension. These changes in ankle excursion parallel the work outputs for the LG and PL muscles on different running slopes. We did not analyze joint kinematics at other joints, though muscle fiber strains in these muscles are also influenced by the excursions of the knee (LG) and toes (PL). Duty factor (stance time/stride time) was relatively unchanged with running slope (0.48±0.01 for 12° decline, 0.49±0.01 for level, and 0.53±0.01 for 12° incline) and stride frequency was also unchanged (strides s1: 2.4±0.04 for 12° decline, 2.4±0.05 for level, and 2.5±0.08 for 12° incline).
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How does the work output of the LG and PL compare quantitatively with the
demand for work on the body? For 12° incline running at a steady speed of
2 m s1, the average mechanical power required to increase
the body's potential energy is 4.1 W kg1 body mass. The
average stride frequency for turkeys running on this slope was 2.52 strides
s1, so the body mass specific work required per stride was
on average 4.1/2.52=1.6 J kg1 stride1, or
0.8 J kg1 step1. The hindlimb musculature
of turkeys is equivalent to approximately 7.7% of body mass for one limb
(Roberts and Scales, 2002).
The mechanical work required on average in each step from each kg of hindlimb
muscle is then 0.8/0.077=10.5 J kg1. The work outputs of
both the LG, 7.0 J kg1, and the PL, 8.1 J
kg1, were not substantially different than the 10.5 J
kg1 that must be developed, on average, by the hindlimb
musculature. This suggests that the LG and PL operate as effective motors
during incline running. The same calculations used above yield a net energy
absorption required per unit muscle of 11.3 J kg1 during
12° decline running (slightly different from incline running due to a
slight difference in stride frequency, i.e. 2.35 versus 2.52). The
energy absorption values of 4.6 J kg1 for the LG and 2.4 J
kg1 for the PL during 12° decline running indicate that
some muscles must operate as much more effective brakes than the LG or PL
during decline running.
How single muscles change mechanical function
Two fundamentally different mechanisms to change muscle work output were
apparent in the mechanical behavior of the LG and PL. Changes in muscle strain
explained virtually all of the change in positive work output from level to
incline running for both muscles. Both the LG and PL did more shortening in
stance from level to incline running, while the timing of peak force and
average force in stance were unchanged. For the LG, changes in strain also
explained the change in mechanical work from incline to decline running, as
the muscle switched from forceful shortening to forceful lengthening. However,
the change in function of the PL reveals a mechanism for altering muscle work
output independent of changes in muscle strain. The timing of peak force
shifted significantly from incline to decline running, as peak force was
produced in the second half of stance for incline running and in the first
half of stance for decline running. This change in timing of peak force
significantly altered muscle work output because the muscle typically
lengthened early in stance and shortened late in stance. The change in timing
of peak force production meant that during decline running more force was
developed during the lengthening period of the stretchshorten cycle
while during incline running more force was developed during the shortening
period. As a result, the muscle did net negative work for decline running and
net positive work for incline running. This mechanism explains in part how the
PL increased net negative work for decline running with virtually no change in
the magnitude of lengthening strain (Daley
and Biewener, 2003). Modulation of the timing of activation and
force production may be a particularly important mechanism for altering muscle
work output in muscles that undergo stretchshorten cycles.
Strategies for changing whole body work output
Our results show that the changing demands for mechanical work of the body
are met in part by a change in work output of individual muscles, but other
studies suggest that this is not the only mechanism used to alter whole body
work output. Recent studies of muscle EMG activities in cats walking on
different surface slopes show that some muscles are active on some slopes but
inactive on others (Carlson-Kuhta et al.,
1998; Smith et al.,
1998
). In the cat proximal hind limb, for example, the biceps
femoris and semimembranosus (two hip extensors) are highly active in stance
during incline walking but show almost no EMG activity during decline walking
(Carlson-Kuhta et al., 1998
;
Smith et al., 1998
). In the
cat distal hindlimb, the plantaris and flexor hallucis longus (two ankle
extensors and digit flexors) are active during incline walking but inactive
during decline walking (Carlson-Kuhta et
al., 1998
; Smith et al.,
1998
). These observations suggest that, in addition to changing
the mechanical function of individual muscles, whole-body work output can be
modified by selective muscle recruitment. For example, incline running might
be powered by increased recruitment of muscles that typically shorten, and
derecruitment of muscles that typically lengthen, to result in an increase in
net mechanical work output for the whole limb. This strategy appears to be
reflected in the function of the rat biceps femoris during running on
different surface slopes. The biceps femoris exclusively shortens on level,
inclined and declined slopes during steady speed walking and running
(Gillis and Biewener, 2002
).
On level and inclined slopes, the muscle is electrically active while
shortening in stance, but on declined slopes EMG activity is absent or very
low (Gillis and Biewener,
2002
). Because biceps femoris does not actively lengthen in stance
during decline running, it does not absorb mechanical energy; however, because
it is switched off, it no longer contributes any positive work.
Conclusion
The demands for mechanical work in running vary widely, from net energy
absorption for decline running and decelerations, to net energy production for
incline running and accelerations. The present results show that the changing
demands for whole body work are met, at least in part, by an ability of single
muscles to change from net energy producers to net energy absorbers. The
observation that the LG and PL act as effective work-producing motors is not
consistent with the idea that the spring-like function of distal limb
extensors limits their ability to perform mechanical work. Both changes in net
muscle strain (for the LG and PL) and timing of force production (for the PL)
appear to be important mechanisms for altering muscle mechanical work output
with demand.
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Acknowledgments |
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References |
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Alexander, R. M. (1974). The mechanics of jumping by a dog (Canis familiaris). J. Zool. Lond. 173,549 -573.
Ahn, A. N. and Full, R. J. (2002). A motor and
a brake: two leg extensor muscles acting at the same joint manage energy
differently in a running insect. J. Exp. Biol.
205,379
-389.
Biewener, A. A. and Corning, W. R. (2001).
Dynamics of mallard (Anas platyrhynchos) gastrocnemius function
during swimming versus terrestrial locomotion. J. Exp.
Biol. 204,1745
-1756.
Biewener, A. A., Corning, W. R. and Tobalske, B. W.
(1998a). In vivo pectoralis muscle forcelength
behavior during level flight in pigeons (Columba livia).
J. Exp. Biol. 201,3293
-3307.
Biewener, A. A., Konieczynski, D. D. and Baudinette, R. V.
(1998b). In vivo muscle forcelength behavior
during steady speed hopping in tammar wallabies. J. Exp.
Biol. 201,1681
-1694.
Biewener, A. A. and Roberts, T. J. (2000). Muscle and tendon contributions to force, work, and elastic energy savings: A comparative perspective. Exerc. Sport. Sci. Rev. 28, 99-107.[Medline]
Carlson-Kuhta, P., Trank, T. V. and Smith, J. L.
(1998). Forms of forward quadrupedal locomotion. II. A comparison
of posture, hindlimb kinematics, and motor patterns for upslope and level
walking. J. Neurophysiol.
79,1687
-1701.
Carrier, D. R., Gregersen, C. S. and Silverton, N. A.
(1998). Dynamic gearing in running dogs. J. Exp.
Biol. 201,3185
-3195.
Dial, K. P. and Biewener, A. A. (1993).
Pectoralis muscle force and power output during different modes of flight in
pigeons. J. Exp. Biol.
176, 31-54.
Daley, M. A. and Biewener, A. A. (2003). Muscle
forcelength dynamics during level versus incline locomotion: a
comparison of in vivo performance of two guinea fowl ankle extensors.
J. Exp. Biol. 206,2941
-2958.
Dickinson, M. H., Farley, C. T., Full, R. J., Koehl, M. A. R.,
Kram, R. and Lehman, S. (2000). How animals move: An
integrative view. Science
288,100
-106.
Gillis, G. B. and Biewener, A. A. (2002).
Effects of surface grade on proximal hindlimb muscle strain and activation
during rat locomotion. J. Appl. Physiol.
93,1731
-1743.
Marsh, R. L., Olson, J. M. and Guzik, S. K. (1992). Mechanical performance of scallop adductor muscle during swimming. Nature 357,411 -413.[CrossRef][Medline]
Nelson, F. E. and Jayne, B. C. (2001). The effects of speed on the in vivo activity and length of a limb muscle during the locomotion of the iguanian lizard Dipsosaurus dorsalis.J. Exp. Biol. 204,3507 -3522.[Medline]
Prilutsky, B. I., Herzog, W. and Allinger, T. L.
(1996). Mechanical power and work of cat soleus, gastrocnemius
and plantaris muscles during locomotion: Possible functional significance of
muscle design and force patterns. J. Exp. Biol.
199,801
-814.
Raikow, R. J. (1985). Locomotor system. In Form and Function in Birds, Vol.3 (ed. A. S. King and J. McLelland), pp.105 -107. London: Academic Press.
Roberts, T. J. and Scales, J. A. (2002).
Mechanical power output during running accelerations in wild turkeys.
J. Exp. Biol. 205,1485
-1494.
Roberts, T. J., Marsh, R. L., Weyand, P. G. and Taylor, C.
R. (1997). Muscular force in running turkeys: The economy of
minimizing work. Science
275,1113
-1115.
Smith, J. L., Carlson-Kuhta, P. and Trank, T. V.
(1998). Forms of forward quadrupedal locomotion. III. A
comparison of posture, hindlimb kinematics, and motor patterns for downslope
and level walking. J. Neurophysiol.
79,1702
-1716.
Taylor, C. R. (1985). Force development during sustained locomotion: a determinant of gait, speed and metabolic power. J. Exp. Biol. 115,253 -262.[Abstract]
Taylor, C. R. (1994). Relating mechanics and energetics during exercise. In Advances in Veterinary Science and Comparative Medicine, vol. 38A (ed. J. H. Jones), pp. 181-215. San Diego: Academic Press.[Medline]
Tu, M. S. and Dickinson, M. H. (1994).
Modulation of negative work output from a steering muscle of the blowfly
Calliphora vicina. J. Exp. Biol.
192,207
-224.
van Ingen Schenau, G. J. (1989). From rotation to translation. Constraints on multijoint movement and the unique role of biarticular muscles. J. Hum. Movement Sci. 8, 301-307.[CrossRef]
Zar, J. H. (1996). Biostatistical Analysis. Upper Saddle River, NJ: Prentice Hall.