Dynamics of leg muscle function in tammar wallabies (M. eugenii) during level versus incline hopping
1 Concord Field Station, Department of Organismic and Evolutionary Biology,
Harvard University, Cambridge, MA 02138, USA
2 Department of Environmental Biology, University of Adelaide, Adelaide, SA
5003, Australia
* Author for correspondence (e-mail: abiewener{at}oeb.harvard.edu)
Accepted 24 October 2003
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Summary |
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Key words: muscle-tendon unit, work, elastic energy, force-length, lateral gastrocnemius, plantaris, muscle, hopping, locomotion, tammar wallaby, Macropus eugenii
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Introduction |
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When an animal changes speed, or moves uphill or downhill, shifts in muscle
shortening or lengthening are clearly required to modulate work output within
the limb as a whole. This raises the question of whether all muscles
contribute similarly to the shift in net work or whether certain muscle groups
are recruited specifically for such tasks and are better suited for modulating
work performance. In this paper, we specifically examine the question of
whether the highly specialized distal leg muscle-tendon units of tammar
wallabies (Macropus eugenii) are capable of shifting their
contractile performance to contribute increased work when wallabies hop up an
incline. In their study of wild turkeys (Meleagris gallopavo),
Roberts et al. (1997) found
that the lateral gastrocnemius (LG) was able to shift from economical, near
isometric, behavior during level running to increased shortening and work
production during uphill running. Thus, despite having an architecture that
favors force economy and tendon elastic savings, the turkey LG's contractile
performance was capable of contributing to the additional potential energy
work associated with lifting the animal's center of mass as it moved uphill.
In the present study, we examine the same question by comparing the
contractile performance of the plantaris (PL) and LG muscle-tendon units of
tammar wallabies (Macropus eugenii) during level versus
incline (10°) hopping on a treadmill. Our previous study of these two
muscles during steady level hopping over a broad range of speeds showed that
both muscles contracted with limited length change (PL: <2%; LG: <5%),
similar to the length change observed for the turkey LG (<6%;
Roberts et al., 1997
). As a
result, net muscle work was negligible compared with the amount of elastic
energy stored and recovered in the muscles' tendons. In the present study, we
test the hypothesis that, unlike the turkey LG, the specialized design of the
leg muscles and tendons of tammar wallabies, associated with their ability to
recover substantial elastic energy during hopping, dramatically reduce
metabolic energy rates (Baudinette et al.,
1992
), results in no change in their contractile role during level
versus incline hopping. In a related study
(Daley and Biewener, 2003
), we
examine the same question for two agonist distal leg muscles of the guinea
fowl (Numida meleagris). Although muscles of similar mass but
differing fiber length should have similar capacity for performing work, our
hypothesis is that distal leg muscles with short fibers and long tendons will
generally be more constrained than longer-fibered proximal muscles in shifting
their contractile performance to adjust their work output associated with
acceleration and deceleration, or changes in grade.
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Materials and methods |
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Surgical approach and transducer design/implantation
The general surgical approach, implantation sites and design of the
transducers were similar to our earlier study of level locomotion
(Biewener et al., 1998) but
are briefly described here. Animals were anesthetized using isoflourane gas
administered by a mask. Animals were induced at 3-4% and maintained at 1.5-2%
during the surgical procedure. All electrodes were soaked in a bacterial
disinfecting solution (CetylcideTM disinfectant) and placed in a
UV-sterilizing surgical instrument container overnight prior to surgery. The
bellies of the lateral gastrocnemius (LG) and plantaris (PL) were exposed by a
postero-lateral skin incision. All electrodes and transducers were then passed
subcutaneously from a small incision made above the hip over the pelvis to the
opening in the leg over the muscles. Piezoelectric SONO crystals (2.0 mm;
SonometricsTM) were inserted parallel to the fascicles in the mid-region
of the LG by piercing the fascial epimysium of the muscle and creating a small
pocket, with sharp-pointed scissors, into which the crystal was inserted.
Because the LG is unipennate, crystals were inserted to varying depth to match
the pinnation angle of the fascicles (26°;
Table 1). Pairs of crystals,
located 10-14 mm apart, were then aligned to maximize their signal-to-noise
ratio. This was done by monitoring the transducers' output via the
recording cable connected to a sonomicrometer amplifier (Triton 120.1), with
the signals displayed on a Tektronix 2205 oscilloscope during the surgical
procedure. After optimal alignment was established, the crystals were anchored
into position by suturing the openings and anchoring the lead wires to the
muscle's surface with 4-0 silk. Bipolar off-set twist hook EMG electrodes (0.1
mm silver enamel insulated; California Fine Wire) were then implanted
immediately adjacent to each crystal pair. Access to the PL required making an
incision through the aponeurosis connecting the lateral and medial (MG) heads
of the gastrocnemius to expose the PL, which lies deep to the MG and LG. The
PL is a multipennate muscle. SONO crystals and EMG electrodes were implanted
in a medial compartment of the PL, which was selected as a site for obtaining
fascicle length recordings in order to minimize disruption to the overlying MG
and LG (Fig. 1). Interpretations of muscle length change for the LG (and MG) and PL are
therefore based on these localized recordings of fascicle length change, which
are assumed to be representative of the muscle as a whole (see below).
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After implanting the muscle transducers, stainless-steel E-shaped tendon
buckle force transducers (Biewener et al.,
1998) were implanted on the PL and common Achilles tendons
(Fig. 1). Exposure of the
tendons was achieved by extending the incision from the muscle bellies
parallel to the tendons. The tendon buckles were implanted so that they did
not interfere with each other when the ankle was passively flexed and
extended. Their position was secured with 3-0 suture sewn through an edge of
the tendon and anchored to the buckle via a figure-of-eight loop
passed through the fastening holes in the buckle arms. Because the soleus
muscle in tammar wallabies is extremely small and merges with the LG muscle
and aponeurosis (Biewener et al.,
1998
), the Achilles tendon buckle measured the combined force of
the MG, LG and soleus.
Animals were allowed to recover from surgery for 24-36 h and then hopped at the two speeds and two inclines for several repeated trials, sufficient to yield 10-15 steady hops for any trial and condition. High-speed digital video recordings (Redlake, PCI-500 at 125 Hz) were also obtained of the animals in lateral view. The videos were synchronized to the muscle-tendon recordings by means of a post-trigger pulse sampled together with the muscle-tendon signals at 5 kHzby means of a BioWareTM type 2812A1-3 A/D system (DAS1602/16 A/D board; Kistler Instruments Corp., Amherst, NY, USA) operated using BioWareTM v.3.0 software. Experimental data stored on disk were subsequently analyzed using IGOR Pro and customized Matlab (v.5.3; The MathWorks, Natick, MA, USA) routines.
Muscle fascicle length change and force
Measurements of the fractional length change of muscle fascicles were based
on the change in length between crystal pairs relative to their resting length
(Lfract=L/Lrest).
Resting length was determined both when the animal was lying at rest in a
burlap bag in between treadmill trials and again postmortem. Values of
Lrest measured for both conditions were the same. Before
analysis, fractional length recordings were corrected for the offset error
introduced by the faster speed of sound propagation through the epoxy lens of
the crystals relative to the muscle (determined to be 0.82 mm for the
SonometricsTM 2.0 mm crystals) and for the 5 ms delay introduced by the
Triton 120.1 amplifier's filter. Mean fascicle length changes for the muscle
as a whole were calculated as
Ltot=LfractxLf,
where Lf is the mean fascicle length of the muscle. This
assumes that all fascicles within the muscle undergo uniform length changes.
While this may not be the case, and requires verification by future studies,
our measurements do not allow us to test this assumption.
After completing the experimental recordings, the animals were euthanized
(gas anesthesia followed by 100 mg kg-1 sodium pentobarbital
injected by cardiac puncture) and the locations and alignment of the SONO
crystals and EMG electrodes verified by dissection of the muscles in
situ. In all cases, crystal alignment was found to be within 0-7° of
the fascicle axis (so that errors due to crystal alignment were less than 1%).
Exposure and inspection of the tendons showed no significant signs of
inflammation or damage by the buckle transducers. The distal-most portion of
the muscle and its aponeurosis were then cut and isolated with the tendons,
which were left with their distal ankle and foot skeletal attachments left
intact. The proximal end of the muscle and aponeurosis were then tied
repeatedly and secured to a uniaxial tension transducer with heavy nylon cord
(250 N capacity). The tied proximal end was then immersed in liquid nitrogen
and frozen. Before conducting tensile force calibrations, the buckle
transducer and adjacent region of the tendon were warmed to room temperature
(25°C). The difference in test (room) temperature versus in vivo
temperature was considered to have a negligible effect on the buckle
calibrations. Repeated in situ pull calibrations of the isolated
tendons yielded simultaneous recordings of force and buckle voltage output
that were calibrated by means of least-squares regression during both the rise
and fall in force. This provided a dynamic calibration of in vivo
muscle-tendon force measured by the tendon buckle. This was repeated for the
second isolated tendon. As in our previous experiments
(Biewener et al., 1998), we
observed only a slight hysteresis in slope (difference in the force rise slope
being less than 2% of the slope of force decline), with r2
values exceeding 0.985.
EMG signal intensity
EMG intensity for single bursts of muscle activation was determined by
averaging the spike amplitude of the rectified EMG signal. EMG intensities
were then converted to a relative scale for each muscle by dividing this value
by the largest value recorded in that muscle for that animal. Thus, for a
given animal, the largest burst intensity recorded in a given muscle was
assigned the value of 1, and all other bursts from that muscle ranged between
0 and 1.
Muscle and tendon stress and tendon elastic strain energy
To obtain measurements of tendon and muscle cross-sectional area for
computing muscle and tendon stress and tendon elastic energy savings, the
tendons of the contralateral PL and LG + MG were dissected free, their lengths
measured, and weighed to the nearest 0.1 mg using an electronic balance. The
short portion of the plantaris tendon that passes over the calcaneus was
excised before weighing. Previous work
(Ker et al., 1986) has shown
that this portion has a lower elastic modulus than the intervening lengths of
the tendons. Measurement of tendon area was made assuming a density of 1120 kg
m-3 for tendon (Ker,
1981
). Tendon volume was then calculated assuming a uniform tendon
area from muscle origin to tendon insertion and by subtracting the muscle's
fiber length from overall muscle-tendon length to obtain the tendon's `net
length'. Tendon elastic energy recovery was calculated using a modulus of 1.0
GPa to account for the lower modulus of tendon at low (<3%) strains and a
resilience of 93% (Ker, 1981
;
Bennett et al., 1986
;
Shadwick, 1990
).
Before making measurements from the muscles, EMG electrode implantation
sites were verified for proper location in the muscle's belly. The freshly
isolated muscles were then weighed (to the nearest 0.01 g of their mass,
M) and, using a no. 10 scalpel, sectioned in a plane parallel to the
muscle fibers. Measurements of fiber length (l) and pennation angle
() were then made at regular intervals (six per muscle) along the
muscle's length using digital calipers and a protractor to calculate the
muscle's fiber cross-sectional area. Effective fiber cross-sectional area
(=Mcos(
)/
l) was calculated using the mean values
obtained for these measurements (Table
1), using a density (
) of 1060 kg m-3 for the
muscle. Slight errors in the plane of section and possible distortion in the
resting length of the fresh muscle during the sectioning and measurement
procedures introduce some uncertainty for the values of resting fiber length
and cross-sectional area obtained using this approach. Measurements of muscle
work for the gastrocnemius muscle as a whole were based on the length changes
recorded in the LG fascicles because the force measurements are for both LG
and MG heads. We chose this approach because of the uncertainty of
partitioning the amount of force that each head contributed separately to our
combined tendon force buckle recordings.
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Results |
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Joint kinematics
Representative graphs of knee, ankle and metatarsophalangeal (MP) joint
angle changes over time for three strides at 4.2 m s-1 by wallaby
#1 are shown in Fig. 3. Similar
patterns were observed in the other three animals. These data show that the
knee and ankle joints flex and extend at the same time during stance,
consistent with the small net strains that the biarticular LG and
multiarticular PL muscles achieve while producing force (see below). The MP
joint shows more variable degrees of initial flexion early in stance, followed
by substantial extension during the latter half of limb support. Differences
between level versus incline hopping are most apparent at the ankle
joint, which maintains a more flexed range of excursion during incline
hopping. Increased flexion is also most consistently observed at the MP joint
during incline hopping late in support, as the animal's limb transitions into
its swing phase, but is more variable at the onset of stance. The knee, by
contrast, showed little change in flexion during the first half of limb
support but extended to a greater degree than the ankle and MP joints late in
stance during incline hopping.
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In vivo 'work loop' patterns
Graphs of muscle-tendon force relative to fascicle length change further
demonstrate the similar in vivo behavior and work performance of the
two hind leg muscles during level and incline hopping
(Fig. 4). Although some
variation in the patterns of force-length behavior was observed among
individual animals, the work loop behavior of the LG and PL was highly
consistent within each individual. In general, the LG contracted with varying,
but modest, degrees of fascicle shortening and lengthening, yielding in some
cases net work output (e.g. wallaby #2) while in others net energy absorption
or negative work (e.g. wallaby #3). In all cases, the early rise in LG force
('shoulder' seen in records presented in
Fig. 2) was associated with
fascicle shortening. As noted above, we interpret this as representing muscle
shortening in series with elastic stretch of the muscle's aponeurosis and
tendon, when both are most compliant at the onset of force development and the
foot is being decelerated prior to ground contact. Force development then rose
either in an isometric manner or with moderate stretch of the fascicles (mean
LG strain during force rise: level, 1.27±4.0%; incline,
3.14±3.16%; N=4), after the foot was placed on the ground for
weight support. In all cases, the LG fascicles remained nearly isometric or
shortened only slightly during the decline in muscle-tendon force later in
support (mean LG strain during force decline: level, -2.23±1.55%;
incline, -2.52±2.21%; N=4).
Although the PL fascicles also showed a brief early phase of shortening at low force levels early in stance (Fig. 4B), this was generally more limited than that observed for the LG fascicles (Fig. 4A). During the rapid rise in force, the fascicles were stretched (mean PL strain: level, 6.34±1.25%; incline, 7.84±0.72%) and then shortened by similar amounts during force decline (mean PL strain: level, -6.23±0.97%; incline, -7.43±1.21%; N=4).
In general, these patterns of lengthening and shortening fascicle strain
during stance were consistent among the four animals studied
(Fig. 5). Although the
magnitude of lengthening and shortening strain was generally greater in the PL
compared with the LG, the net strains of the two muscles over the course of
limb support were similar and, as noted above, generally quite small
(averaging 1%). As a result, neither muscle shifted its work performance
during level versus incline hopping
(Fig. 6;
Table 2). On average, both
muscles absorbed net energy under both level and incline conditions, although
the amount absorbed by the PL was trivially small. Assuming that the MG
fascicles undergo the same length changes as the LG fascicles, the
mass-specific work performed by the gastrocnemius as a whole amounted to -6.0
J kg-1 muscle to -10.0 J kg-1 muscle. For the PL, net
mass-specific muscle work ranged from -1.4 J kg-1 muscle to -2.0 J
kg-1 muscle.
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Muscle and tendon stresses
Although muscle-tendon forces increased slightly with hopping speed, no
consistent increase in muscle-tendon force
(Table 2), and thus tendon
stress (Fig. 7) and elastic
energy savings (Table 2),
occurred with a shift from level to incline hopping at either 3.3 m
s-1 or 4.2 m s-1. Whereas PL forces increased on an
incline, LG forces decreased relative to level hopping
(Table 2). Peak muscle stresses
in the PL (mean, 144 kPa) were slightly larger but generally similar in
magnitude to those developed within the gastrocnemius (LG + MG mean = 128
kPa). For the gastrocnemius, peak tendon stresses averaged 25.2 MPa for all
conditions. For the PL, peak tendon stresses were of similar magnitude,
averaging 24.9 MPa for all conditions. These stress levels indicate that both
tendons operated with strains of 2.5%, yielding elastic energy savings
for the gastrocnemius of 0.43 J on the level and 0.36 J on an incline. Elastic
energy recovery by the PL tendon averaged 0.46 J on the level and 0.55 J on an
incline. Consequently, tendon energy savings exceeded net muscle work by
approximately threefold in the gastrocnemius and 20-fold in the PL.
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Muscle activation patterns
Consistent with the similar contractile patterns of force and length change
that were observed during level and incline hopping, we also observed uniform
patterns in the timing of neural activation (EMG) relative to force
development and fascicle strain (Fig.
8). Associated with its earlier development of force, activation
of the LG occurred 48±11 ms (level) and 50±16 ms (incline) prior
to limb contact, preceding PL EMG onset by 29±6 ms during level hopping
and 38±9 msduring incline hopping. EMG onset preceded force development
by 14±5 ms in the LG and 17±13 ms in the PL for all conditions.
In addition to deceleration of the foot, activation of both muscles prior to
limb support probably corresponded to an initial series-elastic stretch of the
muscle's aponeurosis and tendon (evidenced by fascicle shortening; Figs
2,
4), which are most compliant at
low force levels. EMG offset occurred shortly after peak force development in
both muscles, lasting 67±5% of the duration of force development by the
LG and 69±7% of the duration of force development by the PL. In both
muscles, therefore, EMG offset occurred well before force declined to zero
(Fig. 8).
Whereas no change in LG EMG phase and duration was observed, PL EMG phase and duration were modestly, but significantly, reduced during incline versus level hopping (Table 2). Correspondingly, normalized EMG intensity (mean spike amplitude) showed no change in the LG but was significantly increased in the PL when the animals hopped on an incline versus a level surface (Table 2). Nevertheless, the general uniformity of EMG timing relative to force development and the onset of stance during both level and incline hopping was consistent with the fact that stride frequency, limb contact time and duty factor did not change when the animals hopped on a level versus an incline at both speeds (Table 2). All three variables exhibited small, but significant, changes with speed; whereas duty factor [F(1,3)=12.17, P=0.007] and limb contact time [F(1,3)=96.79, P=0.001] decreased with speed, stride frequency increased slightly [F(1,3)=27.41, P=0.001].
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Discussion |
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Interestingly, in an earlier study, Griffiths
(1989) found that the MG of
thylogale wallabies (Thylogale billardierii) performs positive work
when the animals accelerate from rest. Griffith's results were based on tendon
buckle recordings similar to our own, but length measurements were based on
indirect measures of joint kinematics and muscle-tendon moment arms. The
length changes determined from these measurements are for the muscle-tendon
unit as a whole, so it is difficult to quantify how much of the work was done
by the muscle itself based on the work loop shown for when the animal
accelerated (fig. 6 in
Griffiths, 1989
). Assuming
that nearly all of the net shortening (15 mm) is due to fiber shortening
(although this suggests nearly 100% shortening strain if the MG fibers are of
similar length to the MG of a tammar wallaby;
Biewener and Baudinette, 1995
),
this would suggest that the MG does
25-30 J kg-1 when a
wallaby accelerates from rest. The uncertainty of such indirect estimates of
muscle fiber shortening makes it difficult to compare with our present
findings. But it would be interesting to explore further whether acceleration
from rest would enable the gastrocnemius and PL muscles to contribute
substantial positive work to the animal's movement. We clearly did not observe
such a shift in function for incline hopping at steady speed in tammar
wallabies.
An important question to address is whether the net mechanical work
performed by a wallaby hopping up a 10° incline requires much of an
additional increase in limb muscle work and whether we should expect these two
muscles to make a significant contribution to this work. The net positive
mechanical power required for a 6.6 kg wallaby (mean mass of our four
subjects) to raise its center of mass while hopping up a 10° slope at a
speed of 4.2 m s-1 is 47 W
[=Mgu(sin)=6.6x9.81x4.2xsin(10),
where g is gravitational acceleration and u is the
animal's speed]. A stride frequency of 3.49 s-1
(Table 2) means that 13.5 J of
additional work is required per stride and 6.75 J of this extra work is
performed by each limb. In comparison, the amount of energy that the muscles'
tendons (including the MG) store and recover in each stride (0.91 J) is much
less. For muscles that function to perform mechanical work, we might expect
them to produce up to 30 J kg-1
(Alexander, 1992
). Given that
the combined mass of the gastrocnemius (MG + LG) and PL muscles averages 0.062
kg, they might be capable of delivering as much as 1.86 J. In terms of maximal
work, these muscles might therefore contribute as much as 28% of the total
work required of the hind limb as a whole. In comparison, the mass of these
three distal ankle extensors is 20.4% of the total mass of the hind limb
muscle extensors per each limb as a whole (0.304 kg; C. McGowan, unpublished
data). Thus, even though these muscles have the capacity to contribute a
significant fraction of the muscle work required for incline hopping, and are
of sufficient size to do so, our recordings indicate that they are not
recruited to perform this role.
These results demonstrate that the energy-saving roles of the tammar
wallaby LG and PL via force economy and tendon strain energy recovery
are retained whether these animals hop over level ground or on an incline. In
addition to retaining their spring-like behavior, neither muscle-tendon unit
significantly altered the amount of force that each transmitted. Consequently,
a similar level of stress and energy savings in both tendons was also
maintained. In general, tendon elastic energy savings exceeded muscle work by
3-20-fold during both level and incline hopping. We have observed similar
differences previously, with tendon energy savings exceeding muscle work by as
much as 30-fold at faster hopping speeds
(Biewener et al., 1998).
The uniformity of PL and LG muscle-tendon dynamics further reflects the
overall uniformity of limb support dynamics; each wallaby's stride frequency,
limb contact time and duty factor also remained the same under both level and
incline conditions at a given speed. Consequently, any increase in metabolic
cost with incline hopping, and at faster speeds on an incline, would most
likely be due to an increase in the rate of potential energy work that the
animal must perform to raise its center of mass. Kram and Dawson
(1998) reported a significant
increase in metabolic rate with increased hopping speed on an incline for a
single red kangaroo (Macropus rufus). Both red kangaroos
(Dawson and Taylor, 1973
) and
tammar wallabies (Baudinette et al.,
1992
) are well known for their ability to hop at faster speeds on
a level without increasing their metabolic rate. Therefore, our results here
suggest that if tammar wallabies show a similar increase in metabolic rate
while hopping on an incline, it is more likely due to the cost of potential
energy work than to a reduction in the economy of muscle force generation or
tendon energy recovery.
Mechanical roles of proximal versus distal limb muscles
Because muscle mass, fiber length and architecture differ among muscles
operating at different joints within an animal's limb, it seems likely that
other muscles may not function in the same way as the LG and PL muscles. It is
possible that other distal hind leg muscles (e.g. the MG or flexor digitorum
longus) may shorten more and contribute net work to raising the wallaby's
center of mass during incline hopping, but we believe this is unlikely.
Because the medial and lateral heads of the gastrocnemius are linked by a
common aponeurosis and tendon and span the same joints (knee and ankle), it
seems likely that the fascicles of the MG behave similarly to those in the LG.
This was an assumption in our calculation of the combined work that the LG and
MG performed. Nevertheless, measurements of MG fascicle behavior would be
needed to confirm this. In addition, while it is possible that the flexor
digitorum muscle contributes net work to incline hopping, we believe it is
more likely that proximal knee and hip extensors perform the increased
mechanical work needed to elevate the animal's center of mass on an incline.
Recent studies of rats moving uphill and downhill on a treadmill over a range
of speeds and gaits (Gillis and Biewener,
2002) show that knee and hip extensors alter their shortening
behavior in vivo when they are active, in a manner that is consistent
with the modulation of work production. In rats, the biceps femoris (BF)
shortens more (from 16% to 21%), presumably doing more net work, when rats
shift from level to incline locomotion (15°;
Gillis and Biewener, 2002
).
Correspondingly, the vastus lateralis (VL) undergoes less net lengthening and
presumably less energy absorption at the knee during level versus
incline locomotion. Although initial lengthening of the rat VL is generally
uniform, the amount of subsequent shortening strain varies with gait and
grade, being greatest when the rats gallop and when they move uphill.
Interestingly, rats also increase the stance duration and duty factor of their
hind limb during incline versus level locomotion, in contrast to the
absence of such changes observed here in tammar wallabies. Large active
shortening strains (recorded in the semimembranosus of dogs;
Gregersen et al., 1998
) and
analyses of joint work in goats (Pandy et
al., 1988
) and humans (Belli et
al., 2002
) also suggest that proximal limb muscles may play a
greater role in work modulation than distal leg muscles. However, because of
the likely transfer of work by biarticular muscles across the knee to the
ankle (van Ingen Schenau,
1990
), interpretations of a proximo-distal `division of labor' of
muscle work drawn from studies of joint work alone are limited and must be
viewed with caution. This may be offset, to some extent, when interpretations
of muscle work are also based on patterns of muscle strain and EMG timing.
Nevertheless, the absence of force measurements in more proximal muscles
necessarily hinders an evaluation of whether a proximo-distal division of
labor exists in terms of work modulation versus elastic energy
savings. Additional study of proximal muscles and limb muscles of other
species, as well as the development of improved methods for evaluating
proximal muscle forces, is needed to better test the generality of this
view.
Importantly, the results of Roberts et al.
(1997) for the turkey LG show
that specialization of muscle-tendon architecture per se may not
limit a muscle's ability to contribute to changing demands of mechanical work.
In part, this is because differences in muscle architecture alone do not favor
differences in work performance. Although shorter fibered muscles favor
increased energy economy because they can generate greater force per unit
volume of muscle that is activated
(Biewener and Roberts, 2000
;
Roberts et al., 1998
), the
increase in force is offset by the reduced length change for a given fiber
strain, maintaining work and power output similar to that of a longer-fibered
muscle. In a recent study of two distal leg muscles of guinea fowl (Numida
meleagris), Daley and Biewener
(2003
) found that the LG and
digital flexor (DFIV) both increase their net shortening and work production
when guinea fowl shift from level to incline (16°) running. However,
assuming that all limb extensors do the same mass-specific work, the
contribution of these two distal muscles to the animal's incline potential
energy work was only one-third of that predicted for their mass. Consequently,
these results also suggest that proximal limb muscles may play a greater role
in modulating work to accommodate varying locomotor demands, such as changes
in grade. Interestingly, the guinea fowl LG also contributed to work
production (7.7 J kg-1 muscle) during level running by shortening
10-15%, compared with nearly zero net work done by the DFIV
(Daley and Biewener, 2003
).
The basis for the difference in LG behavior compared with the turkey LG
(Roberts et al., 1997
) is
unclear but may reflect differences in body size and underlying differences in
leg stiffness associated with tendon stiffness and length, with guinea fowl
having less stiff limbs and relatively longer and thinner uncalcified
tendons.
Hence, in addition to muscle architecture, tendon geometry is also an
important determinant of the mechanical role and contractile behavior of a
muscle (Alexander, 1988;
Biewener, 1998a
;
Ker et al., 1988
). With long
thin tendons, elastic energy saving is favored for a given level of force, but
this also increases the series-elastic compliance against which a muscle's
fibers must shorten to control length and limb and joint positions.
Consequently, the pinnate design of distal leg muscles that attach to long
tendons is well suited to elastic energy savings but less suited to positional
control. By contracting under near isometric conditions, or over short ranges
of stretch followed by limited shortening, muscles can generate greater forces
and therefore increase the economy of force generation, despite their role in
work modulation being reduced. This is clearly the behavior that we observed
here for two of the main hind leg muscle-tendon units of tammar wallabies.
Even more extreme are the highly specialized fore- and hindlimb digital
flexors of horses and other large ungulates
(Biewener, 1998b
;
Dimery et al., 1986
). The very
short fibers of these muscles attach to such long tendons that they cannot
possibly contribute meaningful work or length control
(Biewener, 1997
;
Wilson et al., 2001
). Recent
measurements by Wilson et al.
(2001
) show that the retention
of extremely short fibers in these muscles can contribute to viscous damping
of potentially damaging or destabilizing limb vibrations, in addition to
favoring elastic energy savings in the tendons.
Neural activation in relation to contractile dynamics among muscle
agonists
Not surprisingly, the stereotypic contractile behavior of the tammar
wallaby LG and PL resulted from generally uniform patterns of muscle
activation during level versus incline locomotion. In both instances,
activation and force development of the LG preceded the PL, occurring 48-50 ms
prior to limb contact. Activation of the PL followed so that its force
development began at the onset of limb support. The earlier activation of the
LG is consistent with its role in decelerating the inertia of the foot and
countering ankle flexion. Interestingly, the use of active muscle force to
control foot inertia in wallabies is distinct from the role of passive
muscle-tendon properties used by turkeys to decelerate their foot when running
(Roberts et al., 1997). In
addition to extending the ankle, the PL also serves as an agonist of the
flexor digitorum muscle at the MP and phalangeal joints, which may explain its
more delayed force development pattern
(Biewener and Baudinette,
1995
). Earlier activation of the LG also corresponds with the
earlier and more substantial initial shortening strain of the muscle's
fascicles compared with the PL. Even so, initial shortening at the onset of
force development was observed in both muscles
(Fig. 4) and is likely to
reflect fascicle work done to stretch the muscles' aponeurosis and tendon when
these are most compliant at low force levels
(Bennett et al., 1986
;
Shadwick, 1990
). This
presumably increases the overall stiffness of the muscle-tendon unit, which
allows for rapid force development (important for tendon elastic strain
storage and recovery) once the foot is solidly in contact with the ground.
Consistent with this interpretation, fascicle strains in the LG and PL were
very small (<2%) once force development exceeded 33% of peak force
(Fig. 4). As we have also
observed in the rapidly contracting pectoralis muscle of birds during flight
(Biewener et al., 1998
;
Dial and Biewener, 1993
),
activation of the wallaby LG and PL ends shortly after the muscle develops
peak force. Much of force development therefore occurs after muscle
stimulation has ended. This probably allows the muscle to relax by the end of
limb support (or wing downstroke), avoiding unnecessary work to re-extend the
muscle by its antagonist.
Changes in the relative phase of muscle activation are likely to be an
important means by which muscle work is modulated. In contrast to our findings
for the wallaby LG and PL, Roberts et al.
(1997) found that activation
of the turkey LG during uphill running was phase-advanced relative to the
onset of limb support and showed evidence (based on integrated EMG) of
increased muscle recruitment. This earlier activation was consistent with the
increased shortening and work performed by the turkey LG during uphill
running. Presumably such a shift in the timing of neural activation might also
enable the tammar wallaby LG and PL to contribute useful muscle work during
incline hopping, but this was not observed (indeed, the PL showed a reduced
phase advance during incline hopping). Although more extreme grades might
involve such a phase advance in neural activation, one reason why wallabies
may not do this is the loss of force that would result from fascicle
shortening. Such a loss (due to force-velocity effects) would necessarily
require increased recruitment of these muscles, similar to that observed for
the turkey LG. However, this would also incur a greater metabolic cost to
generate the same level of force. Given that the magnitude of force did not
change significantly during level versus incline hopping in these two
muscles, increased shortening would necessarily have reduced their economy to
generate comparable levels of force over the duration of limb support. Thus,
it seems clear that more proximal muscles of the tammar wallaby must
contribute the additional work required for incline hopping.
Varying muscle EMG patterns with respect to shifts in locomotor grade,
presumably to modulate muscle work, have been observed in other species that
have been studied. In rats, neural activation of the BF and VL did not shift
temporally but increased intensity during incline versus level and
decline running (Gillis and Biewener,
2002). Similar increases in EMG intensity (suggesting greater
activation or increased recruitment volume) with incline locomotion have also
been observed in cats (Buford and Smith,
1990
) and horses (Robert et
al., 2000
), as well as in the turkey LG
(Roberts et al., 1997
). In
guinea fowl, no significant shift in the activation of the LG and DF-IV with
respect to uphill running was observed
(Daley and Biewener, 2003
).
Whereas our results here for tammar wallabies showed no change in LG EMG
phase, duration or intensity with a shift to incline hopping, we did observe a
significant increase in EMG intensity relative to reductions in phase and
duration in the PL. Consequently, it seems clear that varying patterns of
neural activation of limb muscles are observed when animals change locomotor
grade. Most generally, changes in motor recruitment are observed, but our
results for wallabies show that such patterns may be absent or compensated for
by an opposing shift in duration when changes in force and work output are
minimal.
In summary, while there is evidence that distal muscle-tendon units are
capable of contributing to work modulation by the limb as a whole
(Roberts et al., 1997), it
seems likely that, for at least some species, a `division of labor' may exist
among different muscle groups within the limb that is favorable in terms of
metabolic energy expenditure. This view, and our working hypothesis, holds
that more proximal, longer-fibered muscles are better suited to length and
work modulation, while more distal muscles favor energy savings by economical
force development and tendon elastic storage. This is supported by our
findings reported here for the distal leg muscles of tammar wallabies, as well
as recent observations for a few proximal muscles in the hind limbs of other
terrestrial vertebrate species. Even so, further work is needed to explore how
contractile performance varies among different muscle groups and joints within
the limb as a whole, particularly under varying conditions of locomotor
performance that demand changes in muscle work and force.
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