In vivo muscle function vs speed II. Muscle function trotting up an incline
1 Equine Research Center, California State Polytechnic University, Pomona,
CA 91768-4032, USA
2 Biological Sciences Department, California State Polytechnic University,
Pomona, CA 91768-4032, USA
3 Concord Field Station, Department of Organismic and Evolutionary Biology,
Harvard University, Bedford, MA 01730, USA
* Author for correspondence (e-mail: sjwickler{at}csupomona.edu)
Accepted 22 December 2004
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Summary |
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Key words: Locomotion, quadruped, sonomicrometry, muscle
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Introduction |
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In steady-state trotting at different speeds in the horse, an elbow
extensor (the lateral head of the triceps) and a knee extensor (the vastus
lateralis) provide a comparison of muscle strains in paralleled-fibered
muscles from limbs that have different roles in forward locomotion
(Hoyt et al., 2005). In the
horse, the triceps had shortening strains of around 10% while the vastus
shortened 8% during the stance phase of level trotting
(Hoyt et al., 2005
). Although
these strains are of similar magnitude, the patterns of length change are
complex and reflect the different roles of the forelimb and the hindlimb: the
former acts more as a stiff spring-like strut
(McGuigan and Wilson, 2003
)
and the latter modulates power for propulsion
(Dutto et al., 2004
).
Because of the 250% increase in metabolic rate in horses trotting up a 10%
incline (Wickler et al., 2000)
which is, presumably, a result of the increased requirement for mechanical
work, we hypothesized that muscle strain during trotting would be increased in
both the triceps and the vastus over that observed when trotting on the level
(Hoyt et al., 2005
). Because
the time of ground contact when going up a 10% incline is similar to that on
the level (Hoyt et al., 2000
),
an increase in strain on the incline would produce increased strain rate.
Owing to force-velocity effects, an increased shortening velocity means that
active muscle fibers produce less force. So, although muscle forces on the
incline need not be increased (Biewener et
al., 2004
; Roberts et al.,
1997
), an increase in shortening velocity suggests that a greater
volume of muscle must be recruited to maintain the same force. Based on this
reasoning, we hypothesized that the strain rate of both muscles would be
elevated during incline trotting and that EMG (electromyographic) activity
would be increased in both muscles as well. We examined the lateral head of
the triceps and the vastus lateralis while trotting up a 10% incline
(5.7°) over a range of speeds.
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Materials and methods |
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Surgical procedures
Surgery was done on standing, sedated horses (butorphanol tartrate, Fort
Dodge Animal Health, Fort Dodge, IA; 0.1 mg kg-1 and detomidine
hydrochloride, Pfizer Animal Health, Exton, PA; 20-40 µg kg-1)
and local anesthesia (lidocaine HCl, Pro Labs Ltd., St Joseph, MO, USA). The
location of the lateral triceps (M. triceps brachii caput laterale) and vastus
(M. vastus lateralis) was determined using palpable landmarks: anatomic
locations were studied on several cadavers prior to surgery and anatomic
validation of sonomicrometer crystal placement was done on three horses not
part of this study that were euthanized for medical conditions not related to
musculoskeletal dysfunction.
The fascia of the triceps and vastus was exposed by removing subcutaneous fat and, in the case of the triceps, incision through the omobrachialis muscle. One pair of 2 mm omni-directional, spherical, piezoelectric crystals (Tack crystals, Sonometrics Corporation, London, Ontario, Canada) was implanted 1 cm deep, 10-15 mm apart in a line parallel to muscle fiber orientation to measure changes in muscle fiber length. The crystals were anchored to muscle fascia using 0 silk suture and a tension relief loop.
Electromyography electrodes (AS636, Cooner Wire, Chatsworth, CA, USA) were
inserted by a sew-through technique
(Carrier, 1996) 1 cm away from,
and parallel to, the sonomicrometry crystals. The EMG signal was amplified
(1,000-10,000, depending on signal strength) and filtered (60 Hz notch and
100-1,000 Hz bandpass). A ground wire was implanted subcutaneously into the
dorsal aspect of the horse's sacral region. Banamine® (flunixin meglumine,
Schering-Plough Animal Health Corp., Union, NJ; 20-40 µg kg-1)
was administered post-surgery to reduce pain and act as an
anti-inflammatory.
Data from the sonomicrometry crystals were obtained using Sonometrics System Software and output to the data acquisition software that also sampled EMG signals at 3704 Hz (LabVIEW®, National Instruments, Austin, TX, USA).
Data collection
A biaxial accelerometer (±50 g; CXL25M2, Crossbow
Technology, Incorporated, San Jose, CA, USA) was taped on the lateral aspect
of the hoof of the right hindlimb to record hoof contact and break-over (the
end of stance when the hoof leaves the treadmill). All accelerometer data were
collected at 3704 Hz.
Each horse was run on a high-speed treadmill under two conditions: on the
level and up a 10% incline. Incline data are the focus of this paper. Horses
were run under each condition at speeds from 2.5-4.5 m s-1 in 0.25
m s-1 increments. The conditions and speeds were randomly ordered.
Horses were brought up to speed and, after 45 s at speed, data were collected.
All 18 experimental conditions (nine speeds at 0% and 10% incline) were run in
succession, with a 30 min. break after the first nine (results for 0%, level
trotting, are given in Hoyt et al.,
2005). Sonomicrometry crystals were removed at the end of the day
and the surgical wounds sutured and dressed. No animal, either during the
study or after removal of the crystals, experienced any lameness.
Kinematic data
Reflective markers (Peak Performance Technologies, Englewood, CO, USA) were
glued to the skin on the lateral side of each limb, using standard palpable
positions (Back et al., 1993).
The horses were filmed at 125 Hz using a Model PCI Motion Scope® camera
(Redlake Camera Corp., Morgan Hill, CA, USA) placed approximately 8.5 m away
from the treadmill. A linear calibration was performed daily. Five consecutive
strides were captured and digitized (Motus®, Peak Performance
Technologies, Englewood, CO, USA) for each horse at each speed and condition
(level and incline). The angular data were smoothed using a cubic spline
filter, normalized for time using a cubic spline fit, and five strides for
each horse, speed and condition were averaged using the trial averaging
feature of Motus. These data were used to determine mean joint angle of the
knee and elbow at first hoof contact, mid-stance, maximum extension (elbow)
and flexion (knee) and break-over, and analyzed for range of motion between
these events. The angles reported are for the anterior aspect of the elbow
joint and the posterior aspect of the knee.
Data processing
First hoof contact, break-over and second hoof contact were determined
using the record from the accelerometer and the high-speed video, and from
these were calculated duration of stance phase (tc=time of
contact) and duration of swing phase. All other stride parameters were derived
from these measurements and speed. The timing of the EMG and sonomicrometry
records, relative to stance phase, was based upon the simultaneously collected
accelerometry record.
Muscle length changes (and velocities of shortening) were analyzed only for
the time of contact because of its central role in determining metabolic cost
(Kram and Taylor, 1990),
although recent work identifies a significant energetic cost associated with
the swing phase (Marsh et al.,
2004
). All muscle fascicle lengths were normalized to their
fractional length change (or strain) by dividing measured lengths L
by the resting muscle length Lo
(L/Lo). The measurement of Lo
was recorded with the animal standing with its metacarpals and metatarsals
perpendicular to the surface of the treadmill. In order to calculate total
strain (muscle shortening) over the range of speeds, sonomicrometry records of
individual strides were temporally normalized to 100% of time of contact
(tc) using a cubic spline interpolation. Changes in muscle
lengths (
L) were measured at increments of 0.5% of
tc (201 increments per contact period). Because strain
patterns were analyzed in conjunction with kinematics on the level
(Hoyt et al., 2005
), the
average normalized muscle length data for results on the incline were divided
into phases based upon the kinematics of the appropriate joint (joint
kinematics were determined from five strides recorded simultaneously
comprising a sub-set of the ten strides averaged for muscle length). The net
strain (change in muscle length, with shortening being negative) occurring
during each phase was determined for each animal and trial. Stain rate
(quantified as L s-1) during each phase was determined
from the net strain and the duration of the phase in that trial.
Electromyography records were filtered using a second order low pass filter (1000 Hz), rectified and integrated, and analyzed for: (1) when the EMG started relative to hoof contact, (2) total duration of the EMG signal (including if it started before stance), (3) the length of the signal (only during stance) as a percentage of tc, and (4) the integrated EMG (IEMG) during stance.
Statistics
A two-way analysis of variance with repeated measures was run on all data
using SuperANOVA software (Abacus Concepts Inc., Berkeley, CA, USA) with
significance set at P<0.05. The two variables tested were speed
and muscle, and the four horses were used as the repeated measure. An
additional ANOVA was run using speed and condition (level vs incline)
to test for differences between conditions. For those conditions in which
there was a significant interaction, differences between conditions were
analyzed using a designed contrast analysis (Abacus Concepts Inc., Berkeley,
CA).
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Results |
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Strain and strain rate
In an effort to analyze better the concentric and eccentric contractions of
the muscles during stance, muscle strain patterns were divided into phases
based on the kinematics of the joint (Fig.
3) - an approach used by Hoyt et al.
(2005).
Triceps
Phase 1 was a period of elbow extension, and the end of this phase
increased with speed from 20 to 30% of stance. This was an anomalous phase
when the joint extended but the muscle lengthened 5.2%
(Table 1). Phase 2 was a period
of elbow flexion that lasted for 10% of the stance phase at all speeds, and
during which the triceps shortened by 1.4%. In the third phase, the elbow
extended while the triceps shortened concentrically by 18%. There was no
change with speed in the amount of strain during phase 3
(Fig. 4). Because phase three
lasted for 50% of the entire stance period and included midstance, when ground
reaction forces reach a maximum, it seems probable that most of the concentric
work required to trot uphill was done during this phase. For this reason, and
because there was no effect of slope on the strain observed during phases 1
and 2, only the data for phase 3 are plotted in
Fig. 4 and considered in
subsequent discussions.
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Shortening strain rate (Fig. 4) of the triceps increased with speed (P=0.005) and was greater on the incline than on the level (P=0.050). At the lowest speed the shortening rate during incline trotting was approximately three times greater than on the level but it was only 1.2 times greater at the highest speed (4.5 m s-1).
Vastus
There were two distinct patterns of muscle strain observed in each of two
horses during level locomotion (Hoyt et
al., 2005) but these differences were attenuated on an incline.
Phase 1 (Fig. 3) was a period
of knee flexion and muscle shortening that lasted for the first 14% of stance
(Table 1), a period that did
not change with speed but was shorter than during level trotting. The vastus
shortened by 6.4%, an amount similar to than on the level. Phase 2 was only
observed in two horses, and lasted for only a brief period of stance (about
3%). During level trotting, this phase was characterized by substantive
lengthening in two horses. However, when these horses trotted up an incline
this lengthening was attenuated, amounting to 0.6%. The magnitude of this
change was unaffected by speed. Phase 3 on the incline was characterized by a
brief period of knee extension (starting at 17% of the stance period and
ending at 31%) and vastus shortening of 3.6%
(Fig. 5). Shortening strain was
not different with speed (P=0.49). No difference in phase 3
shortening strain was observed between level and incline. Phase 4 was a period
of knee flexion that lasted from 31% of stance until about 60%, during which
the vastus shortened by 5.4%, a value statistically not different from the 2%
shortening observed in the muscle during this phase of level locomotion. Phase
4 muscle shortening did not differ with speed. Phase 5 lasted from 59% of
stance until approximately 90% of stance and was characterized by a period of
knee extension and vastus shortening. The vastus shortened 9.7% compared to
3.1% during level locomotion but did not change with speed. Thus total
shortening strain during phases 3, 4, and 5 was greater (18.5% vs
8.1%) on the incline. There was no effect of speed (P=0.194) when
phases 3-5 were combined and analyzed.
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For phase 3 and 5, shortening rates (Fig. 6) increased with speed (P=0.023, P<0.001, respectively) but not for phase 4 (P=0.103). Shortening rates were higher on the incline than on the level for phases 4 (P=0.040) and 5 (P=0.022), but not for phase 3 P=0.729). Thus the average shortening rate during phases 3-5 was 1.7 times as fast on the incline (0.958 L s-1) as on the level (0.568).
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EMG
Triceps
EMG activity (Fig. 7) of the
triceps initiated prior to foot contact (termed here as `activation phase
advance') and increased slightly with trotting speed (P=0.005), so
that at 4.5 m s-1 triceps EMG activity preceded foot contact by 8.5
ms. This differed from level trotting, where triceps activation was phase
advanced by an average of 36 ms relative to foot contact
(Hoyt et al., 2005) and did
not change with speed (P=0.746). The percentage of time during the
stance that the triceps EMG was active decreased with speed
(P<0.001) and was 19.4% longer on the incline than on the level
(P=0.001). Even though triceps EMG duration decreased with speed, its
integrated activity (IEMG) increased (P<0.001) with speed and
averaged 80% higher on the incline compared with the level
(P=0.003).
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Vastus
At low trotting speeds on the incline, the vastus became active at hoof
contact, and similar to the triceps, became more phase advanced relative to
limb contact as speed increased (P<0.001). The percentage of time
that vastus EMG was active during stance also decreased with speed
(P=0.006) but the muscle was active 12% longer on the incline
compared with the level (P=0.001). Similar to triceps, vastus IEMG
increased with speed (P=0.024) and was 113% greater on the incline
than on the level (P=0.003).
Stride parameters
Fig. 8 gives details of the
stride parameters. The horses' stride period decreased with speed
(P<0.001) and averaged 5% longer on the incline than on the level
(P=0.048). The horses' swing period in the forelimb did not change
with speed (P=0.499) but decreased in the hindlimb
(P<0.001) and was 11% shorter in the forelimb than the hind when
averaged over all speeds (P=0.001). When compared to level trotting,
there was no difference in swing time for the forelimb (P=0.149) or
the hindlimb on the incline (P=0.075). The time of ground
contact, tc, decreased with speed in both
limbs (P<0.001) and was 11% longer for the forelimb than the
hindlimb (P=0.048), matching the 11% decline in forelimb swing time.
When compared to level trotting, tc during incline
trotting was 5% longer in the forelimb (P<0.001) but not different
for the hindlimb (P=0.139). Step length (the distance the body moves
during limb contact), increased with speed for both limbs
(P<0.001) and was 11% longer for the forelimb (P=0.052),
associated with the longer contact time of the forelimb. When compared to
level locomotion, step length was 5% longer on the incline for the forelimb
(P=0.001) but did not differ for the hindlimb (P=0.207).
Duty factor, the proportion of time the foot is in contact with the ground
during the entire stride, decreased with speed (P<0.001) and was
12% greater for the forelimb than the hindlimb (P=0.014). When
compared to level locomotion, no difference in duty factor was observed for
either limb (forelimb, P=0.897; hindlimb, P=0.727).
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Discussion |
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Because shortening strains in both muscles were increased on an incline compared to on the level, and limb contact times remained unchanged (Fig. 8), it makes sense that there was an increase in the muscles' shortening strain rates on the incline for both the triceps (Fig. 4) and vastus (Fig. 6). Therefore, because of the force-velocity relationship of skeletal muscle, one would expect to find that more motor units within each muscle must be activated to produce the same force. This would seem to explain the observation that both muscles' EMG activity increased in magnitude and duration (Fig. 7) on an incline. However, the explanation may be more complex than this if muscle forces are changed on an incline.
In general, forces in distal leg muscles have not been found to increase
during incline locomotion in running turkeys and hopping wallabies
(Biewener et al., 2004;
Roberts et al., 1997
). Whereas
no change in the medial gastrocnemius force was observed in turkeys running on
a 10% incline (Roberts et al.,
1997
), lateral gastrocnemius force decreased by 8% and plantaris
force increased by 9% in tammar wallabies hopping on a 10% incline
(Biewener et al., 2004
).
However, in a smaller avian biped, lateral gastrocnemius forces were observed
to increase by 38% and digital flexor (DF-4) by 12% when guinea fowl ran on a
16% incline (Daley and Biewener,
2003
). The increase in muscle force for this species may reflect
the steeper incline and/or its smaller size and differences in muscle-tendon
architecture.
There have been few direct measurements of muscle forces in quadrupeds
locomoting on the level and incline but the available data suggest that muscle
forces may be different under these two conditions. In cats walking up a
30-60° incline, forces in the tendon of the medial gastrocnemius are
higher than on the level but those in the soleus are not changed
(Kaya et al., 2003). In the
horse, unless there are changes in limb mechanical advantage, muscle forces
may not be the same on the incline as on the level because peak ground
reaction force (GRF) changes on an incline: forelimb peak GRF is lower on an
incline than on the level and hindlimb peak GRF is elevated at higher trotting
speeds on an incline (Dutto et al.,
2004
). Therefore, until muscle forces can be empirically
determined in horses, it is not clear whether the increased EMG activity on an
incline is due to increased strain rate alone or also reflects an increase in
muscle force development.
Changes in timing of EMG activity (Fig.
7) are similar to those observed in other species. In the horse
triceps, the muscle was activated 20 ms after contact at low speeds, and 10 ms
prior to contact at 4.5 m s-1. This activation was later than
observed on the level (Hoyt et al.,
2005). In the vastus, the EMG started at contact at lower speeds
and 60 ms prior to contact at 4.5 m s-1 - again, later than on the
level. This delay in the timing of onset of EMGs in the vastus on an incline
is also apparent in the trotting rat
(Gillis and Biewener, 2002
)
and the trotting horse (Robert et al.,
2000
).
The increase in integrated EMG (IEMG) with speed and with incline has also
been observed in: (a) another knee extensor of the horse, the tensor fasciae
latae, and a hip extensor, the gluteus medius
(Robert et al., 2000); (b) the
vastus and biceps femoris of the rat
(Gillis and Biewener, 2002
),
and (c) some hindlimb muscles (but not all) of the cat
(Roy et al., 1991
). The 80%
increase of IEMG does not seem to reflect the 250% increase in metabolic rate
that occurs with a 10% incline (Eaton et
al., 1995
; Wickler et al.,
2000
). However, this is not surprising, as we only measured the
length changes and activity of one muscle in each limb, and we do not know the
force or power output of these muscles or the joints at which they act
(principally the elbow and knee) compared with other joints of the limbs.
Furthermore, the electrodes are small, superficial, parallel to the surface
fibers and, because the volume of the muscle is large relative to the region
sampled by the electrodes, such recordings are sensitive to
compartmentalization of recruitment patterns within the muscle
(English, 1984
;
Scholle et al., 2001
).
Increased muscle fascicle strain on an incline was observed in the turkey
lateral gastrocnemius (Roberts et al.,
1997), in guinea fowl lateral gastrocnemius (45% increase) and
digital flexor (Daley and Biewener,
2003
), but, in tammar wallabies, neither the lateral gastrocnemius
nor the plantaris increased their strain
(Biewener et al., 2004
). In
rats moving up an incline (Gillis and
Biewener, 2002
), strain increased in the biceps femoris, but not
in the vastus (at least during trotting). In contrast to the horse vastus,
which shortens, the rat vastus undergoes substantial lengthening even when
trotting uphill. This suggests that the horse vastus contributes positive work
during incline trotting, but the rat vastus absorbs energy, requiring that
other muscles (including the biceps) increase their shortening to raise the
animal's mass. These differences are probably due to locomotion limb design
and pattern (digitigrade vs unguligrade), or other anatomical
features of muscle origins and insertions. Such differences are certainly
underscored by the different strain patterns observed in the vastus lateralis
of rats (Gillis and Biewener,
2001
) and dogs (Carrier et al.,
1998
) - despite the similarities in the kinematics of their knees
during trotting.
The scaling of metabolic rate during level locomotion over a wide range of
size in mammals and birds is correlated with the inverse of time of contact
(Kram and Taylor, 1990). It
has been hypothesized that 1/tc reflects the rate of force
development by the antigravity muscles. In the present study of incline
trotting in the horse, we observed a decrease in tc for
both fore- and hindlimb as speed increased, consistent with the increased
metabolic rate at higher trotting speeds
(Wickler et al., 2000
).
However, tc was not different between incline and level
conditions at a given trotting speed, even though the horses' metabolic rate
was 2.5 times greater at all trotting speeds
(Wickler et al., 2000
). Much
of the observed increase in metabolic cost on the incline, therefore, must
reflect increased muscle recruitment associated with the increased muscle
shortening strain and the resulting loss of force produced by active
fibers.
As expected, the time of contact decreased relatively more than swing time
as speed increased, resulting in a decrease in duty factor. Typically
(Alexander et al., 1979;
Biewener, 2003
;
Dutto et al., 2004
), a
decrease in duty factor results in an increase in peak ground reaction force
(GRF). On the level, this generalization was true for the forelimb as speed
increased, but not for the hindlimb, where forces were independent of speed
(Dutto et al., 2004
). While
duty factor of both limbs was the same on the incline as on the level, peak
GRF on an incline was not the same as on the level
(Dutto et al., 2004
).
This study originated from an interest in integrating whole animal energetics and muscle function. While the observations of increased muscle strain are consistent with the increased energetic demands for uphill locomotion, we only measured one muscle in each limb. A better linking of muscle contractile patterns to their significance for muscle work, joint dynamics and whole limb movement will require analysis of more muscles of varying architecture, as well as measurements of muscle forces.
Conclusion
The mechanical work required to elevate the center of mass of a quadruped
during locomotion up an incline requires an increase in shortening strain of
the antigravity muscles of both the fore- and hindlimbs. Because fore- and
hindlimb contact times do not differ between level and incline trotting at the
same speed, limb muscles that contribute increased work to move up an incline
must contract with an increased strain rate. We confirmed these changes for
two representative antigravity muscles of the horse: triceps (lateral head)
and vastus lateralis. The increased shortening velocities of these two muscles
probably reduce the force that any given set of activated muscle fiber can
produce. If this pattern holds for other limb muscles that do work to elevate
the horse's center of mass on an incline, then a greater volume of muscle must
be recruited to generate an equivalent force for body support. This was
reflected in significant increases in the EMG intensity (IEMG) of both
muscles. With increasing speed, time of contact (and duty factor) decreases,
compounding the need for additional motor recruitment.
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Acknowledgments |
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