Download Lower extremity muscle activation during horizontal and uphill running

Lower extremity muscle activation during horizontal
and uphill running
MARK A. SLONIGER, KIRK J. CURETON, BARRY M. PRIOR, AND ELLEN M. EVANS
Department of Exercise Science, The University of Georgia, Athens, Georgia 30602-6554
exercise; magnetic resonance imaging; skeletal muscle function
(EMG) (3, 4, 13, 21, 25–27, 37) and
muscle glycogen depletion (9–11) have been used extensively to determine lower extremity muscle activation
during running. However, the restricted sampling area
and invasive nature of these techniques limit their
usefulness, and a quantitative assessment of the muscle
activated is not possible.
Recently, exercise-induced contrast shifts in proton
magnetic resonance (MR) images have been used to
quantify muscle use during exercise (1, 2, 14, 16, 23, 33,
36, 42, 43). MR images provide unparalleled visualization of muscle and associated tissues. More importantly, muscles actively involved in exercise show increased signal intensity and ‘‘light up’’ in MR images,
permitting active and inactive muscle to be distinguished (15). Increased signal intensity results primarily from increases in skeletal muscle proton spin-spin
ELECTROMYOGRAPHY
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relaxation times (T2) and is most evident in T2weighted MR images (15). The exact cause of the
exercise-induced increase in T2 is unknown, but it is
hypothesized to reflect complex changes in the fractions
of extracellular and bound and unbound intracellular
water, resulting from muscle recruitment and metabolic activity (5, 6, 14, 16). Although application of this
new technology to study muscle activation patterns has
been limited, in part because there still is no agreement
on the mechanism underlying and on the physiological
meaning of exercise-induced T2 increases, considerable
data indicate that the method provides valuable practical information about muscle use. The magnitude of
exercise-induced elevations in T2 are directly related to
EMG activity, force and rate of work (1, 5, 14, 23), and
estimates of the cross-sectional area of muscle showing
increased T2 increase in direct proportion to force and
exercise intensity (2, 33). By quantifying the amount of
muscle showing a T2 increase, it is possible to estimate
the portion of individual muscles activated (2, 7, 33).
We recently reported that muscle activation in the
entire lower extremity was greater during exhaustive
uphill vs. horizontal running (39). However, the extent
of individual muscle activation during exhaustive horizontal and uphill running has not been reported, and
the contribution of individual muscles to the greater
overall muscle activation during uphill running is
unknown. Therefore, the specific aims of the present
study were 1) to determine the extent of individual
muscle or group activation during exhaustive horizontal and uphill running and 2) to assess their contribution to the greater overall muscle activation during
uphill vs. horizontal running. Exhaustive running was
selected because 1) it provided a common physiological
condition under which horizontal and uphill running
could be compared; 2) the highest level of muscle
activation during dynamic, ballistic, low-resistance
movement like running is unknown; and 3) to understand the basis for differences in metabolic responses, it
is important to know whether muscle activation is
greater during exhaustive uphill vs. horizontal running
(29, 39). We hypothesized that because running involves dynamic, ballistic, low-resistance movements,
that individual muscles in the lower extremity would
not be fully activated and that extent of activation
would vary depending on function. Uphill running was
expected to show increased activation of the hip and
knee extensors, and plantar flexors.
METHODS
Subjects. The subjects were 12 young women involved in
recreational running for conditioning at the time of the study.
Mean (6 SD) physical characteristics of the subjects were age
(23.8 6 2.7 yr), mass (59.7 6 8.2 kg), %fat (20.0 6 4.9%), and
0161-7567/97 $5.00 Copyright r 1997 the American Physiological Society
2073
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Sloniger, Mark A., Kirk J. Cureton, Barry M. Prior,
and Ellen M. Evans. Lower extremity muscle activation
during horizontal and uphill running. J. Appl. Physiol. 83(6):
2073–2079, 1997.—To provide more comprehensive information on the extent and pattern of muscle activation during
running, we determined lower extremity muscle activation by
using exercise-induced contrast shifts in magnetic resonance
(MR) images during horizontal and uphill high-intensity
(115% of peak oxygen uptake) running to exhaustion (2.0–3.9
min) in 12 young women. The mean percentage of muscle
volume activated in the right lower extremity was significantly (P ,0.05) greater during uphill (73 6 7%) than during
horizontal (67 6 8%) running. The percentage of 13 individual muscles or groups activated varied from 41 to 90%
during horizontal running and from 44 to 83% during uphill
running. During horizontal running, the muscles or groups
most activated were the adductors (90 6 5%), semitendinosus
(86 6 13%), gracilis (76 6 20%), biceps femoris (76 6 12%),
and semimembranosus (75 6 12%). During uphill running,
the muscles most activated were the adductors (83 6 8%),
biceps femoris (79 6 7%), gluteal group (79 6 11%), gastrocnemius (76 6 15%), and vastus group (75 6 13%). Compared
with horizontal running, uphill running required considerably greater activation of the vastus group (23%) and soleus
(14%) and less activation of the rectus femoris (29%), gracilis
(18%), and semitendinosus (17%). We conclude that during
high-intensity horizontal and uphill running to exhaustion,
lasting 2–3 min, muscles of the lower extremity are not
maximally activated, suggesting there is a limit to the extent
to which additional muscle mass recruitment can be utilized
to meet the demand for force and energy. Greater total muscle
activation during exhaustive uphill than during horizontal
running is achieved through an altered pattern of muscle
activation that involves increased use of some muscles and
less use of others.
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Running velocity ranged from 8.9 to 11.9 km/h for uphill and
14.0–19.0 km/h for horizontal running. Immediately after
exercise, MR images of the right lower extremity were once
again obtained after procedures used at rest. For each
individual, the time between termination of exercise and
completion of the postexercise image attainment was the
same from one test session to the next and ranged from 10.9
to 12.3 min.
MR images were analyzed by using a modified version of
the public-domain National Institutes of Health (NIH) Image
program (written by Wayne Rasband and available from the
internet at http://zipy.nimh.nih.gov or on floppy disk from
NTIS, 5285 Port Royal Rd. Springfield, VA 22161, part no.
PB93–504868). For each image, regions of interest were
defined by tracing each muscle or muscle group in the cross
section. The 13 muscle regions of interest were iliopsoas,
gluteus maximus-medius-minimus, sartorius, rectus femoris,
vastus lateralis-medialis-intermedius, adductor magnuslongus-brevis, gracilis, biceps femoris, semitendinosus, semimembranosus, gastrocnemius, soleus, and tibialis anterior
plus all remaining calf musculature. After spatial calibration,
muscle cross-sectional area and transverse relaxation times
T2 were determined for each region of interest. A T2 (2⁄3 of the
signal decay time) was calculated for each pixel within a
region of interest by using the formula T2 5 (ta 2 tb )/ln(ia/ib ),
where ta and tb are spin-echo collection times and ia and ib are
signal levels. Pixels with T2 values between 20 and 35 ms
were used to represent muscle at rest, based on reports in the
literature that resting T2 of muscle is ,28 ms with a SD of ,3
ms (2). Mean T2 values at rest were 29.7 6 0.6 and 29.7 6 0.4
ms for horizontal and uphill running, respectively. Pixels
with T2 values out of this range were considered nonmuscle.
This nonmuscle cross-sectional area was later subtracted
from the postexercise cross-sectional areas for the same test
session. In the postexercise images, active muscle and total
muscle cross-sectional areas for each region of interest were
determined. Pixels with T2 greater than the resting mean
plus 1 SD were assumed to represent muscle that had
recently performed contractile activity (2, 33).
Active and total muscle volumes were calculated by summing the products of the cross-sectional areas and the thickness of each section (10-mm thickness plus 20-mm space) for
each region of interest (18). The active muscle volume was
divided by the postexercise muscle volume to obtain the
percentage of muscle volume that was active. The volumes for
the 13 regions of interest were summed, and the same
calculation was made for the entire lower extremity. Postexercise muscle volumes for the lower extremity were not different (P . 0.05) between horizontal and uphill conditions.
The single-trial reliabilities (intraclass correlation coefficient from one-way analysis of variance) for the right lower
extremity muscle volume and T2 at rest, measured on 3
separate days, were 0.90 and 0.47, respectively; the withinsubjects SD values of replicate measurements were 53 cm3 for
volume and 0.49 ms for T2. The reliability of T2 was low
because the range of values was extremely small (28.5–30.7
ms). There were no significant differences among the three
means (29.7 6 0.6, 29.7 6 0.4, and 29.6 6 0.5 ms). Three
separate measurements of the cross-sectional area of the
same muscle region of interest at rest were obtained for 30
individual muscles. Based on these data, the single-trial
reliability for repeated determinations of a muscle crosssectional area was 0.99. The within-subjects SD of replicate
measurements was 0.53 cm2.
At the final test session, a whole body scan was obtained for
each subject by using dual-energy X-ray absorptiometry
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peak oxygen uptake (V̇O2 peak; 2.91 6 0.52 l/min or 48.6 6 5.2
ml · kg21 · min21 ). After an explanation of the time commitment and procedures involved in the study, each subject
provided written consent and completed medical history and
training background questionnaires. The study was approved
by the Institutional Review Board.
Testing procedures. Subjects completed five test sessions on
separate days. Two of these sessions were used to determine
V̇O2 peak and muscle activation during horizontal running and
two were used to obtain the same measurements during
uphill (10% grade) running. The order of test sessions was
balanced. During the first test session, subjects completed a
discontinuous, speed-incremented treadmill test to exhaustion under one of the two experimental conditions to determine V̇O2 peak. Subjects completed a series of 6-min bouts of
treadmill running in which treadmill speed was increased
until the subject could not finish a 6-min bout. Treadmill
speeds ranged from 7.9 to 17.1 km/h and from 5.3 to 9.8 km/h
for the horizontal and uphill conditions, respectively. During
the bouts of running, metabolic measurements were obtained
by using a computer-automated system. The volume of inspired air was measured by a Rayfield (Rayfield Equipment,
Waitsfield, VT) model 9200 mechanical flowmeter. The concentrations of carbon dioxide and oxygen in the expired air were
measured by Ametek CD-3A and S-A/I electronic gas analyzers. Standard gases analyzed by the micro-Scholander chemical gas analyzer were used to calibrate the analyzers before
the test. One-minute averages of oxygen uptake (V̇O2) and
other metabolic measurements were calculated every 15 s by
using modified Vista (Rayfield Equipment) software. Maximal heart rate (HR) was determined with a Polar Vantage XL
HR monitor. The highest V̇O2 obtained on the test was
operationally defined as the V̇O2 peak if there was a plateau in
V̇O2 between the last two stages of the test, as assessed by an
increase in V̇O2 of ,2.1 ml · kg21 · min21 (40), or if peak HR was
at least 90% of age-predicted maximum and respiratory
exchange ratio was .1.0.
The second test session under each condition involved
collection of MR images by using a 1.5-T superconducting
magnet (General Electric, Milwaukee, WI). These data were
used to assess right lower extremity exercise-induced contrast shifts in MR images. After a 10-min period of rest,
preexercise MR images were obtained of the right lower
extremity. The scanning procedure and data analysis used
were similar to these described by others (2, 33). Before image
collection, an external landmark was placed on the thigh, 20
cm distal to the iliac crest, and the exact location of the
external landmark was recorded on acetate paper. The acetate paper was reapplied at the remaining test sessions to
ensure that the placement of the landmark in the magnet
bore was consistent for each test session. During imaging,
subjects were supine, with their feet held together with an
elastic band, holding as still as possible. After the external
landmark was aligned with the cross-hairs of the imager, a
series of contiguous transaxial images 1 cm thick and spaced
2 cm apart were obtained from the region between the
patellar crest and iliac crest. A second series of transaxial
images 1 cm thick and spaced 2 cm apart were then obtained
of the region between the patellar crest and the ankle. Two
T2-weighted images (repetition time 5 1,300 ms; echo times 5
30 and 60 ms) were obtained within a 40-cm field body coil. A
256 3 128 matrix resolution and one excitation were used.
Scan time was 364 s, 182 s for each (patellar crest to iliac crest
and patellar crest to ankle) imaging sequence.
The subject then completed a bout of high-intensity (115%
V̇O2 peak) treadmill running to exhaustion. Mean treadmill
time was 2.6 6 0.5 min and ranged from 2.0 to 3.9 min.
MUSCLE ACTIVATION DURING RUNNING
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(Hologic QDR 1000-W, software version 5.5) to determine
total percent body fat.
Statistical analysis. A t-test for dependent samples was
used to determine the significance of differences between
dependent variables measured during uphill and horizontal
running. A significance level of P ,0.05 was used for the total
set of 14 comparisons (total lower extremity and 13 muscle
regions of interest), with the significance level for individual
comparisons (P # 0.004) adjusted by using the Bonferroni
technique.
RESULTS
Fig. 1. Percentage of muscle volume activated during horizontal and
uphill running. S, soleus; TA, tibialis anterior; GN, gastrocnemius;
SM, semimembranosus; BF, biceps femoris; ST, semitendinosus; GR,
gracilis; A, adductor; V, vastus; RF, rectus femoris; SR, sartorius; G,
gluteus; ILPM, iliopsoas. * Significantly different from other condition at P # 0.004.
Fig. 2. Spin-spin relaxation time (T2) of individual muscle regions of
interest for horizontal and uphill (10% grade) treadmill running.
* Significantly different from other condition at P # 0.004.
correlated (r 5 0.63) and, therefore, provided somewhat
different information.
During uphill running, the percentage of individual
muscle volume activated ranged from 44 to 83% (Fig.
1). The muscles most activated were the adductors
(83 6 8%), biceps femoris (79 6 7%), gluteal group
(79 6 11%), gastrocnemius (76 6 15%), and vastus
group (76 6 14%). The least activated muscles were the
rectus femoris (44 6 20%), soleus (55 6 14%), tibialis
anterior (58 6 16%), and gracilis (59 6 16%).
Mean T2 values varied from 30.1 to 37.9 ms during
uphill running. The muscles with the most intense use
were the gluteal group (37.9 6 3.5 ms), adductors
(36.2 6 1.4 ms), biceps femoris (35.8 6 2.3 ms),
gastrocnemius (35.6 6 2.3 ms), and semimembranosus
(35.5 6 2.3 ms). The least intensely used muscle was
the rectus femoris (30.1 6 2.0 ms). Under the uphill
condition, mean T2 and the percentage activation
results for the 13 muscle regions of interest were quite
highly correlated (r 5 0.86).
As reported previously (39), the mean percentage of
the right lower extremity muscle volume activated was
significantly (P ,0.004) greater during uphill (73 6 7%)
compared with horizontal (67 6 8%) running. The
mean percentage of muscle volume activated increased
significantly (P # 0.004) from horizontal to uphill
running for the vastus group (23%) and for soleus (14%)
and decreased significantly (P # 0.004) for the rectus
femoris (29%), gracilis (18%), and semitendinosus (17%).
Mean lower extremity T2 values were not significantly (P ,0.004) different between horizontal (34.0 6
0.9 ms) and uphill (34.2 6 1.0 ms) running. Mean T2
increased significantly (P # 0.004) from horizontal to
uphill running for the vastus group (1.6 ms) and
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During horizontal running, the percentage of the
volume of individual muscles or groups activated varied from 41 to 90% (Fig. 1). Those most activated were
the adductors (90 6 5%), semitendinosus (86 6 13%),
gracilis (76 6 20%), biceps femoris (76 6 12%), and
semimembranosus (75 6 12%). The least activated
were the soleus (41 6 18%), vastus group (53 6 11%),
sartorius (53 6 22%), and iliopsoas (59 6 15%).
Mean T2 values, which reflect the intensity of muscle
use, ranged from 32.1 to 37.2 ms during horizontal
running (Fig. 2). The muscles showing the most intense
use were the gluteal group (37.3 6 1.4 ms), adductor
group (36.9 6 1.2 ms), semitendinosus (36.9 6 1.8 ms),
and semimembranosus (35.0 6 1.0 ms). The least
intensely used were the iliopsoas (32.1 6 1.1), rectus
femoris (32.2 6 1.9), and vastus group (32.8 6 1.1).
Mean T2 and the percentage of muscle volume activated during horizontal running were only moderately
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MUSCLE ACTIVATION DURING RUNNING
decreased significantly (P # 0.004) for the gracilis (4.7
ms), semitendinosus (2.8 ms), and rectus femoris
(2.1 ms).
DISCUSSION
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Knowledge of muscle use during physical activity is
important in understanding the basis of movement; in
diagnosing disease; in normalizing metabolic and cardiovascular responses during exercise; and in understanding the effects of training, muscle disuse, and
rehabilitative treatments such as electromyostimulation. EMG has provided extensive information on the
temporal pattern and intensity of individual muscle
activation during physical activities, but this technique
is limited because only small areas of selected muscles
can be studied, and EMG signals are affected by a host
of factors that can make interpretation of data difficult
(3). Insight into muscle use during physical activity
also has been obtained from studies measuring glycogen depletion in different fiber types (9–11). However,
muscle biopsies are usually obtained only from a small
area of a one or a few muscles and, therefore, do not
provide comprehensive information on the amount of
muscle activated and the pattern of activation in
different muscles.
We used the powerful technique of MR imaging to
quantify the activation of individual muscles in the
lower extremity during exhaustive horizontal and uphill running. MR imaging provides unparalleled visualization of the muscle groups and most individual
muscles in a given limb segment. Exercise-induced
contrast shifts in T2-weighted MR images reflect muscle
recruitment and intensity of use (1, 14, 15, 23, 31, 38,
43). Furthermore, the absolute cross-sectional area and
volume of muscle that show the contrast shift (2, 33, 39)
can be quantified, providing unique information on the
proportion of available muscle that is activated, which
is not available through other approaches. This method
has been used to quantify muscle recruitment during
acute voluntary physical activity (2, 7, 32, 38) and
electrical stimulation of muscle (2) and consequent to
muscle unweighting (35) and training (8, 33). Our
interests were in quantifying individual lower extremity muscle activation during exhaustive running to
determine whether muscles are maximally activated at
the point of fatigue and in determining the contribution
of individual muscles to the greater overall muscle
activation during uphill compared with horizontal running to fatigue.
The primary finding was that muscles of the lower
extremity were not uniformly and maximally activated
during exhaustive horizontal and uphill running. The
percentage of the volume of 13 individual muscles or
muscle groups activated varied from 41 to 90% during
horizontal running and from 44 to 83% during uphill
running. Similarly, the intensity of muscle use as
reflected by the T2 values for individual muscle regions
of interest varied from 30 to 38 ms. Thus, even during
exhaustive exercise in which the energy demand could
not be sustained, some involved muscles were quite
heavily used, whereas others were not. This is not
surprising given the varying roles of different muscles
in the lower extremity in producing force at various
phases of the gait cycle during running (27). However,
even muscles that were most heavily involved were not
maximally activated during either horizontal or uphill
running. Less than complete activation of involved
muscle may reflect the ballistic, dynamic nature of
movements during running and the fact that nearmaximum levels of force are not needed. Furthermore,
in a 2- to 3-min effort, the maximal rate of power output
is less than during shorter efforts (28), which should
result in less muscle mass activated, assuming muscle
activation is proportional to power output. Failure to
recruit all available muscle is consistent with the fact
that in large muscle activity motor units rely primarily
on recruitment and less on rate coding to modulate
force (12). However, because the exercise was carried to
the point of exhaustion, these data suggest that there is
a limit to the extent to which additional muscle mass
recruitment can be utilized to meet the demand for
force and energy.
The incomplete activation of all available muscle is
consistent with studies involving exhaustive, heavyresistance exercise by using the same MR imaging
technique. In these studies involving leg extension by
electromyostimulation (2) or voluntary effort in the
squat or neck movements (7, 32, 33), five sets of 10
muscle actions to exhaustion (100% maximal load)
were accomplished by activating 70–85% of the involved muscle. As in the present study, the range of
individual muscle activation varied from 40% or below
to 90% or above. These studies involving heavyresistance exercise are consistent with the concept that
there may be a neural limitation to motor unit recruitment in some forms of exercise that prevents the full
force potential of muscle from being utilized during
voluntary contractions (12). Our data suggest that this
phenomenon exists for exhaustive horizontal and uphill running of 2- to 3-min duration.
Our data seem to conflict with studies on cycling that
have suggested that all fibers in some muscles are
activated during supramaximal exercise to exhaustion.
Glycogen depletion data on supramaximal cycling at
approximately the same relative intensity [122% maximal V̇O2 (V̇O2 max)] and duration as in the running in the
present study have suggested that all type I and type II
fibers in the lateral portion of the vastus lateralis are
activated (41). However, at higher intensities resulting
in exhaustion in 1 min (150% V̇O2 max) and 30 s (194%
V̇O2 max), respectively, higher rates of glycogen depletion
were observed, suggesting that muscle use was not
maximal at the lower intensity and implying that
increased frequency of stimulation must have accounted for the increased work output at higher intensities. However, differential activation of seven muscles
involved in force production during incremental cycling, with the gluteus maximus showing the greatest
relative activation at high intensities, has been found
(see Ref. 19a). Thus the extent to which the data from
lateral portion of the quadriceps can be used to represent
muscle recruitment and metabolic changes in other
MUSCLE ACTIVATION DURING RUNNING
activated increased significantly from horizontal to
uphill (10% grade) running for the vastus (43%) and
soleus (35%) muscles/muscle groups, whereas the increase for the gastrocnemius (11%) was not significant
(P . 0.004). The vastus lateralis was analyzed with the
vastus medialis and vastus intermedius as one group
(vastus); therefore, the change in activation for the
vastus lateralis alone could not be distinguished. The
results of the two studies are consistent in showing that
activation of the soleus and quadriceps muscles increased with uphill running.
The interpretation of our values for the percentage
activation of muscles depends in part on the validity of
the criterion used to classify whether muscle is active.
Adams et al. (2) first proposed that a T2 increase
greater than the resting mean 11 SD be used as the
criterion for classifying pixels of muscle active. Although arbitrary, this criterion has been used in a
number of previous studies (2, 7, 33, 39), and its
validity is supported by several observations. 1) The
mean T2 of resting skeletal muscle is consistently
28–29 ms, with an SD of ,3 ms or less in various
studies (2). Only a small amount of low-intensity
exercise is needed to significantly increase T2 values
(43). For example, Yue et al. (43) found that only five
repetitions of elbow flexion-extension exercise at 25%
maximal voluntary contraction or two repetitions at
80% maximal voluntary contraction were necessary to
detect a statistically significant (3–4%) increase in T2.
Moderate-to-heavy rates of work produce relative large
increases in T2, averaging 7–35% (7, 15, 17, 35, 36, 43),
and the magnitude of increase in T2 is independent of
muscle size (7, 36). Furthermore, exercise does not alter
the shape of the distribution of T2 values but simply
shifts the distribution to higher values (35). Thus the
T2 increase is a sensitive index of muscle activity. 2)
Elevations in T2 within the range observed in the
present study are directly related to EMG activity,
force, and rate of work (1, 14, 23), and estimates of the
cross-sectional area of muscle activated increase in
direct proportion to force and exercise intensity (2, 33).
Thus these indexes of muscle activity accurately reflect
intensity of muscle use. 3) Estimates of the percentage
of individual muscles activated by using this criterion
are reasonable, ranging from ,25% to over 90% (2, 7,
32, 33). Use of a different T2 cut-off point as the
criterion for ‘‘activated’’ muscle would obviously change
the absolute values, but any large change would result
in values that are implausible (35).
It is possible that the estimates of activated muscle
are slight underestimates, because increases in T2 in
some pixels may to too small to be considered active and
some T2 increases that may have exceeded the criterion
immediately after exercise may have dropped below the
criterion because of the time required to complete the
scans. The latter effect would be greater for muscle in
the leg, because it was always scanned after the thigh
and the time after exercise until the second scan was
completed was longer than usual. However, the mean
T2 for muscles in the leg were over 3 SDs above the
criterion, indicating that there would be few pixels that
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muscles of the lower extremity during cycling can be
questioned. In addition, data from cycling cannot be
generalized to running because of the marked differences in movement pattern.
EMG studies have provided considerable information on the phase of the gait cycle during which
individual muscles are active during horizontal running (27), but quantitative information comparing the
degree of activation of different muscles has not been
possible. We have shown that during exhaustive horizontal running, the muscles with the highest percentage of their volume activated were the adductor group
(90%), hamstrings [semitendinosus (86%), biceps femoris (76%), semimembranosus (75%)], gracilis (76%),
rectus femoris (74%), gluteal group (72%), and gastrocnemius (68%). All of these muscles except the rectus
femoris had relatively high T2 values (.34 ms), reflecting a high intensity of use. The gluteal group had the
highest T2 (37 ms), indicating that the portions of this
muscle group that were activated were used very
intensely. Our findings supplement those from EMG
studies by indicating that muscles involved in hip
stabilization and adduction (adductors and gracilis),
hip extension (gluteal and hamstrings), knee and hip
flexion-extension (hamstrings, rectus femoris, and gastrocnemius), and plantar flexion (gastrocnemius) were
the most intensely used during horizontal running.
We previously reported that the percentage of the
lower extremity muscle volume activated was greater
during uphill compared with horizontal running by 9%
(39). The present study shows that not all of the lower
extremity muscles were activated to a greater extent
during this condition; instead, the greater overall muscle
activation during uphill running was achieved through
increased activation of some muscle groups (vastus and
soleus) and less activation of others (rectus femoris,
gracilis, and semitendinosus). It is interesting that the
range of individual muscles/muscle group activation
was less during uphill running (44–83%) than during
horizontal running (41–90%), perhaps reflecting the
slower, more restricted movements performed. T2
changes were similar to changes in the volume of
muscle activated, as reflected by the relatively high
correlation between the two measurements (r 5 0.86)
during uphill running.
We are aware of only one other study comparing
lower extremity muscle utilization between horizontal
and uphill running. Costill et al. (10) determined
glycogen depletion of the vastus lateralis, gastrocnemius, and soleus muscles during horizontal and uphill
running. Subjects completed 2-h bouts of horizontal
and uphill (6% grade) treadmill running at 75% of
mode-specific V̇O2 max. Mean treadmill speeds were 8.3
and 13.8 km/h for uphill and horizontal conditions,
respectively. They reported that muscle glycogen was
depleted to a greater extent during uphill running for
all three muscles evaluated. Glycogen depletion for the
soleus and gastrocnemius increased 30% from horizontal to uphill running, whereas the increase for the
vastus lateralis was approximately threefold. In the
present study, the percentage of the muscle volume
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MUSCLE ACTIVATION DURING RUNNING
which additional muscle mass recruitment can be
utilized to meet the demand for force and energy.
Greater total muscle activation during exhaustive uphill than horizontal running is achieved through an
altered pattern of muscle activation that involves increased use of some muscles and less use of others.
We thank St. Mary’s Hospital, Athens, GA, for use of the magnetic
resonance imager, Debbie Eliopulos for technical support, and Mike
Conley and Gary Dudley for assistance with image analysis and
review of the manuscript.
Address for reprint requests: K. J. Cureton, Dept. of Exercise
Science, Ramsey Center, 300 River Rd., Univ. of Georgia, Athens, GA
30602-6554 (E-mail: [email protected]).
Received 23 August 1996; accepted in final form 21 July 1997.
REFERENCES
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initially exceeded the criterion that were not counted as
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certain, large error is unlikely, and the comparisons of
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valid.
The exact cellular mechanisms underlying the exercise-induced contrast shifts in transverse relaxation
times (T2) of MR images are unknown (1, 23, 43).
Because proton-weighted MR images are based on
signals from hydrogen atoms and because the primary
source of hydrogen in the human body is water, exerciseinduced changes in muscle T2 have been hypothesized
to be caused by movement of water into and among
compartments in muscle (15). This issue is complex;
multiple water fractions with different T2 values (extracellular water T2 5 196 ms, intracellular free water
T2 5 40–45 ms, and intracellular bound water T2 5
,16 ms) contribute to the T2 of skeletal muscle (20, 24),
and all probably change with exercise. However, simple
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explain T2 changes with exercise, because increased
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(14), head-down tilt (6), or external leg negative pressure (34) is associated with little, if any, increase in T2.
The T2 change with lower body negative pressure is
fundamentally different than that observed during
exercise (34). Increased muscle perfusion also is an
unlikely cause, because muscle T2 increases after
exercise with vascular occlusion (15). These findings
suggest that complex intracellular events are probably
responsible for the exercised-induced T2 increase. Decreased pH and/or lactate accumulation after exercise
may contribute to the T2 increase after exercise. Patients with McArdle’s disease, who lack phosphorylase,
the enzyme needed for breakdown of muscle glycogen,
and who do not experience lactate accumulation during
heavy exercise, have little T2 increase after exercise
(16, 22). Studies showing that T2 is negatively correlated with pH support this suggestion (22, 42). This
association is apparently not due to an osmotic effect of
lactate accumulation, because patients with mitochondrial myopathies, who display high lactate but little pH
change, show little T2 change during exercise (22).
Decrease in pH may decrease intracellular water bound
with macromolecules and increase free intracellular
water (19, 34). However, Cheng et al. (5) have shown
that the time course of the increase in T2 at the
beginning of exercise and the decrease during recovery
are faster than for pH. Thus the increase in T2 with
exercise appears to be related to the biochemical events
associated with muscle recruitment and increased energy metabolism, but the precise role of pH change
remains to be clarified.
We conclude that during high-intensity horizontal
and uphill running to exhaustion lasting 2–3 min
muscles of the lower extremity are not maximally
activated, suggesting there is a limit to the extent to
MUSCLE ACTIVATION DURING RUNNING
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