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Vol. 83, Issue 6, 2073-2079, December 1997
Department of Exercise Science, The University of Georgia, Athens, Georgia 30602-6554
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
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 ± 7%) than during horizontal (67 ± 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 ± 5%), semitendinosus (86 ± 13%), gracilis (76 ± 20%), biceps femoris (76 ± 12%), and
semimembranosus (75 ± 12%). During uphill running, the muscles
most activated were the adductors (83 ± 8%), biceps femoris (79 ± 7%), gluteal group (79 ± 11%), gastrocnemius (76 ± 15%), and vastus group (75 ± 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.
exercise; magnetic resonance imaging; skeletal muscle function
INTRODUCTION ELECTROMYOGRAPHY (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 relaxation
times (T2) and is most evident in T2-weighted 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 (± SD) physical
characteristics of the subjects were age (23.8 ± 2.7 yr), mass
(59.7 ± 8.2 kg), %fat (20.0 ± 4.9%), and peak oxygen uptake
( Testing procedures.
Subjects completed five test sessions on separate days. Two of these
sessions were used to determine
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 = 1,300 ms; echo times = 30 and 60 ms) were obtained within a
40-cm field body coil. A 256 × 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%
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 magnus-longus-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 ( 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 within-subjects 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 ± 0.6, 29.7 ± 0.4, and 29.6 ± 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 cross-sectional 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 (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 RESULTS 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 ± 5%), semitendinosus (86 ± 13%), gracilis (76 ± 20%), biceps femoris (76 ± 12%), and semimembranosus (75 ± 12%). The least activated were the soleus (41 ± 18%), vastus
group (53 ± 11%), sartorius (53 ± 22%), and iliopsoas (59 ± 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 ± 1.4 ms), adductor group (36.9 ± 1.2 ms), semitendinosus (36.9 ± 1.8 ms), and semimembranosus
(35.0 ± 1.0 ms). The least intensely used were the iliopsoas (32.1 ± 1.1), rectus femoris (32.2 ± 1.9), and vastus group (32.8 ± 1.1). Mean T2 and the percentage of muscle volume activated
during horizontal running were only moderately correlated
(r = 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 ± 8%), biceps femoris (79 ± 7%), gluteal group (79 ± 11%), gastrocnemius (76 ± 15%), and vastus group (76 ± 14%). The least activated muscles
were the rectus femoris (44 ± 20%), soleus (55 ± 14%),
tibialis anterior (58 ± 16%), and gracilis (59 ± 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 ± 3.5 ms), adductors (36.2 ± 1.4 ms), biceps femoris (35.8 ± 2.3 ms), gastrocnemius (35.6 ± 2.3 ms), and semimembranosus (35.5 ± 2.3 ms). The least intensely used muscle was the rectus femoris (30.1 ± 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 = 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 ± 7%) compared with horizontal (67 ± 8%) running. The mean
percentage of muscle volume activated increased significantly
(P Mean lower extremity T2 values were not significantly
(P <0.004) different between
horizontal (34.0 ± 0.9 ms) and uphill (34.2 ± 1.0 ms) running.
Mean T2 increased significantly (P DISCUSSION 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 near-maximum 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, heavy-resistance 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 heavy-resistance 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
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 = 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
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 +1 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 initially exceeded the criterion
that were not counted as active because the T2 had fallen below the criterion during the first 10-12 min of recovery. Thus, whereas the absolute accuracy of the estimates of the percentage of muscle volume activated cannot be know for certain, large error is unlikely, and the comparisons of the relative activation of individual muscles or
muscle groups during horizontal and uphill running should be 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, exercise-induced 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 = 196 ms,
intracellular free water T2 = 40-45 ms, and
intracellular bound water T2 = <16 ms) contribute to the T2 of
skeletal muscle (20, 24), and all probably change with exercise.
However, simple movement of water into the muscle does not fully
explain T2 changes with exercise, because increased muscle
cross-sectional area due to venous occlusion (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 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.
O2 peak; 2.91 ± 0.52 l/min or 48.6 ± 5.2 ml · kg
1 · min1).
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.
O2 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
O2 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
(O2) 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
O2 obtained on the test was
operationally defined as the
O2 peak if there was
a plateau in O2
between the last two stages of the test, as assessed by an increase in
O2 of <2.1
ml · kg1 · min1
(40), or if peak HR was at least 90% of age-predicted
maximum and respiratory exchange ratio was >1.0.
O2 peak)
treadmill running to exhaustion. Mean treadmill time was 2.6 ± 0.5 min and ranged from 2.0 to 3.9 min. 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.
of the signal decay time) was calculated for
each pixel within a region of interest by using the formula T2 = (ta 
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 ± 0.6 and 29.7 ± 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).
0.004) adjusted by
using the Bonferroni technique.
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.
[View Larger Version of this Image (58K GIF file)]
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.
[View Larger Version of this Image (49K GIF file)]
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%).
0.004) from horizontal to uphill running for the vastus group (1.6 ms) and decreased significantly (P 0.004) for the gracilis (4.7 ms), semitendinosus (2.8 ms), and rectus
femoris (2.1 ms).
O2
(O2 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%
O2 max) and 30 s (194%
O2 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 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.
O2 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 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.
ACKNOWLEDGEMENTS
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.
FOOTNOTES
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: Kcureton{at}coe.uga.edu).
Received 23 August 1996; accepted in final form 21 July 1997.
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