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Environmental Physiology and Medicine Directorate and Occupational Health and Performance Directorate, US Army Research Institute of Environmental Medicine, Natick 01760-5007; and Department of Health Sciences, Sargent College of Allied Health Professions, Boston University, Boston, Massachusetts 02215
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Fulco, Charles S., Steven F. Lewis, Peter N. Frykman, Robert
Boushel, Sinclair Smith, Everett A. Harman, Allen Cymerman, and Kent B. Pandolf. Muscle fatigue and exhaustion during dynamic leg exercise
in normoxia and hypobaric hypoxia. J. Appl. Physiol. 81(5): 1891-1900, 1996.
Using an
exercise device that integrates maximal voluntary static contraction
(MVC) of knee extensor muscles with dynamic knee extension, we compared
progressive muscle fatigue, i.e., rate of decline in force-generating
capacity, in normoxia (758 Torr) and hypobaric hypoxia (464 Torr).
Eight healthy men performed exhaustive constant work rate knee
extension (21 ± 3 W, 79 ± 2 and 87 ± 2% of 1-leg knee
extension O2 peak uptake for
normoxia and hypobaria, respectively) from knee angles of
90-150° at a rate of 1 Hz. MVC (90° knee angle) was
performed before dynamic exercise and during 
5-s pauses every 2 min
of dynamic exercise. MVC force was 578 ± 29 N in normoxia and 569 ± 29 N in hypobaria before exercise and fell, at exhaustion, to similar levels (265 ± 10 and 284 ± 20 N for normoxia and
hypobaria, respectively; P > 0.05)
that were higher (P < 0.01) than
peak force of constant work rate knee extension (98 ± 10 N, 18 ± 3% of MVC). Time to exhaustion was 56% shorter for hypobaria
than for normoxia (19 ± 5 vs. 43 ± 7 min, respectively;
P < 0.01), and rate of right leg MVC fall was
nearly twofold greater for hypobaria than for normoxia (mean slope = 
22.3 vs. 11.9 N/min, respectively;
P < 0.05). With increasing duration
of dynamic exercise for normoxia and hypobaria, integrated
electromyographic activity during MVC fell progressively with MVC
force, implying attenuated maximal muscle excitation. Exhaustion, per
se, was postulated to relate more closely to impaired shortening
velocity than to failure of force-generating capacity.
muscle endurance; strength; electromyography; quadriceps femoris
muscles; hypoxia; muscle contraction; oxygen uptake; perceived
exertion; muscle ischemia
INTRODUCTION NUMEROUS MODELS have been used to study human muscle
fatigue, but the mechanisms remain poorly defined. A major limitation of dynamic exercise models involving conventional ergometry such as
treadmill or stationary cycling is difficulty reconciling measurement of fatigue with its broad definition, i.e., a gradual decline of muscle
force-generating capacity resulting from physical activity (6). Because
fatigue defined in this manner is not readily observable in ordinary
dynamic exercise, "an inability to sustain a target work rate"
has become a popular operational definition (13). As a result, the
physiological correlates of fatigue have focused primarily on the
moment a constant work rate can no longer be sustained, i.e., the point
of exhaustion, and it has been impossible to clearly distinguish
fatigue from exhaustion. To circumvent these limitations, we recently
developed a model featuring integration of dynamic knee extension
exercise isolated to the knee extensor muscles with serial measurement
of maximal voluntary static contraction (MVC) force of these muscles
(18). Our approach permits linkage between gradually falling
force-generating capacity of dynamically exercised muscle and specific
physiological, biochemical, and psychological factors under a variety
of dynamic exercise conditions. As an initial step, using this
approach, we compared the rates and myoelectric manifestations of
muscle fatigue and the physiological determinants of exhaustion during
dynamic knee extension exercise under normoxic control conditions with
those under conditions of hypobaric hypoxia. This was accomplished by
measuring force and integrated electromyographic (iEMG) activity during
constant work rate dynamic exercise performed to exhaustion with the
knee extensor muscles of one leg and during knee extensor MVCs
performed at frequent intervals throughout dynamic exercise under each
condition. Dynamic exercise was performed at the same force, velocity,
power output, and energy requirement in normoxia and hypobaric hypoxia. This enabled us to link differences in muscle force-generating capacity
and myoelectric activity between normoxic and hypoxic conditions with
corresponding metabolic differences relating specifically to a
difference in inspired oxygen pressure.
METHODS
3 h
postprandially. Potential impact of diurnal factors on exercise
performance was prevented by conducting each subject's testing at the
same time of day. On days of hypobaric testing, chamber pressure was
reduced by 21 Torr/min immediately after the subject entered the
chamber. After a chamber pressure decline of 294 Torr in 15 min,
subjects rested at a barometric pressure of 464 Torr for 15 additional
min before beginning preexercise MVC measurements. Total time spent
under hypobaric conditions never exceeded 90 min for any subject, and
no symptoms of hypobaric illness were observed.
Device for studying fatigue of dynamic exercise.
The specially designed device for performing one-leg dynamic knee
extension exercise interspersed with maximal static one-leg knee
extension contractions has been described in detail (18). Briefly, it
consists of a platform on which the subject sits, an attached
minimal-friction weight-pulley system with an ankle harness,
transducers for measurement of force and ankle displacement during
dynamic knee extension, and separate force transducers for measurement
of force of static knee extension MVC. To precisely control work rate,
two columns of 14 light crystal diodes (LCDs) are placed vertically in
front of the subject. The right LCD column is wired in series to the
position transducer, such that the number of LCDs lit is proportional
to ankle displacement during knee extension. The left LCD column is
connected to a synthesizer/function generator, which automatically and
sequentially lights from 1 (at the 90° knee angle starting
position) to 14 (corresponding to ankle displacement on reaching
150° of knee extension) to 1 (return to 90° starting position)
at a predetermined knee extension rate of 1 Hz. To maintain correct
distance and rate of dynamic knee extension, the subject continuously
matches the column of LCDs controlled by leg movement with that
controlled by the synthesizer/function generator. The LCD units
simplify subject and investigator monitoring of adherence to the
required work rate. Because the knee extension movement encompasses
60° and there are 13 intervals between LCDs, the maximum allowable
difference between the desired and actual knee extension angle is
4.62°. Muscle exhaustion is defined as a mismatch of only one LCD
between the right and left LCD columns for three consecutive knee
extensions. This effectively means that exhaustion is associated with
an inability to complete the last 5° of knee extension contraction,
from 145 to 150°, at the required contraction rate. Voltages
proportional to force and ankle displacement are continuously recorded.
Work rate (in W) is determined by multiplying mean force developed per
contraction, distance of ankle movement during knee extension from 90 to 150°, and rate of knee extension (1 Hz).
To measure the decline in force-generating capacity and rate of muscle
fatigue, the exercise device allows performance of maximal voluntary
static contractions of the knee extensor muscles during brief (<5-s)
pauses in dynamic knee extension. This procedure involves rapid
disconnection of the ankle harness from the weight-pulley system,
connection to a force transducer dedicated to measurement of MVC force,
actual measurement of MVC force, and reconnection to the weight-pulley
system.
Determination of MVC force.
On each day of definitive testing, the subjects performed three or more
practice knee extensor MVCs with each leg. Each practice MVC was
followed by 1 min of rest. MVC force of the leg used for dynamic
exercise (the active right leg) was then measured immediately before
and at the end of every 2 min during and immediately after dynamic knee
extension. MVC force of the leg resting during dynamic exercise (the
inactive left leg) was measured shortly before dynamic knee extension
of the active right leg and within 2 s after completion of exercise of
the right leg. Each MVC lasted for 2-3 s. A knee angle of 90°
was used.
Graded knee extension exercise to peak work rate.
Peak knee extension work rate was determined in a series of four to
eight 4-min one-leg exercise bouts of graded intensity separated by 4 min of rest. Increments of work rate applied for each bout were
individually determined on the basis of performance during the
preliminary sessions and ranged from 2 to 10 W. Exercise was terminated
at the point of muscular exhaustion, as defined above. Additional
details of peak exercise testing and criteria for defining peak work
rate and oxygen uptake are described elsewhere (18).
Submaximal constant work rate knee extension exercise.
For each subject, one-leg dynamic knee extension at a frequency of 1 Hz
was performed to exhaustion at the same constant work rate (21 ± 3 W) under normoxic and hypobaric conditions. This absolute work rate
corresponded to 62 ± 3 and 79 ± 2% of individual peak one-leg
work rate in normoxia and hypobaria, respectively. The oxygen uptake
during minute 4 of exercise at this
absolute work rate corresponded to 79 ± 2 and 87 ± 2% of peak
one-leg oxygen uptake for normoxia and hypobaria, respectively. The
time course of fatigue was determined from MVC measurements during
pauses of 5 s at the end of every 2 min of exercise and immediately after exercise.
Electromyographic measurements.
Surface electromyogram (EMG) recordings from electrodes placed
cutaneously over the bellies of three of the quadriceps femoris muscles
(vastus lateralis, vastus medialis, and rectus femoris) and one of the
hamstrings (biceps femoris) were acquired during dynamic knee extension
and maximal voluntary static knee extension. To minimize day-to-day
variation in electrode placement, electrode sites were marked daily
with indelible ink. EMG signals were collected for 12 s every 2 min of
dynamic knee extension. Each specific recording period encompassed
2-4 s of dynamic knee extension before MVC, 3-5 s of static
knee extension for measurement of MVC, and 2-4 s of dynamic knee
extension after each MVC. The portion of each collection period used
for analysis of EMG involved a total of 3 s: 1 s each for a
complete dynamic knee extension/relaxation before and after MVC and 1 s
during the force plateau of the MVC. All recordings of EMG and force
and position transducer signals were collected simultaneously every 2 min at a rate of 1 kHz with use of an Ariel Performance Analysis System
(APAS, Ariel Life Systems, San Diego, CA). The bandwidth used for
collection of all EMG signals was 0-500 Hz. The EMG signals were
preamplified at the leg to minimize the noise-to-signal ratio and
stored on analog tape for subsequent computer processing and analysis.
For each analysis of EMG during submaximal exercise and MVC, the raw EMG signals were integrated. For each subject and each 2-min segment of
exercise, iEMG activity for the three quadriceps femoris muscles was
averaged to provide a composite value for quadriceps iEMG activity
during MVC and dynamic knee extension, respectively. Composite
quadriceps iEMG activity during MVC of dynamically exercised muscle and
during dynamic knee extension contractions, per se, was expressed as a
percentage of composite iEMG activity during MVC of rested unfatigued
muscle and used in statistical analysis. Comparisons of changes in iEMG
activity during dynamic knee extension as a function of exercise
duration were made with respect to iEMG activity for the first
contraction of constant work rate exercise.
Other measurements.
Respiratory gas exchange, including minute ventilation, oxygen uptake,
carbon dioxide production, and respiratory exchange ratio, was
monitored during consecutive 20-s periods at rest and throughout each
exercise session with use of a metabolic measurement cart (model 2900, Sensormedics, Anaheim, CA). Before each test, the metabolic cart was
calibrated with certified gases. Heart rate was determined from
continuous electrocardiographic recordings at rest and during exercise.
Continuous measurement of the arterial oxygen saturation of fingertip
blood was performed noninvasively using a Sensormedics finger oximeter.
Every 2 min during dynamic exercise, subjects rated their perceived
exertion localized to the active muscles using the 6- to 20-category
rating scale developed by Borg (7).
Data analysis.
Paired t-tests were used to detect
differences between normoxia and hypobaric hypoxia in peak dynamic
exercise responses and duration of submaximal knee extension exercise
to exhaustion (i.e., endurance time) and differences between MVC force
before and after exhaustive dynamic knee extension for the active and
inactive legs under each condition. For each subject under each
condition, standard least-squares regression analysis was performed on
1) the decline in MVC force (in N)
relative to duration (in min) of constant work rate exercise,
2) the decline in percentage of MVC
force relative to increasing percentage of endurance time, and
3) the decline in percentage of
maximal iEMG activity during MVC relative to increasing percentage of
endurance time. Paired t-tests were
then used to compare the mean slopes and intercepts of the respective
regression lines for normoxia vs. hypobaric hypoxia. For constant work
rate exercise, data for oxygen uptake, pulmonary ventilation, arterial
oxygen saturation, ratings of perceived exertion (RPE), composite iEMG
activity, and MVC of dynamically exercised muscle were subjected to
two-way analyses of variance (ANOVA) with repeated measures on two
factors: 1) experimental conditions,
i.e., normoxia vs. hypobaric hypoxia, and
2) exercise duration. If a
significant F value was identified, Tukey's multiple comparison procedure was used to assess the
significance of specific differences in mean values with respect to
experimental conditions or exercise duration. For all analyses, a
difference was accepted as significant if
P < 0.05. Data are presented as means ± SE.
RESULTS
1.0. Arterial oxygen saturation during peak exercise
was 96 ± 1 and 84 ± 6% for normoxia and hypobaria,
respectively (P < 0.05). Peak values were 35 ± 2 and 35 ± 2 l/min for pulmonary minute ventilation and 116 ± 5 and 124 ± 7 beats/min for heart rate under normoxic and hypobaric conditions, respectively
(P > 0.05 for both).
Muscle endurance, fatigue, and exhaustion.
Throughout constant work rate knee extension, peak force of dynamic
contraction was 18 ± 3% of MVC of rested muscle under each
condition. Mean time to exhaustion was 42.8 ± 7.1 min in normoxia
and 19.1 ± 5.0 min in hypobaria (P < 0.001; Fig. 1). For each subject, MVC
force declined linearly for normoxia and hypobaria. Representative data
are shown in Fig. 2. The mean slope of
decline in MVC force with respect to exercise duration was nearly
twofold greater for hypobaria (22.3 ± 3.9 N/min) than for
normoxia (11.9 ± 3.9 N/min,
P < 0.05). There was no difference in intercept.
;
n = 8 subjects) endurance times to
exhaustion during constant work rate knee extension exercise for
normoxia and hypobaria. * Shorter
(P < 0.05) mean time to exhaustion
for hypobaria than for normoxia. Note much greater range of times to
exhaustion for normoxia (15.5-68.0 min) than for hypobaria
(10.0-26.5 min).
) and hypobaria (
). Regression lines are as follows: for normoxia (solid line), MVC (in N) = 23.2x + 694, r = 0.99; for hypobaria (dashed line),
MVC (in N) = 47.5x + 654, r = 0.98.
The shortest endurance time for individual subjects in hypobaria was 10 min (Fig. 1). Paired comparisons between normoxia and hypobaria for a given duration beyond the first 10 min of exercise but before exhaustion would involve a smaller number of observations and more limited statistical power. We therefore restricted some paired comparisons to the first 10 min of exercise plus the point of exhaustion. The decline from resting level in knee extensor MVC force became statistically significant (P < 0.05) by minute 4 of exercise in hypobaria but not until minute 8 of exercise in normoxia (Fig. 3). The difference in muscle force-generating capacity between normoxia and hypobaria became statistically significant (P < 0.05) at minute 4 of submaximal dynamic knee extension when MVC was 510 ± 29 and 422 ± 29 N for normoxia and hypobaria, respectively. At the point of exhaustion for normoxia, MVC force of the knee extensor muscles of the active leg reached a similar (P > 0.05) level for constant work rate exercise (265 ± 10 N, 47 ± 3% of MVC of rested muscle) and graded work rate exercise (255 ± 29 N, 46 ± 7% of MVC of rested muscle). At the point of exhaustion for hypobaria, MVC force of the knee extensor muscles of the active leg also was similar (P > 0.05) for constant work rate exercise (284 ± 20 N, 49 ± 3% of MVC of rested muscle) and graded work rate exercise (275 ± 10 N, 48 ± 4% of MVC of rested muscle). In addition, at the point of exhaustion for constant work rate exercise, MVC force of the knee extensor muscles of the active leg and the percentage of MVC of dynamically exercised muscle represented by the peak force achieved in dynamic contraction, per se, were each similar (265 ± 10 and 284 ± 20 N and 39 ± 4 and 37 ± 5%; both P > 0.05) for normoxia and hypobaria, respectively.
) and hypobaria ().
* Significant (P < 0.05)
difference between normoxia and hypobaria.
a P < 0.05 from rest (minute 0);
b P < 0.05 from minute 2;
c P < 0.05 from minute 4;
d P < 0.05 from all previous values.
Myoelectric measurements during constant work rate exercise. Mean composite iEMG activity of the vastus lateralis, vastus medialis, and rectus femoris muscles during MVC of rested muscle was similar: 2.7 ± 0.2 and 3.3 ± 0.6 mV · s (P > 0.05) for normoxia and hypobaria, respectively. Mean quadriceps iEMG activity during MVC fell significantly (P < 0.05) over the first 10 min of dynamic knee extension exercise in normoxia and hypobaria (Fig. 4A). The fall in quadriceps iEMG activity during MVC over the first 10 min of dynamic knee extension was greater for hypobaria than for normoxia (P < 0.05). The difference between iEMG activity during MVC of dynamically exercised muscle and that during MVC of rested muscle became statistically significant by 4 min of exercise in hypobaria and by 10 min of exercise in normoxia. The difference in iEMG activity during MVC of exercised muscle for normoxia and hypobaria became statistically significant (P < 0.05) after 4 min of dynamic knee extension.
) vs. hypobaria (
) for MVC
(A) and dynamic exercise
(B). * Significant difference
(P < 0.05) between normoxia and
hypobaria.
a P < 0.05 from start value;
b P < 0.05 from minute 2;
c P < 0.05 from minute 4;
d P < 0.05 from all previous values.
Quadriceps iEMG activity during the first dynamic knee extension was 36 ± 4% of that for MVC of rested muscle in normoxia vs. 40 ± 5% of that for MVC of rested muscle in hypobaria (P > 0.05; Fig. 4B). Over the first 10 min of exercise, quadriceps iEMG activity during dynamic contractions rose to 51 ± 6 and 69 ± 6% of that for MVC of rested muscle in normoxia and hypobaria, respectively (P < 0.05 for both increases). The rise in quadriceps iEMG activity during dynamic contractions was greater for hypobaria than for normoxia (P < 0.05). By minute 4 of exercise, quadriceps iEMG activity during dynamic contractions was 77 ± 9 and 48 ± 5% of that during MVC of dynamically exercised muscle for hypobaria and normoxia, respectively (P < 0.05; Fig. 5). The difference between hypobaria and normoxia for iEMG activity during dynamic contractions persisted through minute 10 of exercise. However, at the point of exhaustion, iEMG activity during dynamic contractions was 129 ± 16 and 114 ± 10% of that during MVC of dynamically exercised muscle, i.e., similar (P > 0.05), in hypobaria and normoxia, respectively.
) and hypobaria ().
* Significantly different (P < 0.05) from normoxia.
a P < 0.05 from start value;
b P < 0.05 from minute 2;
c P < 0.05 from minute 4;
d P < 0.05 from minute 6;
e P < 0.05 from minute 8;
f P
<0.05 from all previous values.
Under each condition, iEMG activity during MVC and MVC force declined by nearly the same relative amount with respect to percentage of endurance time (Fig. 6). For normoxia, the ratio of percentage of maximal iEMG activity during MVC to percentage of MVC force remained constant at ~1.0 throughout dynamic knee extension. For hypobaria, there was a similar relationship. At the point of exhaustion under each condition, the ratio of iEMG activity to MVC force was approximately the same as that for unfatigued muscle.
) and iEMG activity () during
knee extensor MVC relative to duration of constant work rate knee
extension expressed as a percentage of endurance time in normoxia
(A) and hypobaria (B). Force and iEMG activity
are expressed as percentages of maximal values observed during MVC of
rested muscle. Lines show average (n = 8) declines in MVC force and iEMG derived from average slope of
individual regression equations relating percent changes in MVC force
and maximal iEMG activity to percentage of endurance time.
iEMG activity of the major antagonist to the knee extensor muscles, i.e., the biceps femoris, did not increase (P > 0.05) during dynamic knee extension. Oxygen uptake during constant work rate exercise. For normoxia and hypobaria, similar (P > 0.05) approximately steady-state values for oxygen uptake were achieved between minutes 2 and 4 of dynamic exercise (Fig. 7A). Oxygen uptake during the transition from rest to steady state also was similar (P > 0.05) for normoxia and hypobaria. At minute 10 of constant work rate exercise and at exhaustion, oxygen uptake was higher (P < 0.05) for hypobaria than for normoxia. For each condition, oxygen uptake was higher at exhaustion than at minute 10 of exercise (P < 0.05).
) and hypobaria ().
* Significant difference (P < 0.05) between normoxia and hypobaria.
a P < 0.05 from previous values;
b P < 0.05 from rest;
c P < 0.05 from minute 2;
d P < 0.05 from minute 4.
Ventilation during constant work rate exercise. For normoxia, pulmonary minute ventilation reached an approximate steady state between minutes 4 and 6 of dynamic exercise (Fig. 7B). At exhaustion, ventilation was slightly higher (P < 0.05) than after 4 min of exercise. For hypobaria, ventilation rose gradually throughout dynamic exercise. At minute 4 of knee extension, ventilation initially became higher for hypobaria than for normoxia. This difference persisted until exhaustion. Arterial oxygen saturation during constant work rate exercise. For normoxia, arterial oxygen saturation was 96 ± 1% at rest and remained about the same over the duration of dynamic exercise (Fig. 7C). For hypobaria, arterial oxygen saturation was 78 ± 1% at rest (P < 0.05 vs. normoxia), rose to 83 ± 1% at minute 6 (P < 0.05) of exercise, and then remained at ~84% until exhaustion. The rise in arterial oxygen saturation from the resting level in hypobaria became statistically significant after minute 4 of dynamic exercise. Perceived exertion during constant work rate exercise. Under both conditions, local RPE increased progressively with exercise duration (Figure 7D). Local RPE tended to increase more in relation to exercise duration for hypobaria than for normoxia. By minute 8 of exercise, local RPE was higher (P < 0.05) for hypobaria than for normoxia.
DISCUSSION
4 from active muscle.
Metaboreceptor afferent discharge has been implicated in a reflex from
fatigued muscle that leads to diminished muscle excitation (4, 19), and, in general, muscle contraction under ischemic or hypoxic conditions is linked with increased release of these metabolites and
increased activation of the metaboreceptor afferents (25, 29, 32). Our
study design did not include specific tests for involvement of
metaboreceptor afferent mechanisms, but the exercise conditions are
likely to have included ischemia in addition to hypobaria. Peak force
of constant work rate knee extension averaged 18 ± 3% of MVC and,
in five of the eight subjects, was 20% of MVC. Intramuscular
pressure measurements imply partial occlusion of arterial inflow to
human quadriceps during static knee extension at tensions equivalent to
20% of MVC (14, 33). However, muscle microcirculation and, hence,
oxygen delivery may be compromised at tensions <15% of MVC (33). On
the average, for our subjects, peak force of dynamic knee extension was
15% of MVC for ~13% of the entire work period. Additional
experiments are necessary to determine whether the extent of muscle
ischemia likely associated with this level of force or the addition of
hypobaric hypoxia contributes importantly to possible afferent
mechanisms affecting parallel progression of muscle fatigue and
diminished muscle excitation in this exercise model.
ACKNOWLEDGEMENTS
The authors thank James Devine (Altitude Chamber) for thoughtfulness, patience, and unlimited cooperation during the many design changes of the knee extension device; Paul B. Rock for insightful reading of the manuscript; and Julio Gonzalez for expertise in some of the drawings.
FOOTNOTES
Address for reprint requests: C. S. Fulco, Altitude Physiology and Medicine Div., USARIEM, Kansas St., Natick, MA 01760-5007.
Received 23 October 1995; accepted in final form 16 April 1996.
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