Download Age-related enhancement of fatigue resistance is evident in men

J Appl Physiol 97: 967–975, 2004.
First published May 14, 2004; 10.1152/japplphysiol.01351.2003.
Age-related enhancement of fatigue resistance is evident
in men during both isometric and dynamic tasks
Ian R. Lanza, David W. Russ, and Jane A. Kent-Braun
Department of Exercise Science, University of Massachusetts, Amherst, Massachusetts 01003
Submitted 16 December 2003; accepted in final form 11 May 2004
ankle dorsiflexors; compound muscle action potential; contractile
properties; central activation
to the human neuromuscular system are the generation of force or power and the
maintenance of force or power during sustained activity. In
older adults, reduced force generation, or muscle weakness,
occurs largely due to a loss of muscle mass (18, 35). It is
generally accepted that this sarcopenia is likely to develop in
most muscle groups after the sixth decade of life (35). In
contrast, there is far less consensus as to the effect of old age
on the ability to maintain force or power during activity and
thereby to avoid fatigue (3). The results of some investigations
suggest that older men and women fatigue more than young
(12, 13, 34), which is consistent with studies in animal models
(14). Other investigators, however, have demonstrated similar
fatigability in young and old subjects (2, 33, 36), whereas still
TWO MAJOR FUNCTIONAL CHALLENGES
Address for reprint requests and other correspondence: J. A. Kent-Braun,
Dept. of Exercise Science, Totman Bldg. 108, University of Massachusetts,
Amherst, MA 01003 (E-mail: [email protected]).
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others have observed that older adults fatigue less than young
(6, 17, 29). In these studies, fatigue is often quantified as a
decrease in maximal force-generating capacity in response to
exercise, although endurance time at a given force output is
also used as a measure of fatigue.
Even less clear than the effect of old age on the magnitude
of fatigue is its effect on the potential mechanisms that contribute to fatigue. Human aging is accompanied by a number of
changes in the neuromuscular system that might affect fatigue,
including motor unit remodeling (11), reduced maximal motor
unit discharge rates (25), and a general shift toward a greater
type I fiber composition (22). The extent of these age-related
alterations appears to vary by muscle group and level of
habitual physical activity (3, 21, 30). The impact of these
various alterations may depend on the motor task used to
evaluate fatigue (8). From a functional standpoint, maintaining
successful independent living with increasing age requires the
repeated use of both isometric and dynamic contractions, yet
few data are available that provide a reasonably direct comparison of fatigue during these two types of contraction in older
adults.
The purpose of the present study was to investigate the
impact of old age on one aspect of the task specificity of
muscle fatigue in humans. The particular design of this study
allowed us to examine the effects of contraction type (isometric
vs. dynamic) on fatigue while keeping muscle group and
subject characteristics consistent. We hypothesized that older
adults would fatigue less than young during intermittent maximal isometric contractions, consistent with existing data demonstrating enhanced fatigue resistance with age during intermittent maximal (6, 17) and submaximal isometric exercise
(29). In this latter study, older subjects also demonstrated less
intracellular acidosis and accumulation of Pi, which was suggested as a mechanism for their lesser fatigue (29). We further
hypothesized that older adults would fatigue more than young
during intermittent, maximal dynamic contractions, due to
greater central activation failure and impaired power production in the older subjects. Empirical support for this latter
hypothesis is derived from our laboratory’s previous results
suggesting that age-related impairments in dynamic tasks may
exceed those of isometric tasks (27, 31), whereas theoretical
support is provided by the potential impact of age-related
alterations in central motor function (25) during tasks of
greater neural complexity such as maximal dynamic contractions. Finally, one recent study showed greater central activation failure in the unfatigued muscles of older compared with
young subjects that worsened with fatigue, suggesting an
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967
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Lanza, Ian R., David W. Russ, and Jane A. Kent-Braun.
Age-related enhancement of fatigue resistance is evident in men
during both isometric and dynamic tasks. J Appl Physiol 97: 967–975,
2004. First published May 14, 2004; 10.1152/japplphysiol.01351.
2003.—It has been suggested that the effects of old age on the ability
to resist fatigue may be task dependent. To test one aspect of this
hypothesis, we compared the neuromuscular responses of nine young
(26 ⫾ 4 yr, mean ⫾ SD) and nine older (72 ⫾ 4 yr) healthy, relatively
sedentary men to intermittent isometric (3 min, 5 s contract/5 s rest)
and dynamic (90 at 90°/s) maximum voluntary contractions (MVC) of
the ankle dorsiflexor muscles. To assess the mechanisms of fatigue
(defined as the ratio of postexercise MVC to preexercise MVC), we
also measured isometric central activation ratios (CAR), tetanic
torque, contractile properties, and compound muscle action potentials
before and immediately after exercise. Because dynamic contractions
are more neurally complex and metabolically demanding than isometric contractions, we expected an age-related fatigue resistance observed during isometric exercise to be absent during dynamic exercise. In contrast, older men (O) fatigued less than young (Y) during
both isometric (O ⫽ 0.77 ⫾ 0.07, Y ⫽ 0.66 ⫾ 0.02, mean ⫾ SE; P ⬍
0.01) and dynamic (O ⫽ 0.45 ⫾ 0.07, Y ⫽ 0.27 ⫾ 0.02; P ⫽ 0.04)
contractions (ratio of postexercise to preexercise MVC), with no
evidence of peripheral activation failure in either group. We observed
no obvious limitations in central activation in either group, as assessed
using isometric CAR methods, after both isometric and dynamic
contractions. Preexercise half-time of tetanic torque relaxation, which
was longer in O compared with Y, was linearly associated with fatigue
resistance during both protocols (r ⫽ 0.62 and 0.66, P ⱕ 0.004, n ⫽
18). These results suggest that relative fatigue resistance is enhanced
in older adults during both isometric and isokinetic contractions and
that age-related changes in fatigue may be due largely to differences
within the muscle itself.
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MUSCLE FATIGUE IN AGING
increased susceptibility of older adults to impaired voluntary
activation (43).
In the present study, we compared fatigue in young and
older men during two intermittent maximal voluntary contraction (MVC) protocols; one using isometric contractions
(MVIC) and the other using dynamic contractions (MVDC).
We recruited and studied young and older adults of similar
physical activity levels to minimize the potentially confounding effect of habitual physical activity on muscle function.
Potential mechanisms of fatigue were examined by measuring
central and peripheral activation and muscle contractile properties, each of which may be altered by the aging process (12,
15, 43). The ankle dorsiflexor muscles were chosen for study
because their function is highly relevant to locomotion and the
prevention of falls in the elderly (32).
METHODS
Nine young (26 ⫾ 4 yr) and nine older (72 ⫾ 4 yr) men were
recruited from the University community and area Councils on Aging.
In response to recent studies demonstrating an effect of sex on muscle
fatigue (10, 42), we included only men in this study. All subjects
provided informed consent in accordance with the procedures approved by the Human Subjects Review Board at the University of
Massachusetts, Amherst. All subjects were in good health, free from
disease or medication that might affect our measurements, and right
leg dominant. Each subject’s ankle and brachial artery blood pressures
were measured to confirm the absence of latent peripheral vascular
disease in the study leg (38).
Volunteers were enrolled in the study only if they had exercised
⬍20 min/day twice per week in the previous 2 mo. To quantify
physical activity patterns, each subject wore a three-dimensional
accelerometer (Tritrac Professional Products, www.stayhealthy.com)
for 7 days. Accelerations were recorded in all three dimensions, and
the vector magnitude was averaged over the 7-day period to obtain a
daily average, as previously reported (28).
Experimental Setup
Subjects performed isometric and dynamic contractions of the left
leg using a Biodex System 3 dynamometer (Biodex Medical, Shirley,
NY). The subjects were positioned with ⬃120° of hip extension (full
hip extension ⫽ 180°) and ⬃150° of knee extension (full knee
extension ⫽ 180°). Straps mounted on the seat were tightened across
the hips and thigh to prevent extraneous movement by the subjects.
The leg was positioned such that the axis of rotation of the ankle joint
was aligned with that of the dynamometer. The left foot was stabilized
with a thermoplastic mold and secured to the footplate by using
inelastic straps across the metatarsal-phalangeal joints. The dynamometer’s internal goniometer was calibrated by using a manual
goniometer. Thereafter, all joint angle measurements were obtained
from the dynamometer. The analog signals corresponding to torque,
velocity, and joint angle were acquired and digitized by using customized Labview software (National Instruments, Austin, TX).
Surface electromyography (EMG) and electrical stimulation were
applied as described elsewhere (26), and they were used to assess
central activation, peripheral excitability, and the contractile properties of the ankle dorsiflexor muscles. All stimulating and surface EMG
electrodes were 10-mm-diameter gold-plated disks. All stimulation
pulses (200 ␮s) were delivered with a constant current stimulator
(model DS7A, Digitimer, Hertfordshire, UK) at supramaximal intensity (115% of the intensity that produced a maximum-amplitude
compound muscle action potential).
J Appl Physiol • VOL
For the isometric protocol, we assessed voluntary activation of the
ankle dorsiflexors by superimposing a train of supramaximal stimuli
(50 Hz, 750 ms) on a MVIC. The resultant torque response was
sampled at 500 Hz. The central activation ratio (CAR) was calculated
as the peak MVIC divided by the peak total torque, where total torque
was the sum of the MVIC and the superimposed tetanus (26). A CAR
⬍1.0 indicates incomplete voluntary activation. The CAR measure
was made before, at the end of, and during recovery from the
isometric exercise. As a second measure of central activation, we
compared the fall of MVIC with the fall of tetanic isometric torque, as
described by Bigland-Ritchie and colleagues (7). Tetanic torque was
obtained by stimulating (50 Hz, 750 ms) the relaxed muscle under
isometric conditions. The CAR and tetanic torque measures were
recorded during the final MVIC and immediately after the final
MVIC, respectively.
Assessment of central activation during dynamic contractions is
difficult for a variety of reasons (see DISCUSSION). For the dynamic
fatigue protocol, we chose to address this issue by estimating central
activation using the isometric CAR technique, with the understanding
that this measure may not wholly reflect changes in central drive
during dynamic contractions. The CAR was obtained before and
immediately after exercise (⬍5 s after last dynamic contraction) and
at intervals throughout the recovery period.
Peripheral Excitability
The compound muscle action potential (CMAP) was used to assess
the excitability of the neuromuscular junction and sarcolemma before,
immediately after, and throughout 10 min of recovery from exercise.
The CMAP was obtained by delivering a single supramaximal stimulus of 0.2-ms duration and sampling the resultant EMG signal at
2,500 Hz. Changes in the peak-to-peak amplitude and duration of the
CMAP served as indicators of changes in the excitability and propagation velocity of the neuromuscular junction and/or muscle membrane (26).
Contractile Properties
The maximal rate of torque development (RTD) and the half-time
(t1/2) of torque relaxation were determined from the electrically
stimulated, isometric tetanic torque, as described previously (29).
These measurements were performed before and immediately postexercise and at 5 and 10 min of recovery. The RTD provides an index
of the muscle’s in vivo contractile speed and the t1/2 is an indirect
indicator of several processes of torque relaxation, including calcium
handling by the sarcoplasmic reticulum and/or dissociation of calcium
from troponin (1, 9).
Habituation Sessions
Each subject reported to the laboratory for habituation on two
occasions before the fatigue sessions. Subjects performed repeated
maximal isometric and dynamic voluntary contractions until subsequent efforts were within 10% of the previous effort. Measures of
central and peripheral activation and contractile properties were also
obtained. After completion of the habituation sessions, the subjects
returned to the laboratory on two additional days to perform the
fatigue protocols. A minimum of 48 h elapsed between visits.
Experimental Sessions
This study was designed to compare muscle fatigue across age
groups during isometric and concentric dorsiflexor muscle contractions. The exercise protocols were made to be as similar as possible,
with the exception of the contraction mode. After completing two
habituation sessions, subjects participated in two experimental sessions consisting of either the isometric or the dynamic fatigue test.
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Subjects
Central Activation
MUSCLE FATIGUE IN AGING
Statistics
Subject characteristics (height, mass, physical activity) were compared across age groups by using unpaired t-tests. To assess reliability
of baseline measures across the two testing sessions, repeated-measures ANOVA was used to determine whether preexercise measures
of MVIC, MVDC, and tetanic torque were similar across sessions
(days), and intraclass correlation coefficients (ICC) were calculated
for each of these measures.
Within each testing session, a mixed-model two-factor (age, time)
repeated-measures ANOVA was used to assess changes in MVIC,
J Appl Physiol • VOL
MVDC, CAR, CMAP amplitude, CMAP duration, RTD, and t1/2 of
tetanic torque relaxation during exercise. Where age ⫻ time interactions were found, post hoc comparisons were performed by using the
Tukey-Kramer adjustment for multiple pairwise comparisons. A separate mixed-model repeated-measures ANOVA was used to assess
recovery of these variables. For each protocol, we assessed the
completeness of recovery within each age group by comparing the
MVC after 10 min of recovery with the preexercise MVC by using
AVOVA. As a secondary measure of central activation for the
isometric protocol only, the fall of MVIC was compared with the fall
of tetanic torque by using ANOVA. To compare the relative fatigue
induced by the two protocols, two-factor (age, condition) ANOVA
was used to compare the fall in isometric tetanic force after the
isometric protocol with the fall in isometric tetanic torque after the
dynamic protocol in both age groups.
For each protocol, associations between fatigue and both strength
(MVIC, MVDC) and contractile properties were determined by using
linear regression analysis for all subjects combined. Descriptive data
are presented as means ⫾ SD; all other data are means ⫾ SE.
RESULTS
Subjects
The average ages of the young and older groups were 26 ⫾
4 and 72 ⫾ 4 yr, respectively. The young subjects were taller
than the older subjects (181 ⫾ 5 vs. 172 ⫾ 4 cm; P ⬍ 0.001).
There were no differences between groups in body mass
(young ⫽ 72 ⫾ 8, older ⫽ 75 ⫾ 6 kg; P ⫽ 0.38) or physical
activity level (young ⫽ 152 ⫾ 35, older ⫽ 159 ⫾ 59 arbitrary
units; P ⫽ 0.77).
Torque, Power, and Fatigue
There were no differences in preexercise measures of
MVIC, MVDC or tetanic torque across test days (ANOVA,
P ⫽ 0.50 – 0.82 for the three variables; ICC r ⫽ 0.80 – 0.99).
Before the isometric protocol, the older subjects produced
⬃14% less MVIC torque than the young, although this was not
a statistically significant difference (Table 1). Before the dynamic protocol, the older men produced 25% less preexercise
MVDC power compared with the young (P ⫽ 0.002; Table 2).
Preexercise peak tetanic torque was 25.5% lower in older
subjects at the isometric fatigue session (P ⫽ 0.03) and 17.3%
lower at the dynamic fatigue session (P ⫽ 0.14; Tables 1
and 2).
Both young and older subjects had significant reductions in
MVIC and tetanic torque after the isometric fatigue protocol
(Table 1, Fig. 1A). The young group showed a greater decline
in MVIC (P ⫽ 0.005) and tetanic torque (P ⫽ 0.006) than the
older group (Fig. 1A, Table 1). During the 10-min recovery
period, there was a main effect of age such that older men had
relatively higher MVICs compared with young men (P ⬍
0.001), presumably due to the difference in MVIC at fatigue
(Fig. 1A). After 10 min of recovery, MVIC torque had returned
to preexercise levels in the older men but not in the young men.
However, there were no group ⫻ time interactions in the
recovery of MVIC or tetanic torque, suggesting a similar
overall pattern of torque recovery in the two groups and that
age group differences in recovery were due to the differences
present at the end of the exercise. Fatigue during the isometric
protocol was only modestly associated with preexercise MVIC
(r ⫽ 0.46, P ⫽ 0.06).
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Each fatigue test was separated by at least 48 h, and the order of
testing was randomized. We measured voluntary torque, electrically
stimulated torque, central and peripheral activation, and contractile
properties before and 0, 2, 5, and 10 min after each fatigue protocol.
Preexercise measurements. Before both the isometric and dynamic
fatigue tests, supramaximal stimulus intensity was determined, and
preexercise measurements of CMAP, MVIC, CAR, MVDC, and
contractile properties were taken, in that order. Three CMAPs were
recorded with 1 min of rest between successive measurements. Preexercise isometric strength was then determined by having subjects
perform two to three MVICs (⬃5-s duration), with 2 min of rest
between contractions. Subjects repeated this measure until the difference in peak torque from successive MVICs was 10% (typically 2–3
contractions). The highest value during these contractions was recorded as subject’s preexercise MVIC. Three MVDCs at 90°/s were
then performed, and the highest peak power was recorded as the
subject’s preexercise MVDC. After 2 min of rest, CAR was determined. After a further 2 min of rest, tetanic torque (50 Hz, 750 ms)
and contractile properties were assessed. With the exception of the
MVDC measurement, all preexercise measures were performed under
isometric conditions.
Isometric fatigue protocol. After the preexercise measurements
were completed, subjects performed 3 min of intermittent (5 s contract/5 s relax) MVICs. Subjects were encouraged verbally and received visual torque feedback from a computer monitor. All isometric
contractions were performed with the ankle plantar flexed to 30° from
neutral, which has been shown to be the optimal angle for torque
production in the dorsiflexors of young (37) and older (44) subjects.
Fatigue was defined as the decline in peak isometric torque, expressed
as the ratio of the peak torque produced during the last contraction to
the peak torque produced during the preexercise MVIC. Central
activation was measured during the final MVIC of the fatigue task;
peripheral excitability and contractile function were measured immediately after exercise and at 2, 5, and 10 min of recovery. All recovery
measures were performed under isometric conditions.
Dynamic fatigue protocol. On a separate day and again after
completion of the preexercise measures, each subject performed 90
MVDCs at a nominal angular velocity of 90°/s (1.57 rad/s). This
velocity was chosen on the basis of our recent work that showed an
inability of some older subjects to successfully attain target velocities
above 120°/s in an unfatigued state (31). The range of motion (ROM)
about the ankle was mechanically limited to a total of 30° (15° on
either side of the midpoint of the ROM for each subject), a range
previously determined to be manageable for all older subjects (31).
Torque, velocity, and angle data were acquired and digitized at 100
Hz. Peak muscle power (watts) was recorded as the product of peak
torque (N 䡠 m) and angular velocity (rad/s), as described previously
(31). Dynamic fatigue was defined as the fall in peak power production and expressed as the ratio of the average peak power of the last
three contractions to the average peak power of the first three contractions. Because there were approximately three times as many
dynamic contractions as isometric contractions, taking an average of
three dynamic contractions most closely approximates the time frame
of the isometric contractions. End-exercise and recovery measures
were performed as described for the isometric fatigue protocol.
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MUSCLE FATIGUE IN AGING
Table 1. Isometric exercise
Change in Each Group
Postexercise
Preexercise
Young
Older
P (age)
Young
Older
Young
Older
P value
(age ⫻ time)
46.0⫾2.8
34.9⫾2.7
39.5⫾2.7
26.0⫾2.5
0.11
0.03
30.5⫾6.2*
25.7⫾2.5*
30.2⫾5.3*
20.8⫾1.8*
0.66⫾0.02
0.73⫾0.03
0.77⫾0.09
0.80⫾0.03
0.005
0.006
1.00⫾0.00
9.9⫾0.65
16.8⫾1.0
1.00⫾0.00
8.0⫾0.60
16.4⫾17.7
1.0
0.05
0.75
1.00⫾0.00
9.3⫾0.64
19.1⫾0.9*
1.00⫾0.00
7.8⫾0.63
17.7⫾1.0*
0.00
0.96⫾0.04
1.14⫾0.05
0.00
0.98⫾0.03
1.08⫾0.03
1.0
0.71
0.31
0.24⫾0.2
359.0⫾19.3
0.95
0.02
0.24⫾0.01
397.6⫾10.4*
0.27⫾0.01*
424.2⫾31.0
0.00⫾0.00
1.36⫾0.04
0.03⫾0.01
1.21⫾0.12
0.02
0.28
Measure
Torque
MVIC, N䡠m
Tetanic torque, N䡠m
Activation
CAR
CMAP amplitude, mV
CMAP duration, ms
Contractile properties
RTD, %peak torque/ms
t1/2 torque relaxation, ms
0.24⫾0.1
293.0⫾3.5
After the dynamic fatigue task, both young and older subjects showed significant reductions in peak voluntary power
(MVDC) and isometric tetanic torque (Table 2, Fig. 1B).
Similar to the isometric fatigue task, young subjects demonstrated greater MVDC fatigue than older subjects during this
protocol (P ⫽ 0.007); this age-related difference did not reach
significance for tetanic fatigue (P ⫽ 0.09; Table 2). During the
10-min recovery period, MVDC was relatively higher in older
men compared with young (main effect P ⬍ 0.001), again
likely due to the age-group differences in MVDC established at
the end of the exercise protocol (Fig. 1B). There were no
group ⫻ time interactions in recovery of MVDC or isometric
tetanic torque; recovery of MVDC was again incomplete in the
young but not older men. Fatigue during the dynamic protocol
was not strongly associated with either preexercise strength
(MVIC: r ⫽ 0.35, P ⫽ 0.16) or power (MVDC: r ⫽ 0.45, P ⫽
0.08).
Central Activation
Before both testing sessions, all subjects in both age groups
were able to maximally activate their ankle dorsiflexor muscles
during an MVIC, as reflected by the CAR measure (Tables 1
and 2). Immediately after the isometric fatigue protocol, there
was no change in CAR in either age group (Table 1), nor was
there a significant difference in the decline of MVIC compared
with electrically stimulated tetanic torque (P ⫽ 0.08). Similarly, there was no change in either group in the isometric CAR
immediately after the dynamic fatigue task (Table 2).
Peripheral Activation
The CMAP amplitude was greater in young compared with
older adults before isometric (P ⫽ 0.05; Table 1) but not
dynamic exercise (P ⫽ 0.09; Table 2) exercise. The CMAP
duration was similar between young and older groups before
Table 2. Dynamic exercise
Change in Each Group
Postexercise
Preexercise
Measure
Power and torque
MVDC, W
Tetanic torque, N䡠m
Activation
CAR
CMAP amplitude, mV
CMAP duration, ms
Contractile properties
RTD, %peak torque/ms
t1/2 torque relaxation, ms
Young
Older
P value
(age ⫻ time)
Young
Older
P (age)
Young
Older
37.1⫾2.0
34.1⫾3.0
27.8⫾2.0
28.2⫾2.3
0.002
0.14
10.4⫾2.5*
19.6⫾1.8*
12.2⫾6.6*
17.2⫾2.1*
0.27⫾0.02
0.58⫾0.01
0.45⫾0.07
0.60⫾0.04
0.007
0.09
0.99⫾0.01
10.1⫾0.6
16.2⫾0.9
1.00⫾0.00
8.5⫾0.7
15.3⫾0.7
0.47
0.09
0.55
0.99⫾0.01
10.0⫾0.6
19.8⫾1.0*
1.00⫾0.00
7.6⫾0.9
18.2⫾1.1*
0.00⫾0.01
0.99⫾0.03
1.24⫾0.04
0.00⫾0.00
0.88⫾0.06
1.19⫾0.03
0.64
0.20
0.37
0.24⫾0.00
301⫾9
0.24⫾0.00
367⫾28
0.36
0.09
0.20⫾0.01*
604⫾15*
0.22⫾0.01
596⫾40*
⫺0.04⫾0.01
2.01⫾0.06
⫺0.02⫾0.01
1.64⫾0.08
0.04
0.02
Values are means ⫾ SE for dorsiflexor muscle power, tetanic torque, CAR, CMAP, and contractile properties for 9 young and 9 older subjects. Preexercise
values are shown for both age groups, with P values indicating differences across groups in baseline measures. Postexercise values are also given, and * indicate
where these values differed from baseline within each group (P ⬍ 0.05). The right-most column shows the exercise-induced change relative to each group’s
preexercise values. These changes are expressed at the ratios of postexercise to preexercise values for maximal dynamic voluntary contraction (MVDC), tetanic
torque, CMAP amplitude and duration, and t1/2 of tetanic torque relaxation. Because the CAR and maximal RTD are ratios at baseline, the changes in these
variables are expressed as postexercise minus preexercise values. P values indicate differences across groups in the change for each measure.
J Appl Physiol • VOL
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Values are means ⫾ SE for dorsiflexor muscle torque, central activation ratio (CAR), peripheral activation (CMAP), and contractile properties for 9 young
and 9 older subjects. Preexercise values are shown for both age groups, with P values indicating differences across groups in baseline measures. Postexercise
values are also given, and * indicate where these values differed from baseline within each group (P ⬍ 0.05). The right-most column shows the exercise-induced
change relative to each group’s preexercise values. These changes are expressed at the ratios of postexercise to preexercise values for maximal isometric voluntary
contraction (MVIC), tetanic torque, CMAP amplitude and duration, and half-time (t1/2) of tetanic torque relaxation. Because the CAR and maximal RTD are ratios
at baseline, the changes in these variables are expressed as postexercise minus preexercise values. P values indicate differences across groups in the change for
each measure.
MUSCLE FATIGUE IN AGING
971
Fig. 1. Fatigue during the 2 protocols. A: isometric torque expressed relative
to preexercise maximal voluntary isometric contraction (MVICpre), during 3
min (shaded bar) of intermittent MVICs and 10 min of recovery in 9 young and
9 older men. Values are means ⫾ SE. Young men fatigued more than older
men (P ⫽ 0.005), with no group ⫻ time interaction during recovery. B: peak
power, expressed relative to the preexercise maximum voluntary dynamic
contraction (MVDCpre), during 90 dynamic contractions (shaded bar) in 9
young and 9 older men. Values are means ⫾ SE. Young men fatigued more
than older men (P ⫽ 0.007) with no group ⫻ time interaction during recovery.
See text for details.
exercise (Tables 1 and 2). Fatiguing isometric exercise elicited
no significant change in the amplitude of the CMAP in either
age group, although the duration of the CMAP increased
similarly in both groups (Table 1).
As with isometric exercise, there was no change in CMAP
amplitude in either group after dynamic exercise, but there was
an increase in the duration of the CMAP that was similar in
both groups (Table 2). There were no differences across age
groups in CMAP amplitude or duration during recovery from
either exercise protocol (data not shown).
Contractile Properties
Before exercise, the maximum RTDs were similar between
groups (Tables 1 and 2). The t1/2 of torque relaxation was
longer in the unfatigued muscles of older compared with young
subjects before the isometric exercise (P ⫽ 0.02; Table 1),
although this difference was not significant before dynamic
exercise (P ⫽ 0.09; Table 2). Interestingly, for all subjects
combined, slower torque relaxation before exercise was associated with increased fatigue resistance during both the isometJ Appl Physiol • VOL
Fig. 2. Relationships between fatigue (MVCpost-to-MVCpre ratio) and preexercise half-time (t1/2) of tetanic torque relaxation after isometric (A) and
dynamic (B) exercise in 9 young and 9 older men. Preexercise t1/2 was
associated with the ability to resist fatigue during both protocols. That is,
longer t1/2 values before exercise were associated with less fatigue, or higher
MVCpost/MVCpre, during exercise.
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ric (r ⫽ 0.62, P ⫽ 0.005, n ⫽ 18) and dynamic (r ⫽ 0.66, P ⫽
0.004, n ⫽ 18) protocols, as shown in Fig. 2.
After isometric exercise, the RTD did not change in young
subjects, but did increase in older subjects (Table 1), with a
significant difference between the two groups in the magnitude
of this response (P ⫽ 0.02). In contrast, isometric fatigue was
accompanied by a slowing of the processes of force relaxation
(t1/2) in young but not older subjects, although the magnitude
of this response was not significantly different between age
groups (Table 1). Overall, the exercise-induced slowing of t1/2
was not well correlated to fatigue during isometric exercise
(r ⫽ ⫺0.41, P ⫽ 0.10, n ⫽ 18; Fig. 3), presumably due in part
to the lack of change in this variable in the older group.
Dynamic exercise resulted in decreases in the RTD in young
but not older subjects, with the result that the magnitude of this
response was greater in the young (P ⫽ 0.04; Table 2). Torque
relaxation slowed markedly in both young and old groups in
response to the dynamic contractions; the magnitude of this
response was greater in young compared with older subjects
(Table 2; P ⫽ 0.02). In contrast to isometric exercise, with
dynamic exercise there was a significant association between
torque relaxation and fatigue (r ⫽ ⫺0.75, P ⫽ 0.001, n ⫽ 18;
Fig. 3) such that those who slowed the most in response to
exercise had the greatest fatigue. There were no differences
972
MUSCLE FATIGUE IN AGING
ing dynamic contractions is somewhat problematic. Although
fatigue resulted in prolonged CMAP durations, there was no
overall decrease in peripheral excitability in young or older
men during either fatiguing protocol. These results support our
first hypothesis that older adults fatigue less than young adults
during maximal isometric exercise. However, our second hypothesis was not supported, because older men showed no
greater fatigue or central activation failure after repeated maximal dynamic contractions compared with young men. Overall,
these results provide a unique observation that fatigue resistance in the ankle dorsiflexors is relatively enhanced in healthy
older adults under both isometric and dynamic conditions.
Torque, Power, and Fatigue
between the groups in the recovery of contractile properties
(data not shown).
Isometric vs. Dynamic Exercise
To evaluate the task specificity of fatigue using a torque
measure common to both protocols, we measured isometric
tetanic torque before and immediately after each protocol. Both
groups demonstrated a greater fall in tetanic torque after the
dynamic protocol (Table 2) than after the isometric protocol
(Table 1; P ⬍ 0.001 both groups), with no effect of age.
DISCUSSION
The main results of this study were that older men fatigued
relatively less than young men of comparable habitual physical
activity level during both isometric and dynamic exercise of
the ankle dorsiflexor muscles and that the magnitude of fatigue
was associated with in vivo muscle contractile properties. Our
measures of central activation suggested that there were no
age-related differences in the ability to fully activate the
dorsiflexors muscles before or immediately after either type of
exercise, although the measurement of central activation durJ Appl Physiol • VOL
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Fig. 3. Relationships between fatigue and exercise-induced changes in t1/2 of
tetanic torque relaxation after isometric (A) and dynamic (B) exercise in 9
young and 9 older men. Change in t1/2 was associated with the magnitude of
fatigue developed during dynamic but not isometric exercise, such that greater
slowing of force relaxation was observed in those who fatigued more. Axes are
the same for A and B to illustrate the greater impact of dynamic exercise on
both fatigue and the change in torque relaxation.
Before exercise, older men generated ⬃14% less voluntary
isometric torque (not significant; Table 1), and ⬃25% less peak
muscle power (P ⫽ 0.002; Table 2) compared with the young
men. The observation that the loss of power was somewhat
greater than the loss of isometric torque in the unfatigued
muscle is consistent with our laboratory’s recent work in this
muscle group (31) and may be due, in part, to age-related
differences in the time required to reach target velocity during
dynamic contractions. Our laboratory previously found that
older subjects require ⬃21% more time than young subjects to
reach a target velocity of 90°/s in the ankle dorsiflexors (31).
Although all subjects in the present study achieved the target
velocity of 90°/s during the preexercise dynamic contractions,
the brevity of each contraction (1 s) may have resulted in the
attainment of peak torque at a more extended position in the
ROM in the older subjects, thus limiting their ability to develop
maximal power. Furthermore, the relatively greater neural
complexity of the dynamic task, discussed below in Central
Activation, also may have contributed to the loss of power in
the older group.
Our observation of increased fatigue resistance in older men
during isometric exercise is consistent with other studies involving intermittent isometric contractions of the plantar flexors (6), adductor pollicis (17), and ankle dorsiflexors (29).
However, some studies have shown no effect of age on muscle
fatigue during isometric contractions of the knee extensors (6,
43), ankle dorsiflexors (6), and elbow flexors (2). A comparison across these studies reveals that protocols using duty cycles
of 50% or less (i.e., work periods shorter than rest periods)
have found increased fatigue resistance with age (6, 29),
whereas those involving duty cycles ⬎50% have found no
effect of age on muscle fatigue (19, 43). A lower duty cycle
may favor the relatively more oxidative nature of older muscle
(29), as sufficient time would pass during the rest period for the
adequate replenishment of oxygen to the working muscle. This,
in turn, might be expected to enhance fatigue resistance in
older adults under these conditions.
In the present study, older men also fatigued less than young
men during repeated maximal dynamic contractions of the
ankle dorsiflexors, a muscle group used primarily for posture,
balance, and locomotion. The few previous studies that have
examined the effects of age on muscle fatigue by using dynamic contractions have all studied the knee extensors muscles
(30, 33, 36), and all reported no age-related change in fatigue
resistance. The knee extensors are generally involved in more
power-oriented activities than the dorsiflexors, many of which
MUSCLE FATIGUE IN AGING
Central Activation
Before both exercise protocols, the young and older groups
demonstrated full activation of the dorsiflexor muscles during
MVICs (CAR, Tables 1 and 2), a result consistent with those
from previous studies (11, 27, 29). For both study groups, no
J Appl Physiol • VOL
change in CAR was observed during the MVIC performed at
the end of isometric exercise, nor were there differences in
voluntary compared with electrically stimulated fatigue, suggesting that there was no central activation failure in either
group as a result of this fatiguing protocol (7). Similarly, there
was no change in CAR in either group at the end of the
dynamic protocol. Overall, these results suggest that there were
no apparent age-related differences in central fatigue that could
explain the enhanced fatigue resistance found in the older men
during both task conditions.
Although these results are consistent with several previous
studies of fatigue during isometric exercise (20, 29), we had
anticipated that the older men would demonstrate impaired
central activation during the dynamic protocol. Maximal contractions require the ability to rapidly and repeatedly recruit all
motor units at high discharge rates (16), the capacity for which
may be diminished with age (25). It has been suggested that a
more complex task such as dynamic exercise places a greater
demand on the central nervous system than a simpler task such
as isometric exercise (23, 40). Consistent with this concept, our
laboratory has previously observed a marked slowing of rapid
foot tap movements in older adults who showed no reductions
in central activation or specific strength during isometric contractions (27). More recently, our laboratory reported a deficit
in dynamic power production across a range of velocities in the
ankle dorsiflexors of older adults that exceeded the decrease in
isometric torque (31), a phenomenon also observed in the
present study at 90°/s (Tables 1 and 2). Thus we had expected
that the greater motor complexity of dynamic exercise would
lead to fatigue due to central activation failure in the older men,
a result we did not observe.
Although the present data suggest that central activation
failure was not a major contributor to the development of
fatigue, these results must be interpreted cautiously for the
dynamic protocol. Our measures of central activation were
limited to isometric contractions. We must infer by the absence
of central activation failure during isometric contractions that
none occurred during the dynamic contractions. Several investigators have attempted to assess voluntary activation under
nonisometric conditions, but all of these methods have serious
limitations. Babault et al. (4) used the interpolated twitch
technique to assess central activation during concentric contractions of the knee extensor muscles, but others have shown
superimposed stimulation to be unreliable during dynamic
contractions (5). Newham et al. (40) assessed voluntary activation during concentric knee extensor contractions by superimposing brief trains of electrical stimulation during the voluntary contraction. Using this technique, the investigators were
able to detect central activation failure at relatively low (20°/s),
but not higher (120°/s), velocities. James et al. (23) assessed
central fatigue during dynamic knee extension by supramaximal electrical stimulation during isokinetic releases. Unfortunately, this technique has limited application in human studies
due to the discomfort associated with prolonged (⬎1,500 ms)
supramaximal nerve stimulation, as well as the need to make
the measurement during a release maneuver, which may prove
difficult to perform quickly at the end of fatiguing exercise.
More work in this area is necessary before we can fully clarify
the role of central activation in the development of muscle
fatigue during dynamic muscle contractions.
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are unlikely to be maintained across the life span. Thus differences between the dorsiflexors and the knee extensors in their
patterns of use may account for some of the discrepancies
reported with regard to the effect of age on muscle fatigue. In
addition, differences in the size and fiber type distribution of
these two muscle groups, discussed below, may similarly
contribute to the different results regarding age-related changes
in fatigue.
To date, very limited data have been available regarding the
task specificity of fatigue in young and older humans. Furthermore, the lack of control for subjects’ health and habitual
physical activity level in previous studies complicates the
interpretation of many results. A unique contribution of this
study is the observation of an age-related enhancement in
fatigue resistance that is apparent during both isometric and
dynamic tasks performed by the same groups of healthy subjects who were matched for activity level. The fatigue tasks in
the present study were designed to be as comparable as
possible. Greater fatigue as a result of the dynamic task was
observed in both older and young individuals, as indicated by
the greater fall of voluntary (Fig. 1, B vs. A) and tetanic (Table
2 vs. Table 1) torque in response to the dynamic protocol.
These data suggest that the age-related resistance to fatigue can
be observed across a range of fatigue levels, as well as across
different tasks.
Before exercise, electrically stimulated isometric tetanic
torque was 17–25% lower in the older compared with the
young group. In response to the isometric protocol, tetanic
torque fell more in the young than the older group, consistent
with the greater voluntary fatigue observed at that time in the
young subjects. The dynamic protocol resulted in a marked
decline in tetanic torque, with no significant effect of age on
this change. The lack of an age effect may have been due in
part to the fact that, whereas the fatiguing contractions were
dynamic in nature, the tetanic torque measures were isometric.
With both the isometric and dynamic protocols, the brief delay
between the final voluntary contractions and the tetanic torque
measure may have allowed some recovery of tetanic torque
that followed. This possibility could account for the slight,
although nonsignificant, difference in the fatigue of the voluntary vs. tetanic contractions after the isometric protocol.
Previous investigators have suggested that preexercise differences in muscular strength (and, by inference, muscle size)
may explain enhanced fatigue resistance with age, presumably
due to less occlusion of blood flow during contractions in
smaller muscle (3, 8). However, we found that, during the
isometric protocol, the relationship between preexercise muscular strength and fatigue could account for only 21% of the
variability in fatigue. Similarly, preexercise dynamic torque or
power could account at most for only 12–20% of the fatigue
developed during the dynamic protocol. Thus, during the
intermittent MVC protocols used in our study, it does not
appear that muscle size, as reflected by MVC, was a major
factor in the development of fatigue.
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MUSCLE FATIGUE IN AGING
Peripheral Activation
Contractile Properties
Before exercise, the maximum rate of tetanic torque development was similar in both age groups (Tables 1 and 2),
consistent with the report of Van Schaik and colleagues (44).
This result suggests that there were no obvious alterations in
cross-bridge or sarcoplasmic reticulum calcium kinetics in the
older subjects (44). In contrast, torque relaxation was somewhat prolonged in the unfatigued muscle of the older men
(Tables 1 and 2). This age-related slowing of relaxation has
been observed in previous studies (29, 41) and probably
reflects the higher proportion of type I muscle fiber content of
the tibialis anterior muscle in older adults [76% in young, 84%
in old (22)]. It is unlikely that slowed torque relaxation in the
older group was due to deconditioning, because physical activity levels were similar between the groups. Interestingly, the
preexercise t1/2 was associated with the degree of fatigue that
developed during both protocols (Fig. 2), illustrating that the
slower muscle of the older group was also more fatigue
resistant.
In response to isometric exercise, the maximum rate of
tetanic torque development was unchanged in young men, but
it increased significantly in older men (Table 1). This result
suggests that calcium release from the sarcoplasmic reticulum,
calcium sensitivity of the myofibrils, and the rate of crossbridge cycling were not impaired (1) and, in fact, may have
been potentiated in the older muscle during exercise. The
isometric exercise protocol prolonged torque relaxation to a
similar extent in both age groups (Table 1). Slowed force
relaxation is often observed in fatigue and is thought to indicate
impaired calcium uptake by the sarcoplasmic reticulum or
slowed cross-bridge detachment resulting from the accumulation of ADP or Pi in the myoplasm (1, 9).
In contrast to the isometric protocol, dynamic exercise
resulted in a decrease in the maximum rate of tetanic torque
development, with the young subjects exhibiting a greater
J Appl Physiol • VOL
ACKNOWLEDGMENTS
The authors thank the subjects for willing participation in this study. We
also thank Theodore Towse, David Pober, Dr. Graham Caldwell, and Dr. John
Buonaccorsi for assistance with various aspects of this work.
GRANTS
This study was supported by National Institute on Aging Grant R01
AG-21094.
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Before exercise, the CMAP amplitude tended to be greater
in young compared with older men, whereas there were no
differences in CMAP duration. These results are consistent
with some previous reports of CMAP in the dorsiflexor muscles (19, 29) and may reflect differences in surface electrode
configuration, subcutaneous fat content, or preexercise muscle
excitability. There were no changes from baseline in CMAP
amplitude in either group after isometric or dynamic exercise,
indicating that there were no fatigue-induced changes in neuromuscular junction or sarcolemmal excitability, a result consistent with a number of other studies (24, 29).
The duration of the CMAP increased comparably in both
groups during isometric and dynamic exercise (Tables 1 and
2), suggesting that the net velocity of neuromuscular transmission or sarcolemmal action potential propagation was slowed
as a result of exercise. Although the effect of slowed impulse
propagation on muscle fatigue is unknown, the absence of age
group differences in the present study suggests that this factor
does not account for the greater fatigue shown by the young
compared with older subjects. Overall, it appears that differences in peripheral activation do not explain the age-related
enhancement in fatigue resistance observed in response to both
isometric and dynamic exercise.
reduction in RTD than the older subjects (Table 2). Exerciseinduced slowing of RTD suggests that fatigue was accompanied by an impairment in the processes of excitation-contraction coupling or cross-bridge function, possibly due to the
metabolic changes within the muscle that occur during fatigue
(1). The greater slowing of RTD in young subjects suggests a
greater impairment of intracellular processes in this group,
which may partially explain why they fatigued more than the
older subjects.
As with the isometric protocol, dynamic exercise also resulted in a prolonged t1/2 for torque relaxation, although in this
case the amount of slowing was greater in the young men
(Table 2). It is reasonable to expect that the 90 dynamic
contractions were more metabolically costly than the 18 isometric contractions (39) and likely resulted in greater accumulation of metabolic by-products such as Pi and proton, which
may explain the prolonged torque relaxation that we observed
after the dynamic protocol. The relationship between fatigue
and the slowing of torque relaxation observed during the
dynamic protocol (Fig. 3) is consistent with the possibility that
much of the fatigue may have been due to metabolic inhibition
of contraction. In the present study, the older men had less of
a slowing of torque relaxation and less fatigue than the young.
The strong association between the slowing of relaxation and
the degree of fatigue suggests that the greater fatigue in young
compared with older individuals may have been the result of a
greater accumulation of inhibitory metabolites in the young
men. This hypothesis is supported by our laboratory’s recent
observation that fatigue, as well as the accumulation of Pi and
proton, was less in older compared with young adults during
incremental dorsiflexor contractions (29).
The results of this study show that older men fatigue less
than young men during maximal isometric and dynamic intermittent exercise of the ankle dorsiflexor muscles. Thus, with
muscle group and subject characteristics held constant, agerelated enhancements in fatigue resistance appear to extend to
multiple contraction modes. In both age groups, the dynamic
condition elicited greater fatigue and perturbance of contractile
properties than did the isometric condition. We found no
evidence of age-related differences in central or peripheral
activation failure that could explain the differences in fatigue,
although the techniques available to assess central motor drive
during dynamic contractions must be refined to fully clarify the
role of central fatigue during repeated dynamic contractions.
Overall, our results suggest that fatigue under both conditions
developed due primarily to mechanisms distal to the sarcolemma. Age-related differences in muscle metabolism, as suggested here by the associations between contractile properties
and fatigue, could explain the relatively increased fatigue
resistance observed in the older men.
MUSCLE FATIGUE IN AGING
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