Copyright /999 by The Gerontological Society ofAmerica
JournalofGerontology: BIOLOGICAL SCIENCES
1999, Vol. 54A, No. 10, B452-B458
Slowed MuseIe Contractile Properties Are Not
Associated With a Decreased EMGlForce Relationship
in Older Humans
Alexander v. Ng and Jane A. Kent-Braun
Magnetic Resonance Unit, Department ofRadiology, University ofCalifornia, San Francisco.
Wetestedthe hypothesis that, as a result ofslowermusclecontmctileproperties, the electromyogram (EMG)/jorcerelationship is decreased during voluntarycontractionsin oldercomparedto young humans. Westudied22 young (32 ± 1 yr, mean
± SE) and 20 older (72 ± 1) men and women. Toquantitate ankle dorsiflexor muscle properties, we measured isometric
twitch time to peak force and maximal relaxation rate, the rates oftetanic (50 Hz, 1 s)force development and relaxation,
and the stimulatedforce-frequency relationship. The voluntaryEMG/jorce relationshipwasdetermined during isometrie
dorsiflexionfrom 10% to 100% MVC (maximal voluntaryisometric contractionforce) in 10% MVC increments. Twitch
time to peak force and the ratesoftetanie force developmentand relaxation wereslowerin the oldersubjects.Greaterrelativeforce wasproduced in oldercompared to young adults at 10Hz. During voluntarycontractions,EMG wasgreaterin
older compared to young subjects at lower intensities (10% and 20% MVC). Thus, although the older adults exhibited a
slowingofcontractile propertiesand summation offorce when stimulatedat 10Hz, the voluntaryEMG/jorce relationship
was increasedratherthan decreased at low contraction intensities, comparedto young adults.Weconcludethat the slowing
ofcontractileproperties does not result in increasedneural "efficiency" ofvoluntaryforce production in olderadults. This
novelobservationmay have importantfunctional relevanceto the performance ofactivities ofdallyliving,particularlyin a
morefrail olderpopulation.
M
USCLE contractile properties are typically slowed in
aging humans. This slowing is indicated by prolonged
contraction and relaxation times during stimu1atedcontractions
(1-5). One mechanism for this slowing is thought to be a loss
of motor units, leading to a differentialloss of type II muscle
fibers and a shift toward a slower fiber type profile (1,6-9).
It has been suggested that the slowing of muscle contractile
properties with age can resu1t in fusion of muscle force at
lower motor unit firing rates (5,10,11). Such early summation
of force may be indicated by a left-shifted force frequency relationship, whereby greater relative force is produced at lower
frequencies of stimulation (3,12). It has been suggested that
this summation may be advantageous during voluntary contractions, resulting in an increase in neural "efficiency" (5) or
decreased central motor drive (10) necessary to produce a desired voluntary force. Neural efficiency may be assessed by the
electrical activity required to produce a desired muscu1arforce.
This relationship can be examined by recording the electromyogram (EMG) and force during graded contractions. It is
not clear whether force summation at lower frequencies of
stimulation as the result of the age-related slowing of contractile properties confers an advantage in terms of neural efficiency during vo1untarycontractions.
The purpose of this study was to examine neural efficiency
in aging by determining whether the EMG/force relationship is
decreased in older adults. We tested the following hypotheses:
compared to healthy young subjects, healthy older adults show
(a) slower muscle contractile properties, (b) a left-altered stimulated force-frequency relationship, and (c) a decreased EMG/
force relationship. Because habitual physieal activity level may
affect measures of muscle function, young and older experiB452
mental groups were intentionally se1ected for similar levels of
activity, and physical activity was measured.
MErnODS
Subjects
The young group consisted of 12 men and 10 women aged
25-44 years, and the older group comprised 9 men and 11
women aged 65-82 years. Subjects were recruited from the
surrounding San Francisco Bay Area community, and were selected to be nonsmoking and healthy (e.g., no cardiovascular,
metabolic, or immunologie disorders ), based on a standardized
health interview developed for these studies. Subjects were also
selected to be no more than recreationally active, defined here
as no more than two regular exercise sessions per week (e.g.,
hiking, walking, tennis) for the previous 3 months. Using preenrollment interviews, young and older subjects were subjectively screened for similar activity levels. Signed informed consent, as approved by the Committee on Human Research at the
University of Califomia at San Francisco, was obtained from
all subjects prior to their partieipation.
PhysicalActivityMeasurements
Physical activity was estimated for all subjects using both a
7-day recall questionnaire (13) and a 3-dimensional accelerometer (Tritrac R3D, Professional Products, Madison, WI). These
methods have been reported previously (14). Briefly, the 7-day
recall is an interview-based questionnaire that estimates caloric
expenditure by query regarding physieal activity levels over the
previous 7 days. The questionnaire is scored by assigning a
multiple of the resting metabolic rate (MET) value to sleep and
MUSCLE FUNCTION IN OWER HUMANS
4 levels of activity (light, moderate, hard, and very hard), and
caloric expenditure is estimated from the MET levels. The accelerometer is a battery-operated motion detector that measures
acceleration along the x, y, and z axes. The net vector magnitude of the three axes can be used as a representative measure
of motion or activity (14,15). Our purpose in having subjects
wear the activity monitors was not to estimate energy expenditure per se, but rather to obtain a quantitative measure of movement or physieal activity.After informed consent was obtained,
subjects were instructed in the use of the accelerometer, whieh
was subsequently worn for a minimum of 7 days during waking hours in a small padded nylon belt pack secured around the
waist. The data were analyzed in raw activity units, where vector magnitudes were summed over the 7-day period and reported as average daily activity. The 7-day recall questionnaire
was administered when the activity monitor was returned, so
that the measurement period was the same for both instruments.
The same investigator (AVN) administered the 7-day recall to
all subjects.
Muscle Forceand EMG Measurements
These methods have been described in detail previously
(16-18). Muscle testing occurred with the subject seated and
both legs extended. The right leg was studied unless there was a
contraindication to do so (e.g., bunions). The leg to be studied
was stabilized with a knee brace, and the foot angle was fixed
at 120 0 plantar flexion. Dorsiflexor isometric force was measured by a transducer mounted under a footplate at the end of a
Lexan tube, which further stabilized the leg. The transducer signal was amplified (TECA electromyograph TE-4, White Plains,
NY) and coupled to an IBM clone 486 personal computer,
which provided visual feedback during voluntary contractions.
Force and EMG data were collected using Labview software
(National Instruments, Austin, TX) and subsequently transferred to a spreadsheet for analysis.
The surface EMG from the tibialis anterior muscle was measured during all contractions using circular electrodes (10 mm
diameter). The active electrode was placed on the belly of the
tibialis, the reference electrode was placed on the medial malleolus, and a copper groundplate was placed on the calf. In addition, stimulating electrodes were placed over the peroneal
nerve, approximately 1 cm distal to the fibular head. Stimulation was achieved with a TECA NS6 stimulator. Filter settings
for the EMG were 1.6 Hz and 16 KHz.
For the compound muscle action potential (CMAP) and
twitch force measurements, data were collected at 2500 Hz for
0.5 s. For the voluntary contractions, data were sampled at 500
Hz. After electrode placement, the CMAP and corresponding
twitch force were obtained in response to a single supramaximal stimulus of 0.2 ms duration. Supramaximality during all
electrically stimulated contractions was ensured by using a voltage 10%-15% greater than that associated with the highest
peak-to-peak CMAP amplitude. Typieal voltages were from
225-275 volts. Three CMAPs and twitches were obtained 1
minute apart. Peak-to-peak amplitude (mV) and duration ofthe
negative peak (ms) were measured for each CMAP and averaged. Peak force (Tw,N) and time to peak force (Tw-TPF, ms)
and maximal rate of relaxation (Tw-MRR) were measured
from each muscle twitch. The maximal rate of relaxation was
deterrnined from the negative df/dt peak, where force was ex-
B453
pressed as % MVC (maximal voluntary isometric contraction
force) and time was in ms (i.e., % force/ms). Contractile data
reported were those associated with the peak twitch.
Force-frequency relationship.-To investigate the stimulated
force-frequency relationship of the dorsiflexors, we measured
peak muscle force during supramaximal, electrically stimulated
contractions of 1 s duration at 1,5, 10,20, and 50 Hz. We were
limited to these frequencies by the stimulator. These contractions were obtained after the twitch and CMAP measurements
described above, and were separated by 1 minute of rest. Force
data were expressed relative to those obtained from the 50 Hz
stimulus train. We also calculated the maximum rate of tetanie
force development (TF-dev, %/ms) and one-halfrelaxation time
(Tet-HRT, ms) resulting from the 50 Hz stimulation. The maximal rate offorce development (dfldt) was calculated as the peak
of the increase in force (% peak force) divided by the change in
time (ms). The one-halfrelaxation time ofthe 50 Hz stimulation was the time to whieh force fell to 50% ofmaximal, determined from the time of the last stimulus artifact.
MVC.-Maximal voluntary isometric contraction force
(MVC) was obtained after the data for the stimulated forcefrequency relationship. Three MVCs were obtained, each during a voluntary 3-5 s maximal dorsiflexion. One minute of rest
separated each MVC measurement, and an subjects received
verbal encouragement during this procedure. The highest force
ofthe three MVC trials was recorded as the MVC.
EMG/voluntary force relationship.-To investigate possible
changes in the EMG force relationship with age, the subjects
performed graded, nonfatiguing isometric contractions from
10% to 100% MVC in 10% increments. Contractions were
10 s in duration and separated by 1 min rest. Subjects monitored target force, displayed on a computer screen, and received
verbal feedback from the investigators. EMG was collected for
3 s after a stable force level had been achieved, as determined
by the investigator. Typically, 2-5 s were required to achieve
this stability. EMG data were rectified and integrated, and the
force was averaged over the corresponding 3 s window. Both
EMG and contraction force were expressed relative to maximal
values. To ensure that no fatigue developed during the course of
these measurements, the MVC performed at the end of this
series was comparedto the initial MVC.
StatisticalAnalyses
Two-way analysis of variance (ANOVA) was used to test for
mean differences between gender and age groups in the individual variables. If there were no within-group gender effects,
including interactions, the data for both sexes were combined
for the young and older groups. In the event of a Gender X Age
interaction, pairwise comparisons were used to determine
where the differences occurred. To examine the stimulated
force-frequency relationship, we tested for differences between
groups in relative muscle force at each frequency using a repeated measures ANOVA with two "between" factors (gender
and age) and one "within" factor (frequency). Because the force
from the 50 Hz train was used as a normalizing variable, this
data point was excluded from the ANOVA. To examine the
EMG/voluntary force relationship, a repeated measures ANOVA
NG AND KENT-BRAUN
B454
tained from all 22 young and 20 older subjects. Reasons for
missing activity monitor data included loss of monitor (n = 1),
monitor failure (n = 1), and subject noncompliance (n = 2).
was used to test for differences between and within groups in
relative target muscle force, expressed as percentage of MVC.
A second repeated measures ANOVA was then used to test for
differences between and within groups in EMG. The final
MVC was used as a normalizing variable and thus was excluded from the ANOVAs. If a significant interaction occurred
in the ANOVA analyses, pairwise comparisons between age
groups were performed. Analyses were performed using
SYSTAT software (Evanston, IL). For all statistical analyses,
differences were considered significant when p < .05. All data
are presented as mean ± SE except subjects' ages, which are
presented as mean ± SD.
Contractile properties and muscle force.-CMAP and muscle contractile properties are summarized in Tables 2 and 3.
There were no age or gender effects in CMAP amplitude or duration. Twitch force tended to be greater in the young compared
to older groups (13.8 ± 2.1 N vs 9.5 ± 1.3, respectively; p =
.09). There was no gender effect on twitch force (p = .38).
Twitch time to peak force was slower in the older compared to
the young group with no gender effect (121.4 ± 3.0 vs 111.0 ±
2.2 ms, respectively; p < .01). Twitch maximal rate of relaxation tended to be slower in the older compared to younger
group, with no gender effect (-0.81 ± 0.05 vs -0.98 ± 0.07
%/ms, respectively; p = .07).
Tetanie (50 Hz) force tended to be less with age (127.4 ±
18.2 N older vs 164.0 ± 11.8 young, p = .09), and was greater
in men than women (175.1 ± 14.6 N, men vs 119.4 ± 12.8,
women; p = .01), with no age-gender interaction. The older
compared to young subjects demonstrated slower tetanic force
development (0.42 ± 0.02 older vs 0.48 ± 0.02 %/ms, young,
p = .03) and half relaxation time (130.3 ± 8.8 ms older vs 107.1
± 7.1 young, p = .05), with no gender effect. For technical reasons or due to subject discomfort, complete data were obtained
from 15 older and 20 young subjects for the tetanic force and
force-frequency analyses.
RESULTS
Subjects. -Anthropometric data are summarized in Table 1.
The mean age difference between the young and older groups
was 40 years (31.7 ± 4.3 vs 71.9 ± 4.1 yr, respectively, mean
± SD). A significant statistical interaction suggested that the age
difference between the young and older women was greater
than the difference between young and older men. The ANOVA
also indicated that women were shorter than men, but did not
differ in weight. Five of the older women were on estrogen replacement therapy (ERT) and six were not.
Physical activity.-There were no differences in physical activity between genders, whether measured by activity monitor
(p = .79) or by questionnaire (p = .34), so gender data have
been combined for both age groups. Physieal activity was similar in the young and older groups, whether measured by activity
monitor (163.0 ± 14.0 vs 137.0 ± 15.1 arbitrary units/d/l000,
respectively; p = .22) or estimated by questionnaire (36.7 ± 1.0
vs 35.5 ± 0.6 kcal/kg/d, respectively; p = .17). These analyses
were based on activity monitor measurements obtained from 20
young and 18 older subjects. The 7-day recall data were ob-
MVC.-Men were shown to be stronger than women (Table
2). There was no age effect on MVC. However, a significant interaction (p = .04) and subsequent pairwise comparisons indicated that the younger men were stronger than the older men
(p = .03). There was no difference in strength between young
and older women (p = .56). In the subjects for whom we had
both measurements (Table 3), MVC and tetanie force yielded
Table1.Anthropometrie and Physieal Aetivity Charaeteristies of 10Young Wornen, 11OiderWornen, 12Young Men, and 9 OiderMen
YoungWomen
OlderWomen
30± 2
167± 3
78 ± 7
181 ± 21
73± I
164± 3
64± 6
127 ± 18
Age (yr)
Height (ern)
Weight (kg)
Physical activity (arb. U/d/l000)
YoungMen
34±
178±
81 ±
145 ±
1
2
6
19
OlderMen
Age Effect
Gender Effect
Interaction
71± 2
178± 3
82± 7
150±23
NA
.65
.38
.28
.64
<.001
.12
.69
.04
.64
.26
.19
Notes: Physical activity was measured with a 3-dimensional accelerometer and expressed as a vector magnitude in arbitrary units. Values are mean ± SE. Analysis
was by two-factor (age, gender) ANOVA. No p value is reported for age (NA) because the groups were selected apriori to be distinctly different in this variable.
Table2.Ankle Dorsiflexor MuscleForceand Contraetile Properties in Young and OiderWornen and Men
CMAP(mV)
CMAP(ms)
Tw(N)
Tw-TPF(ms)
Tw-MRR (%/ms)
MVC(N)
YoungWomen
OlderWomen
8.8 ±
14.4 ±
12.4 ±
108.4 ±
-o.92±
135.7 ±
8.3 ±
14.0 ±
9.0 ±
123.2 ±
-0.82 ±
148.9 ±
0.5
0.7
2.8
3.9
0.08
15.0t
0.9
0.6
2.0
4.1
0.06
16.2
YoungMen
OlderMen
Age Effect
Gender Effect
Interaction
9.0 ± 0.4
15.5 ± 0.6
15.1 ± 3.1
113.2 ± 2.9
-0.98 ± 0.08
261.8 ±19.4*
8.2 ± 0.7
14.4 ± 0.5
10.1 ± 2.0
121.1 ± 4.9
-o.80± 0.09
196.9 ± 21.7
.38
.30
.97
.53
.38
.94
.79
<.01
.89
.28
.87
.28
.63
.09
.02
.07
.16
.04
Notes: Compound muscle action potential (CMAP) amplitude (mV) and duration (ms), twitch force (Tw), twitch time to peakforce (Tw-TPF), twitch maximum
rate ofrelaxation (Tw-MRR), and maximal voluntary contraction (MVC) ofthe dorsiflexors in 10 young women, 11 older women, 12 young men, and 9 older men.
Data are mean ± SE. Analysis was by two-factor (age, gender) ANOVA. *p< .05, young men vs older men; tp< .05, young women vs young men.
MUSCLE FUNCTION IN OLDER HUMANS
similar statistical results. That is, men were stronger than
women, and there was a tendency for the young to be stronger
than the older subjects.
Because five of the older women were on ERT and six were
not, we performed exploratory analyses to determine if ERT
may have affected muscle function. Analyses were by unpaired
t tests, and data are presented as mean ± SE. There were no significant differences between ERT and non-ERT women in
twitch force (9.2 ± 2.7 N vs 9.5 ± 2.3, respectively;p = .94),
MVC (161.8 ± 19.6 N vs 138.1 ± 29.2, respectively;p = .53),
or tetanic force (93.0 ± 10.8 N vs 87.5 ± 28.7, respectively; p =
.86). More importantly, there were no significant differences
between ERT and non-ERT women in the following muscle
contractile properties: twitch time to peak force (125.1 ms ± 3.5
vs 124.1 ± 10.1, respectively;p = .92), rate of tetanic force development (0.41 ± 0.04 %/ms vs 0.47 ± 0.03, respectively; p =
.33), and tetanic half relaxation time (120.8 ± 9.2 ms vs 154.0 ±
33.1, respectively; p = .27).
B455
Stimulatedforce-frequency relationship. - This relationship
is illustrated in Figure 1. There were no gender differences in
the stimulated force-frequency relationship (p = .16), so gender data have been combined in both age groups. There was a
significant Age X Frequency interaction (p < .01), and pairwise comparisons indicated that greater relative force tended to
be produced by the older subjects at the 10 Hz frequency (p =
.05), as shown in Figure 1. As mentioned above, these data
comprise a subset of 15 oider and 20 young subjects.
EMG/voluntary force relationship.-The EMG/voluntary
force relationship is illustrated for both groups in Figure 2.
Because there was no significant gender effect (p = .32), gender
data have been combined for both groups. Both groups successfully increased force in a graded linear fashion, and there were
no differences in relative force held between groups (p = .99).
MVC at the end of this protocol was 97 ± 2% of the initial MVC
in the young group and 95 ± 2% in the oider group. These dif-
Table3. AnkleDorsiftexor MuscleForceand Contractile Properties in a SubsetofYoungand OlderWornen and Men
TF(N)
TF-dev (%/ms)
Tet-HRT (ms)
MVC(N)
YoungWomen
OlderWomen
145.4 ± 18.1
0.49± 0.02
104.9 ± 3.2
148.7 ±20.2
90.5 ±
0.43 ±
133.3 ±
140.8 ±
YoungMen
13.1
0.03
13.6
18.1
179
±
0.46±
108.8 ±
261.8 ±
14.7
0.03
13.0
19.4
OlderMen
AgeEffect
168.8 ± 30.6
0.40± 0.03
127.3 ± 12.0
212.7 ± 31.1
.09
.02
.05
.22
Gender Effect
Interaction
.01
.21
.92
.26
.86
.74
.31
<.01
Notes: Tetanie force from 50 Hz stimulation (TF), maximum rate of tetanic farce development (TF-dev), and tetanic half relaxation time (Tet-HRT) from 8
young warnen, 8 older warnen, 12 young rnen, and 7 older rnen. Mean maximal voluntary contraction force (MVC) statistics from this subset are also provided.
Analysis was by two-way ANOVA. Data are mean ± SE.
100
100
..-.. 80
N
...-..
E 80
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E
::J:
0
It)
-;C
60
ca
';:/!.
0
"-""
CI)
...0
U
LI.
60
:E
40
-0-
~
0
Young
p<O.01
40
*
"-"'
e
..... Older
20
-0-
~
Young
Older
:E 20
W
o
o
o
10
20
30
40
50
Stimulation Frequency (Hz)
Figure 1. Stimulated force-frequency relationship in the ankle dorsiflexors
of young (open squares) and older (closed circles) subjects. Age by frequency
interaction, p < .01. Pairwise comparison revealed that force in the older subjects was relatively higher at 10Hz (p = .05), young versus older. Data are
mean ±SE.
o
20
40
60
80
100
Force (% MVC)
Figure 2. EMG/voluntary force relationship in the ankle dorsiflexors of
young (open squares) and older (closed circles) subjects. EMG = integrated surface electromyogram. Age by force interaction, p =.02. Pairwise comparisons
revealed that EMG in the older group was relatively higher at 10% MYC (p <
.01) and 20% MVC (p = .06). Data are mean ± SE.
B456
NG AND KENT-BRAUN
ferences were not different from initial MVC in the young (p =
.71) or older (p = .89) groups, indicating that no appreciable
muscle fatigue occurred as a result of performing this protocol.
Relative EMG also increased in a linear fashion in both age
groups. Although there was no significant main effect (p = .16),
a significant interaction (p = .02) and subsequent pairwise comparisons indicated that the older group had an increased relative
EMG compared to the young group at 10% MVC (p < .01),
and a tendency toward an increase at 20% MVC (p = .06) and
40% MVC (p = .09).
DISCUSSION
The results of this study demonstrated that, in addition to
slower dorsiflexor muscle contractile properties, the older compared to young subjects had an increase in relative force production during low frequency stimulation (10 Hz). Despite this
relative increase in force production, the surface EMG at low
voluntary force levels was increased, not decreased, compared
to younger adults. Thus, slowed muscle contractile properties in
the older compared to young did not lead to a decreased EMG/
force relationship. Therefore, slower muscle contractile properties in older adults do not result in an increased neural efficiency
during voluntary contractions. This novel observation may have
important functional relevance to the performance of activities
of daily living, particularly in a more frail older population.
Strength andforce.-A decrease in strength with age is a
common (3,5,19-22) but not universal (2,23) finding. We observed differences in dorsiflexor voluntary strength in the men
but not the women. Some of the older women in this study were
on ERT; however, our data, which showed a lack of difference
in strength and contractile properties between women with and
without ERT, suggest that ERT was not a confounding factor in
this study. These data emphasize the importance of accounting
for gender when examining strength in aging, because there
was no difference in strength when groups were compared as a
whole (i.e., older vs young).
Electrically evoked tetanie force was greater in men compared to women, and tended to be higher in young compared
to older subjects (Table 3). In general, tetanie force followed
the same pattern of response that was observed in those subjects for whom we also had MVC measurements. However,
because inadvertent stimulation of antagonist muscles can
occur with peroneal nerve stimulation, tetanic force should be
considered a secondary measure of muscle force to the MVC.
Because we normalized stimulated and voluntary forces to
their respective maximums (i.e., tetanie force and MVC), we
accounted for any influence of varying force on the relationships in Figures 1 and 2.
We have shown a tendency toward lower twitch force production in the older subjects. The effect of age on peak twitch
force is equivocal (2-5,20,24-26). Previous studies using the
dorsiflexor muscle group have shown twitch force in older compared to young subjects to be less (5), unchanged (24,26), or
greater (2). Differences between studies may have been the result of differences in age groups studied, health of subjects, or
methodology.
CMAP amplitude and duration were similar in our young and
older subjects. These findings suggest no difference in neuromuscular or muscle membrane excitability between healthy
young and older adults. Previous investigations involving the unfatigued dorsiflexor muscles have found CMAP amplitude to be
diminished in older adults (2,5). Perhaps the reason for the similarity of CMAP amplitudes in our study was that subjects were
selected to be similar in physical activity, as confirmed by accelerometer. Training can result in an increase in CMAP amplitude (27); if our older subjects were more physieally active than
older subjects in other studies, then a relatively greater CMAP
amplitude could result. Finally, CMAP is dependent not only on
the integrity of neuromuscular transmission, but also on skin and
subcutaneous fat, which may change with age or physical activity. Thus, our data suggest that a diminished CMAP amplitude
does not appear to be a necessary consequence of healthy aging.
Muscle contractile properties.-In contrast to peak twitch
force, the slowing of muscle twitch time to peak force (Table 2)
and tendency toward slowing of twitch relaxation rate reported
here have been consistent findings with age (1-5,12,26). The
effect of aging on muscle contractile pro1?erties during a train of
stimuli is less conclusive (2,4,12,26,28).' Our results are consistent with previous investigators who have reported a prolonged
rate oftetanic force development (4) and relaxation (4,12) in elderly subjects, though this is not a universal observation
(2,26,28). The slower contractile characteristics of older adults
are thought to reflect a relative loss or atrophy of type II muscle
fibers (7,9,29,30) and also suggest a role for altered sarcoplasmic reticular Ca" release or re-uptake (31).
An alternate explanation for the slower contractile properties
in the older subjects is that they may have been less active than
their younger counterparts. Inactivity or muscle disuse can result in a slowing of contractile properties similar to that noted
with aging (32). Our findings show no difference in physical
activity between the young and older groups studied, whether
measured by questionnaire or accelerometer. Therefore, our results regarding contractile properties are not likely to have been
due to an effect of physieal activity level.
There are few studies of the effects of age with respect to
gender on human skeletal muscle contractile properties. In the
dorsiflexors, Vandervoort and McComas (5) have reported that
in a group of 20- to 100-year-olds there was no difference between men and women in twitch time to peak torque and half
relaxation time. Our results are consistent with their results.
However, Hieks and McCartney (33) have indicated that, although twitch time to peak torque was similar, half relaxation
time was shorter in older women, compared to older men. We
observed no gender effects in the age-related slowing of muscle
contractile properties.
Stimulatedforce-frequency relationship.-It has been suggested that slower muscle contraction and relaxation times in
older adults could be an adaptation that preserves relative
strength, as slower muscle contractile properties will result in
tetanic fusion at lower motor neuron firing rates (5,10). The importance of such an adaptation is emphasized by the lower submaximal (34-36) and maximal (37) motor neuron firing rates
reported during voluntary contractions in older humans. Our
hypothesis was that a muscle force-frequency relationship altered to the left, as partially observed in the present study, may
help to maintain adequate force production at lower motor neuron firing rates.
MUSCLE FUNCTION IN OLDER HUMANS
Our observation of a significant increase in relative force
onlyat 10 Hz suggests that muscle contractile properties in the
older subjects were not slowed enough to enhance summation
of force at 5 Hz. It would also appear that at 20 Hz stimulation,
no additional advantage was afforded by the slowed contractile
properties in older adults. The increased relative force produced
at a low stimulation frequency in the older compared to young
subjects is consistent with work by others (2,3,12). These previous studies also reported a slowing of twitch contraction and relaxation rates (2,3) and tetanic relaxation rates in the same subjects (3,12). Interestingly, Narici and colleagues (12) studied
men from 21 to 91 years of age and demonstrated greater relative force production of the adductor pollicis in men older than
80 years along the "entirety" of the force frequency curve at 10,
20, and 30 Hz. This older group also had the greatest prolongation of tetanie force relaxation. These data suggested that
slowed muscle contractile properties were the mechanism for
the altered force-frequency relationship. This alteration may be
most pronounced and associated with the greatest slowing of
contractile properties in the oldest subjects.
Not all previous studies have reported an altered forcefrequency relationship in elderly subjects (25,28). However, in
some studies that did not observe a leftward alteration with age,
the data were expressed as absolute force (4,26), or muscle contractile properties were not obtained from the same subjects (4),
thereby making interpretation of the data difficult. In other studies that did not report an alteration of the force-frequency relationship in older adults, tetanic rates of contraction and relaxation did not differ between the young and older experimental
groups (25), which would negate the suggested mechanism of
any force-frequency alteration.
EMG/voluntaryforce relationship.-The EMG is largely a
function of motor unit recruitment and firing rates (25,28,38).
Therefore, changes in the EMG, in the absence of a change in
CMAP, can be thought to reftect changes in central motor
drive. If less central motor drive is required as the result of a
more favorable muscle force-frequency relationship, then a
change in the EMG/force relationship may occur. This change
would be in the direction of less EMG activity required for a
given voluntary force level. This could be thought of as an increase in neural efficiency (39-42). Such a change in motor
drive, accompanied by the change in force-frequency relationship, could be an adaptation to preserve muscle force-generating capacity despite changes in motor unit number and size
with aging (1,5,8). In contrast to the hypothesized decreased
EMG/force relationship in the older group, we observed an increased relative EMG at low force levels.
One explanation for the increase in relative EMG at 10%
MVC (and tendency at 20% and 40% MVC) is that larger
motor units (1,5,43-45) are recruited at low force levels in elderly adults (1), possibly with less capacity for rate coding.
The result could be greater relative EMG in the young than in
the elderly subjects (11,19). A second possible explanation is
that the increased EMG/force relationship in elders may reftect
reduced neural "coordination" between agonist and antagonist
muscle groups. That is, increased coactivation of antagonist
muscle groups in the older subjects may require greater agonist activation and EMG to produce the desired force. This
may occur despite any advantage from an "improved" force-
B457
frequency relationship. With training, force ftuctuations during
submaximal isometric exercise of the first dorsal interosseous
were shown to be decreased or improved in the older subjects
(23). This improvement in force-holding ability was thought to
be the result of improved coordination between agonist and antagonist muscle groups. The EMG during submaximal contractions was not reported in this previous study (23). However, if
coordination at low force levels was reduced in the older subjects before training, then an increased EMG, such as we have
observed, might have been an expected observation.
Our observation of an increase in EMG at a low relative
force level in the older compared to young group does not support the suggestion of a decreased central motor drive or increased neural efficiency with aging. Because central motor
drive comprises motor unit recruitment and firing rates, knowledge of motor unit firing rates, which we did not measure,
would provide further insight into the mechanism of the altered
EMG/force relationship in the elderly group. Knowledge of antagonist muscle activation (e.g., EMG) would also give insight
into the altered EMG/force relationship.
Limitations.-We chose to have each group perform the voluntary contractions in the same order to avoid any inadvertent
order effect that might occur with randomization. As a result of
our design, some cumulative effect of fatigue, which was not
reftected in a decrease in peak force, may have affected the
EMG signal. However, because the same order was followed in
both experimental groups, and there was no apparent effect of
fatigue on the MVC, we assume that any possible cumulative
effect of fatigue on the EMG would likely have affected both
groups similarly. It is unlikely that any effect of fatigue affected
the results at the lower intensities where the differences in EMG
were most apparent. An advantage of the order used was that it
results in very accurate force targeting by the subjects, as
demonstrated by the small error bars for force in Figure 2.
It might be argued that there may have been a change in activation during the MVCs before or after the contraction protocol. If the MVCs were not truly maximal, then the submaximal
contraction intensities would be underestimated. However, as
there was no difference in pre- versus end-protocol MVC
within groups, there is no evidence to suggest that muscle activation may have differed systematically in either group.
Furthermore, if the older subjects were not maximally activating their muscle during the initial MVC, then they would actually have performed contractions at a lower % MVC than indicated. This would make the increased EMG at low relative
intensities even more significant.Finally, in a larger study of the
effects of age on muscle function (46), we observed no agerelated activation impairment of the ankle dorsiflexors, which is
consistent with the results of others (5).
Summary.-In the dorsiflexor muscles, we have confirmed
previous reports documenting a slowing of muscle contractile
properties in older compared to young adults. In these same
older subjects, we also observed an increased relative force production at 10Hz stimulation. This alteration in the relative
force-frequency relationship was likely a consequence of the
slower muscle contractile properties and could be considered
adaptive or compensatory in nature. However, in spite of this
adaptation, we observed an increase rather than a decrease in
B458
NG AND KENT-BRAUN
the EMG at low levels of voluntary force in the older subjects.
Thus, this novel observation indicates that, in contrast to the
suggested hypothesis, the slowing of muscle contractile properties in older adults does not result in a decreased EMG/force relationship. The consequences of an increased motor drive during voluntary muscle contractions in older adults may have
particular relevance to less healthy adults, as the activities of
daily living typically occur at low intensity levels.
ACKNOWLEOOMENTS
This work was supported by grant R29 AG-12819 from the National Institute
on Aging.
The authors acknowledge the assistance ofMr. Hung T. Dao in the acquisition and analysis of the data, Mr. Tony Hill for technical expertise, and Dr; John
Neuhaus for statistical advice. The authors also thank Dr. Michael W. Weiner
for use of the Magnetic Resonance Unit facilities.
Address correspondence to Dr. Alexander V. Ng, UCSFNA Medical Center,
Magnetic Resonance Unit, 4150 Clement Street (114M), San Francisco, CA
94121. E-mail: [email protected]
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Reeeived Oetober 28,1998
Aeeepted May 26, 1999