Vol. 93, Issue 5, 1616-1621, November 2002
Changes in motor unit discharge rate are not associated with
the amount of twitch potentiation in old men
C. S.
Klein1,
C. L.
Rice1,2,
T. D.
Ivanova3, and
S. J.
Garland3,4
1 Schools of Kinesiology and
3 Physical Therapy, and 2 Departments of
Anatomy and Cell Biology, and 4 Physiology, The
University of Western Ontario, London, Ontario, Canada N6G
1H1
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ABSTRACT |
This study examined, in nine
old men (82 ± 4 yr), whether there is an association between the
magnitude of change in motor unit discharge rate and the amount of
twitch potentiation after a conditioning contraction (CC). The evoked
twitch force and motor unit discharge rate during isometric
ramp-and-hold contractions (10-18 s) of the triceps brachii muscle
at 10, 20, and 30% of the maximal voluntary contraction were
determined before and 10 s, 2 min, 6 min, and 11 min after a 5-s
CC at 75% maximal voluntary contraction. After the CC, there was a
potentiation of twitch force (approximately twofold), and the discharge
rate of the 47 sampled motor units declined (P < 0.05)
an average of 1 Hz 10 s after the CC, compared with the control
condition. The CC had no effect on the variability (coefficient of
variation) of both force and discharge rate, as well as the
electromyographic activity recorded over the triceps brachii and biceps
brachii muscles. In contrast to our earlier study of young men (Klein
CS, Ivanova TD, Rice CL, and Garland SJ, Neurosci Lett 316:
153-156, 2001), the magnitude of the reduction in discharge rate after
the CC was not associated (r = 0.06) with the amount of
twitch potentiation. These findings suggest an age-related alteration
in the neural strategy for adjusting motor output to a muscle after a CC.
motoneuron; rate coding; skeletal muscle; contractile properties; aging
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INTRODUCTION |
THE DECREMENT IN
PHYSICAL performance in adults over 65 yr of age can be ascribed,
in part, to a loss of muscle mass and strength (23, 36).
The impaired physical performance of older adults, such as reduced
force steadiness, may also result from changes in the neural strategies
used to control muscle force secondary to alterations in motor unit
morphology and motor unit behavior (27, 37). An acute
reduction in motor unit discharge rate has been observed in young
adults during brief nonfatiguing (10 s) and fatiguing (several minutes)
constant-force contractions (6, 13, 33). For example, De
Luca and colleagues (6) reported a progressive decrease in
the discharge rate of most motor units sampled during 8- to 15-s
contractions of the first dorsal interosseus and tibialis anterior
muscles at 30-80% of maximal force. However, this
contraction-induced reduction in discharge rate was blunted in the
first dorsal interosseus muscle of older compared with younger subjects
(12). The reason for this age-related difference in motor
unit behavior is unclear.
One possible mechanism to explain this blunted reduction in discharge
rate may relate to the diminished postactivation potentiation (PAP) of
twitch force with advancing age (18, 34, 40). In other
words, because of the lower PAP, a smaller reduction in discharge rate
would be necessary to maintain a constant force output in old compared
with young adults (1). The relationship between PAP and
motor unit discharge rate has not been described in the older
population. However, a significant negative correlation between the
magnitude of the reduction in discharge rate and the amount of PAP was
observed in the triceps brachii muscle of young men (24).
In addition, age-related differences in PAP have not been determined in
the muscles of the upper limb. Thus the purpose of the present study
was to determine the relationship between the acute change in the
discharge rate of motor units and PAP in old men.
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METHODS |
Subjects.
Nine healthy men, 76-86 yr (mean 82 ± 4 yr), participated in
the study. Their mean weight and height were 74.9 ± 13.0 kg and 177.2 ± 5.9 cm, respectively. All subjects were ambulatory and were living independently in the community. They were free of medical
conditions and medications that affect muscle performance. A few
subjects participated in recreational activities such as golfing,
bicycling, and walking, but none was highly trained. The local ethics
review committee of the institution approved all procedures, and
informed, written consent was obtained from each subject. Several
aspects of the present data are compared with data obtained from young
men who completed the same protocol (24).
Maximal voluntary contraction and twitch contractile properties.
Subjects were seated with the nondominant (left) forearm resting in
front of them on a platform in the horizontal plane (13). The shoulder and elbow were positioned securely in 80 and 90° of
flexion, respectively. To measure elbow extensor force, the forearm was
semipronated and the wrist was secured in a U-shaped brace that was
mounted on a force transducer. The maximal voluntary contraction (MVC)
of the elbow extensor muscles was recorded as the greatest force of
three to five attempts, each held for 3 s, with a 2-min rest.
Strong verbal encouragement and visual feedback were provided during
the contractions.
Twitches were evoked by use of a constant voltage electrical
stimulator. The cathode was an 8-mm disc electrode filled with conductive gel, which was placed over the motor point of the lateral head of the triceps brachii. The anode was a lead plate
(8.5 × 5 cm) wrapped in gel-soaked gauze positioned lateral to
the scapula over the teres minor muscle (to stimulate the radial
nerve). Peak twitch force (Pt) at rest was determined by applying
pulses (50-100 µs) of progressively greater voltage until the
force plateaued. The voltage level used to determine Pt was maintained
for the remainder of the protocol.
Motor unit and surface electromyography recording.
Motor unit activity was recorded with branched bipolar fine-wire
electrodes (stainless-steel with formvar insulation, 50 µm in
diameter) inserted subcutaneously over the lateral head of the triceps
brachii (11). Two electrodes were inserted, offset from
each other by a distance of ~2 cm. The positions of the subcutaneous electrodes were adjusted so that one or more motor units were active
during brief voluntary contractions at 10-30% MVC. Surface electromyography (EMG) was recorded with 8-mm electrodes placed in a
bipolar configuration over the lateral head of triceps brachii and
biceps brachii muscles. A ground strap was placed around the right wrist.
Experimental protocol.
Subjects were tested on two occasions with the same protocol previously
described for young subjects (24). On the first visit, the
maximal isometric force (MVC) of the elbow extensor muscles was
determined as described above, and the subjects practiced the entire
protocol but without motor unit activity being recorded. During the
second visit, which was held 3-7 days after the first, motor unit
activity was recorded. To avoid PAP of twitch force before the
conditioning contraction (CC), the MVC was not performed before the
protocol on the second visit. Instead, the peak MVC determined during
the first visit was used to set the target forces for the ramp-and-hold
contractions. However, MVC force was measured at the end of the
protocol during the second visit (see Data analysis).
A maximal twitch of the triceps brachii was recorded before any
voluntary contractions (initial twitch; Fig.
1). For the control sequence of
ramp-and-hold contractions, subjects traced force templates at 10, 20, and 30% MVC or 30, 20, and 10% MVC (balanced across the subjects),
with twitches evoked 2 s after each contraction (control
twitches). There was a 10- to 14-s rest period between each voluntary
contraction. The rate of force increase and decrease during the ramp
phase was 5% MVC/s, and the force plateau was maintained for 6 s.
After the control sequence was recorded, PAP was induced by a 5-s CC at
75% of the MVC. The 75% MVC was chosen, rather than 100% MVC, to
minimize movement of the subcutaneous electrodes during the
contractions. The ramp-and-hold contractions were then repeated at
10 s, 2 min, 6 min, and 11 min after the CC. A maximal twitch was
recorded before and after each ramp-and-hold contraction and 2 s
after the CC, so that the recovery time course of PAP could be
determined. Four subjects agreed to repeat the protocol after a 20-min
rest but performed the contractions in reverse order to their first
experiment, and different motor units were recorded. Therefore data are
presented for nine subjects who completed a total of 13 tests.
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Fig. 1.
Schematic of the experimental protocol showing the three
ramp-and-hold contractions at 10, 20, and 30% of the maximal voluntary
contraction (MVC) before and after the conditioning contraction (CC)
and the twitches evoked after each contraction. The 3 voluntary
contractions and evoked twitches were also recorded at 2, 6, and 11 min
after the CC (not shown). Note that 5 of the 9 subjects performed the
contractions in reverse order (30, 20, and 10% MVC).
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Data analysis.
Force, surface EMG, and motor unit activity were analyzed off-line by
use of customized Spike 2 software. The surface EMG recordings were
amplified, filtered at 10 Hz-1 kHz, and digitized at 2.5 kHz, and
the force recordings were digitized at 0.5 kHz. The subcutaneous EMG
signals were amplified, filtered with a 10 Hz-10 kHz band pass,
and digitized at 20 kHz. Motor unit potentials were identified with a
template-matching algorithm (Spike 2, Cambridge Electronics). The
threshold forces of motor unit recruitment and derecruitment were
determined as the force levels during the ramp phases at which a motor
unit started or stopped discharging, respectively. The discharge rate
(in Hz) of each motor unit was calculated as the average over the
middle 2 s of the 6-s plateau. The coefficient of variation (CV)
of discharge rate, CV of force, root mean square (RMS) of the surface
EMG, and the average force were determined over the same 2-s period.
The RMS of the EMG in the triceps brachii and biceps brachii muscles
during the ramp-and-hold contractions were expressed as the percentage
of the RMS EMG recorded during postprotocol MVCs of the elbow extensors
and flexors, respectively. The contraction time (CT) of the twitch was
determined as the time between the initial increase of force from
baseline and peak force. One-half relaxation time (1/2 RT) was the time
for peak force to fall to half its value.
Statistical analysis.
A two-factor analysis of variance was used to compare the effects of
force level (10, 20, and 30% MVC) and time on the absolute and
relative changes in the variables as a result of the CC. A three-factor
ANOVA (age group × force × time) was used to compare the
present data to the results obtained in young subjects
(24). Post hoc comparisons (Tukey's test) were completed
to separate any force level and time effects. The relationship between
variables was determined with the Pearson's product-moment correlation
coefficient. Unless otherwise noted, data are presented as means ± SD, and the 
level of significance was set at P < 0.05.
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RESULTS |
Contractile and motor unit properties before the CC.
The MVC force and initial Pt, CT, and 1/2 RT (before the control
ramp-and-hold contractions) were 171 ± 40 N, 7.8 ± 4.1 N, 93.3 ± 9.6 ms, and 79.2 ± 21.8 ms, respectively. After each
ramp-and-hold contraction, a control twitch was evoked. The Pt
increased (~20%) significantly (P < 0.05) after the
30% MVC but not after the 10 or 20% MVC control contraction. Thus
contraction intensity as low as 30% MVC was sufficient to evoke some
potentiation of twitch force.
A total of 81 different motor units were sampled during the control
ramp-and-hold contractions before the CC. The recruitment and
derecruitment force thresholds of these motor units were 15.1 ± 6.5 and 14.3 ± 7.5% of the MVC, respectively. The mean motor unit discharge rate, CV of discharge rate, and CV of force during the
control contractions are displayed in Table
1. The mean discharge rate, but not CV of
discharge rate or CV of force, differed significantly (P < 0.001) between the three force levels.
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Table 1.
Mean and variability of motor unit discharge rate and variability of
force during the control ramp-and-hold contractions
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Contractile and motor unit properties after the CC.
The Pt significantly increased to 18.6 ± 9.3 N measured 2 s
after the CC, an increase of 233 ± 29% relative to the initial twitch. The second series of ramp-and-hold contractions started 10 s after the CC. At this point, Pt was potentiated ~150-220%, CT
was reduced by 12%, whereas 1/2 RT was unchanged, relative to the
corresponding control twitch (Fig. 2).
The changes in Pt and CT returned to control levels by 6 and 2 min,
respectively. Of the 81 motor units sampled during the control
contractions, 47 were recorded 10 s after the CC on the basis of
an unchanged shape and amplitude of the motor unit waveform. The other
units could not be followed reliably for analysis because of changes in
the shape of the waveform after the CC. The discharge rate (Hz) of
these 47 units before and after the CC at all force levels is
summarized in Table 2, and the percent
changes are displayed in Fig. 2. The discharge rate, 10 s after
the CC, decreased by 0.5 Hz or more (range 0-3 Hz) in 90% of the
motor units (P < 0.05) at all force levels and
returned to control values by 6 min (Fig. 2). The average plateau force
(N), CV of force, and CV of discharge rate did not change significantly
from control values after the CC. Thus the reduction in discharge rate
could not be attributed to the subjects failing to reach and maintain
the target force.
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Fig. 2.
Relative changes in twitch contractile properties and
motor unit discharge rate of the triceps brachii muscle after the CC.
Values are means ± SE presented as a percentage of the control
response for all tests. Top: peak force (Pt), contraction
time (CT), and one-half relaxation time (1/2 RT) of the twitch pooled
for all contraction levels. Bottom: mean motor unit
discharge rate during the 10, 20, and 30% MVCs. * Significant
difference from control values on the basis of the analysis of the
percentage change in discharge rate and contractile properties.
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The relative increase in Pt 10 s after the CC was not
significantly correlated (r = 0.06, P > 0.05) with the relative decrease in discharge rate (Fig.
3). This figure also shows that the
amount of PAP after the CC was not different between the twitches
evoked after the first, second, and third ramp-and-hold contractions (P > 0.05). The RMS EMG of the triceps brachii was
unchanged after the CC. Also, the level of coactivation (~1-3%)
in the biceps brachii was not affected by the CC. The MVC force taken
at the end of the protocol was not significantly different (paired
t-test) from the MVC force recorded during the first visit,
which suggests that minimal force fatigue occurred during the protocol.
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Fig. 3.
Relationship between changes in twitch force and motor unit
discharge rate 10 s after the CC. Data are presented for the first
(10 or 30% MVC, black circles), second (20% MVC, gray circles), and
third (10 or 30% MVC, open circles) ramp-and-hold contractions for 9 subjects (13 tests). The discharge rate is the mean of 2-5 motor
units as a percentage of the control discharge for each subject. There
was no significant correlation (r = 0.06) between
changes in twitch force and motor unit discharge rate after the CC.
Note that no motor units were recorded in 1 subject during the first
contraction (n = 8) and in 2 subjects
(n = 7) during the third contraction.
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DISCUSSION |
Previous investigators demonstrated that the discharge rate of
motor units decreased during constant-force contractions, and the
magnitude of the reduction was greater at higher (i.e., 50-80% MVC) compared with lower intensities (i.e., 20% MVC) (6, 12, 13,
33). In addition, the discharge rate of motor units declined less in older compared with younger adults during 20-s contractions at
50% of MVC, but not at 20% MVC (12). They proposed that
the blunted response in discharge rate of the older subjects may be a
consequence of less PAP, but contractile properties were not measured
(12). The present study is the first to compare the acute
changes of motor unit and contractile properties after PAP in old
adults. The CC resulted in significant PAP as well as reduction in
motor unit discharge rate. However, unlike our previous results in
young men (24), the reduction in motor unit discharge rate was not significantly correlated with the magnitude of PAP. These findings indicate that the relationship between the acute changes in
motor unit discharge rate and PAP is not well matched in older adults.
Contractile properties and PAP.
The MVC was 41% lower than the values previously recorded in the young
men (24). Most of this strength difference probably reflects age-related muscle atrophy, rather than any major impairment in the ability to fully activate the elbow extensors (23).
The initial Pt of the old men in the present study was 73% lower, but
CT and 1/2 RT were not significantly different, compared with young
adults (24). Others have also reported minimal age-related difference in twitch duration of the elbow extensors or flexors (8, 21, 29). In contrast, a number of investigators found that the twitch duration is prolonged in distal muscles in older compared with younger subjects (3, 4, 7, 31, 32, 40).
The old men demonstrated significant PAP after the control 30% MVC
ramp-and-hold contraction (~20%) and 2 s after the CC (233 ± 30%). These values were similar to the level of PAP after the 30%
MVC (~20%) and 2 s after the CC (212 ± 53%) in young men
(24). Moreover, a similar amount of PAP (~240%) was
reported in the triceps brachii of 65- to 78-yr-old men after a 5-s
MVC, but no young subjects were studied (35). Thus it
seems that age does not impair the capacity for PAP in the triceps
brachii. In contrast to these findings, investigators previously
reported that PAP was 25-75% lower in the dorsiflexor and plantar
flexor muscles in older compared with younger adults (18, 34,
40). The relative maintenance of PAP in the triceps brachii
compared with the lower limb muscles with age may reflect differences
in habitual activity, although this has not been tested experimentally.
The maintenance of PAP in the triceps brachii with age may also be a
reflection of inherent differences in the aging of upper vs. lower limb
muscles. Others have shown that age-related differences of muscle size,
strength, twitch duration, and number of motoneurons were less in the
upper limb (or forelimb) than in the lower limb (or hindlimb) in humans
and animals (15, 17, 25, 29). Thus the contractile
properties and capacity for PAP (at least after a submaximal CC) in the
arm muscles seem to be less affected by age than the lower limb muscles.
Ramp-and-hold contractions before the CC.
Voluntary modulation of force depends primarily on the recruitment and
derecruitment of motor units and their pattern and frequency of
discharge (6). The mean discharge rate during the 10 (~12 Hz), 20 (~14 Hz), and 30% (~16 Hz) MVCs before the CC are
similar to the values recorded in the young men (24) and
to values recorded by others who used intramuscular electrodes (28, 39). In addition, the variability (CV) of
both discharge rate and force (i.e., steadiness) during the 2-s plateau
were relatively low (<15%), and the relative EMG activity of the
triceps brachii and biceps brachii during the contractions were similar to those of the young adults (24). Graves and co-workers
(14) also reported no age-related difference in force
steadiness (i.e., CV) or EMG activity of the agonist and antagonist
muscles during isometric contractions of the elbow flexors at
5-65% of the MVC.
Consistent with our findings, Howard et al. (19) reported
no age-related differences in motor unit discharge rate of the triceps
brachii or biceps brachii during 10-30% MVCs of the elbow extensors and flexors, respectively, although only one subject was over
70 yr of age. Similarly, motor unit discharge rate of the vastus
medialis muscle during submaximal and maximal (MVC) knee extensions was
not different between old (80 yr) and young men (38).
Conversely, an age-related reduction in motor unit discharge rate is
apparent in the elbow extensor muscles during higher intensity (>50%
MVC) contractions (21) and in more distal muscles at low
and high force levels (4, 12, 19, 22, 30, 32). Considering
the present and previous studies, it seems that age has minimal effect
on motor unit properties and force steadiness of proximal compared with
distal muscles, at least during moderate isometric contractions.
Ramp-and-hold contractions after the CC.
Although there was a reduction in the discharge rate of motor units
after the CC, the magnitude of the decrease (~1 Hz) was less than in
the young (~2 Hz) adults (P < 0.001, ANOVA)
(24). Additionally, few motor units demonstrated a
reduction >2 Hz in the old men, but over one-half of the units in the
young group declined by >2 Hz (Fig. 4).
It was anticipated that the old men would demonstrate less reduction in
motor unit discharge rate after the CC compared with the young men and
that this difference might be explained by an age-related decline in
PAP (12, 18, 34, 40). However, as described above, PAP of
the triceps brachii was not affected by age. Moreover, there was no
association between the magnitude of PAP and the reduction in discharge
rate after the CC in the old group, although a significant negative
correlation (r = 
0.74) was demonstrated in the young
group (24).
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Fig. 4.
Change in motor unit discharge rate (Hz) 10 s after
the CC relative to control levels during a 20% MVC in young
(A) and old (B) men. The mean reduction in
discharge rate in the old (1.1 ± 0.7 Hz, n = 28 motor units) was significantly less than the reduction in the young
(2.1 ± 1.0 Hz, n = 22 motor units) determined
in our previous study (24).
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The lower discharge rate observed in the young and old after the CC may
reflect a decrease in voluntary neural input to the motoneuron pool to
maintain the target force when PAP is prominent. This line of reasoning
is indirectly supported by the work of Hutton and colleagues
(20), who found that young subjects, devoid of visual
feedback of the target force, "overshoot" the target force after a
CC, and the magnitude of the force error covaried with the intensity of
the CC. A reduction in neural input to the motoneuron pool after the CC
could also result in a decrease in the number of motor units recruited
(i.e., derecruitment). However, in the few instances that motor unit
derecruitment was clearly observed, recruitment of new motor units
usually occurred. This suggests that there was some rotation among
different motor units during recovery. Although we cannot rule out the
possibility of derecruitment of motor units, this may not be a
significant compensatory strategy for PAP, at least under the current conditions.
In addition to possible changes in neural drive, the modulation of the
decrease in discharge rate to changes in PAP likely requires a
segmental feedback mechanism. For example, the smaller reduction in
discharge rate after the CC in the old compared with the young men may
also stem, in part, from reduced inhibitory influences of the
motoneuron pool, secondary to age-related decreases in presynaptic
inhibition (2, 9) and reflex sensitivity of muscle
(5). Less reduction occurred in the amplitude of the
soleus H-reflex during changes in body posture (26) and during vibration or electrical stimulation of the antagonist muscles in
old compared with young subjects (2, 9). Also, the
amplitude of the H-reflex, muscle stiffness, and stretch-induced
afferent activity are all lower after an isometric CC in young subjects (10, 16), but comparable experiments on older adults have not been done.
In summary, the old men demonstrated significant PAP of the muscle
twitch and a reduction in the discharge rate of motor units after the
CC. However, the magnitude of the reduction in discharge rate was less
than in young men (24), and there was no correlation between PAP and changes in discharge rate. These findings suggest that
rate coding may be less important in older adults for adjusting the
motor output subsequent to PAP.
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ACKNOWLEDGEMENTS |
We are grateful to the subjects who participated in this study.
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FOOTNOTES |
We acknowledge the support of the Natural Sciences and Engineering
Research Council of Canada.
Address for reprint requests and other correspondence:
S. J. Garland, School of Physical Therapy, Elborn College,
Univ. of Western Ontario, London, ON, Canada N6G 1H1 (E-mail:
jgarland{at}uwo.ca).
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
July 19, 2002;10.1152/japplphysiol.00414.2002
Received 10 May 2002; accepted in final form 15 July 2002.
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