Practice reduces motor unit discharge variability in a
hand muscle and improves manual dexterity in old
adults
Kurt W. Kornatz, Evangelos A. Christou and Roger M. Enoka
J Appl Physiol 98:2072-2080, 2005. First published Feb 3, 2005; doi:10.1152/japplphysiol.01149.2004
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[Abstract] [Full Text] [PDF]
J Appl Physiol 98: 2072–2080, 2005.
First published February 3, 2005; doi:10.1152/japplphysiol.01149.2004.
Practice reduces motor unit discharge variability in a hand
muscle and improves manual dexterity in old adults
Kurt W. Kornatz, Evangelos A. Christou, and Roger M. Enoka
Department of Integrative Physiology, University of Colorado, Boulder, Colorado
Submitted 12 October 2004; accepted in final form 28 January 2005
contraction type; first dorsal interosseus; manual dexterity; steadiness;
strength training
AT ABOUT THE AGE OF 60 YR, humans exhibit a progressive yet
variable decline in movement capabilities that is induced by
adaptations in the neuromuscular system. One often-cited example of these adaptations is the decline in muscle strength,
which includes a major role for apoptosis of spinal motor
neurons and incomplete reinnervation of muscle fibers by
surviving motor neurons (10). In addition to the adaptations in
motor unit morphology, however, movement capabilities are
challenged by adaptations in the biophysical properties of the
motor neurons, the loss of cortical neurons (14, 21), and a
decline in the transmission efficacy over supraspinal and reflex
pathways (7).
One possible consequence of changes in motor neuron
properties and the synaptic inputs they receive is an increase in
the variability of motor unit discharge rate, which appears to be
Address for reprint requests and other correspondence: K. W. Kornatz, Dept.
of Kinesiology, Arizona State Univ., Tempe, AZ 85287 (E-mail: [email protected]).
2072
attributable to the amount of synaptic noise that is imposed on
the membrane potential of the motor neuron during the afterhyperpolarization trajectory (4, 34). Although increased discharge rate variability of motor units does not appear to
influence maximal strength, it does contribute significantly to
the fluctuations in muscle force during submaximal contractions (29, 35). The functional significance of the increased
fluctuations in muscle force is that it impairs the ability of an
individual to exert a constant trajectory (6) or to move the limb
accurately to a desired target (19). Experimental evidence from
the first dorsal interosseus muscle during the performance of
isometric, shortening, and lengthening contractions demonstrated that older adults have larger fluctuations in motor output
compared with young adults (17, 25) and that these fluctuations
were associated with greater variability in motor unit discharge
rate (29). Computer simulations further supported these experimental findings (35, 45). For example, when the coefficient of
variation for motor unit discharge increased from 10 to 40%,
which corresponds to the range of values often observed
experimentally (15, 35), there was a parallel increase in the
coefficient of variation in the simulated force.
Auspiciously, the amplitude of the force fluctuations can be
reduced through practice and strength training in healthy subjects (22, 25, 26, 30) and patient populations (2). For example,
Keen and colleagues (25) demonstrated that strength training
of the first dorsal interosseus muscle is an effective intervention to reduce the fluctuations in the abduction force exerted by
the index finger in healthy old adults. Subsequently, it was
shown that the training reduces the fluctuations during anisometric (shortening and lengthening) contractions of the same
muscle and that practice is as effective as strength training
(30). Reductions in force fluctuations through training have
also been related to improvements in hand function of older
individuals (41).
The above observations suggest a hypothesis that variability
of motor unit discharge is a significant contributor to the
impaired ability of older adults to perform steady muscle
contractions (29, 45) and the capacity of both strength training
and practice of a task to lower the enhanced fluctuations
exhibited by older adults (25, 30). The present study used an
intervention that required the older adults to practice the task
for 2 wk followed by strength training for 4 wk to identify the
relative contributions of practice and strength training to improvements in the fluctuations of motor output. The purpose of
the study was to examine the association between discharge
rate variability and the fluctuations in motor output by reducing
the fluctuations and examining the effects on the discharge rate
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Kornatz, Kurt W., Evangelos A. Christou, and Roger M. Enoka.
Practice reduces motor unit discharge variability in a hand muscle and improves manual dexterity in old adults. J Appl Physiol 98: 2072–2080, 2005.
First published February 3, 2005; doi:10.1152/japplphysiol.01149.2004.—A
steadiness-improving intervention was used to determine the contribution of variability in motor unit discharge rate to the fluctuations in
index finger acceleration and manual dexterity in older adults. Ten
healthy and sedentary old adults (age 72.9 ⫾ 5.8 yr; 5 men) participated in the study involving abduction of the left index finger. Single
motor unit activity was recorded in the first dorsal interosseus muscle
before, after 2 wk of light-load training (10% maximal load), and after
4 wk of heavy-load training (70% maximal load). As expected, the
light-load training was effective in reducing the fluctuations in index
finger acceleration during slow shortening (0.25 ⫾ 0.12 to 0.13 ⫾
0.08 m/s2) and lengthening contractions (0.29 ⫾ 0.10 to 0.14 ⫾ 0.06
m/s2). Along with the decline in the magnitude of the fluctuations,
there was a parallel decrease in the coefficient of variation for
discharge rate during both contraction types (33.8 ⫾ 6.8 to 25.0 ⫾
5.9%). The heavy-load training did not further improve either the
fluctuations in acceleration or discharge rate variability. Furthermore,
the manual dexterity of the left hand improved significantly with
training (Purdue pegboard test: 11 ⫾ 3 to 14 ⫾ 1 pegs). Bivariate
correlations indicated that the reduction in fluctuations in motor
output during shortening (r2 ⫽ 0.24) and lengthening (r2 ⫽ 0.14)
contractions and improvement in manual dexterity (r2 ⫽ 0.26) was
directly associated with a decline in motor unit discharge rate variability. There was a strong association between the fluctuations in
motor output and manual dexterity (r2 ⫽ 0.56). These results indicate
that practice of a simple finger task was accompanied by a reduction
in the discharge rate variability of motor units, a decrease in the
fluctuations in motor output of a hand muscle, and an improvement in
the manual dexterity of older adults.
PRACTICE REDUCES VARIABILITY
variability of motor units. The results indicated that reductions
in motor unit discharge rate variability, primarily associated
with the light-load training, were accompanied by lower fluctuations in motor output and improved manual dexterity of old
adults. Some of these data have been presented in abstract form
(27).
METHODS
Ten old subjects (mean ⫾ SD, 72.9 ⫾ 5.8 yr; range, 65– 84 yr)
consisting of 5 men and 5 women volunteered for the study. All study
participants appeared healthy with normal hand function, and were not
using any medications known to influence neuromuscular function. In
addition, all subjects reported being right handed [Edinburgh Handedness Inventory (37)] and moderately active on a daily basis [Paffenbarger Physical Activity Questionnaire (38)]. The Human Research
Committee at the University of Colorado in Boulder approved all
experimental procedures.
Experimental Arrangement
Fig. 1. Position of the hand during the training and experimental sessions. The
left hand was placed palm down with the index finger and thumb extended. A
load was applied in the adduction direction, and an accelerometer was placed
on the thumb side of the index finger.
J Appl Physiol • VOL
ibrated over a 10° range of motion from 5° of index finger abduction
for each subject in every session. The LVDT was placed in series with
the finger splint on one end and a mass on the other. A miniature
piezoresistive accelerometer (model 7265A-HS, Endevco, San Juan
Capistrano, CA) secured to the lateral side of the finger splint at the
proximal interphalangeal joint was used to measure acceleration in the
adduction-abduction plane.
For the single motor unit recordings, electrodes were custom
fabricated using three Formvar-insulated, stainless steel wires (50-␮m
diameter; California Fine Wire, Grover Beach, CA), fixed together
with medical-grade cyanoacrylate glue. A custom coiling apparatus
(29) was used to coil the recording end of the fine wires around a
mandrel (diameter of 0.13 mm) for ⬃3 mm. The wires were then
threaded through a single-use, 27-gauge hypodermic needle, and a
barb of ⬃2 mm in length was created at the tip of the recording end.
The wires were cut perpendicularly with surgical grade scissors to
expose the recording surfaces. The electrode was inserted into the first
dorsal interosseus muscle with the hypodermic needle; up to two
electrodes were inserted in each experiment. Recordings were obtained from two wires within each electrode; the third wire was used
as an alternative bipolar configuration to optimize the recording
quality. The possibility of recording from the same motor unit with the
two electrodes in one experiment was minimized by positioning the
electrodes in different parts of the muscle, making large (5 mm)
adjustments in the location of the electrode in the search for single
motor units and by comparing the behavior of the two motor units.
The signals were amplified (1,000 –2000⫻) and band-pass filtered
(0.2– 8 kHz), displayed on an oscilloscope, and stored on tape (Sony
PC 116 DAT recorder, Sony Magnescale, Montvale, NJ). Motor unit
potentials were detected online using an amplitude window discriminator (DIS 1, BAK Electronics, Rockville, MD).
Experimental Procedures
Each subject participated in a familiarization session and three
experimental sessions. In the familiarization session, subjects received
written and oral descriptions of the project, watched a visual demonstration of the protocol, and were given practice trials of the experimental task. The three experimental sessions included an initial
session before the onset of training, a second session after 2 wk of
light-load training, and a third session after an additional 4 wk of
heavy-load training. Therefore, each subject acted as his or her own
control. Four experimental measurements were made in these sessions: 1) manual dexterity, a test of the ability to work quickly and
precisely with the hands and fingers; 2) recruitment threshold, determination of the minimal inertial load that had to be supported by an
isometric contraction of the first dorsal interosseus for the isolated
motor unit to discharge action potentials repetitively; 3) anisometric
task, shortening and lengthening contractions of the first dorsal interosseus muscle to lift and lower a light inertial load; and 4) onerepetition maximum (1-RM) load, identification of the maximal load
that could be lifted by a shortening contraction of the first dorsal
interosseus muscle. The discharge of motor units was recorded during
the anisometric task. Each experimental session lasted ⬃1.5 h.
Manual dexterity. The manual dexterity of the subjects was assessed at the beginning of every experimental session, before the
insertion of the fine-wire electrode, with the Purdue pegboard test
(Lafayette Instrument, Lafayette, IN). This standardized, reliable (9)
means of evaluating hand and finger function involved retrieving
small metal pegs from a cup and placing them in a line of holes. The
number of pegs placed in the holes within 30 s was recorded. The test
was repeated twice with each hand, and an average value for each
hand was determined.
Recruitment threshold. This measurement was denoted as the
minimal load at which a motor unit discharged action potentials
repetitively. To determine this load, the subject attempted to maintain
a constant finger position (5° of abduction) with the help of a target
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The experiments were performed on the left hand (nondominant).
Each subject was comfortably seated in an upright position facing a
17-in. computer monitor, which was positioned 1.5 m in front of the
subject at eye level. The monitor was used to display the position of
the index finger for the subject. Both arms were slightly abducted and
flexed to ⬃90° at the elbow. The forearms and hands were supported
in the prone position by platforms with the right hand resting comfortably. The left hand was placed in a manipulandum with the third
to fifth digits flexed and secured around a handle. The left index finger
was kept extended with a splint secured to the lateral aspect of the
finger, and thumb extension was maintained by a support (Fig. 1).
This arrangement allowed abduction of the index finger about the
metacarpophalangeal joint in the horizontal plane, a movement produced almost exclusively by contraction of the first dorsal interosseus
muscle (32).
The displacement of the index finger about the metacarpophalangeal joint was detected with a low-friction, linear variable displacement transducer (LVDT; Novotechnik, Stuttgart, Germany) and cal-
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PRACTICE REDUCES VARIABILITY
Steadiness Training
Subjects performed steadiness training by lifting and lowering
loads under identical conditions as in the experimental session. The
LVDT was calibrated over a 10° range of motion before all training
sessions, and subjects attempted to match the experimental template
by displacing the index finger. There were 5 s of rest after each trial.
All training was done in the laboratory under supervision, where
emphasis was placed on performing steady contractions. Training was
executed three times every week and consisted of 6 sets of 10
repetitions for a total of 60 trials per training session. Verbal encouragement was provided during the training sessions. The training
involved a light load (10% 1-RM) for the first 2 wk and then a heavy
load (⬃70% 1-RM) for the final 4 wk. 1-RM load was tested every
week, and training loads were adjusted accordingly. On average, each
training session lasted ⬃30 min.
Data Analysis
The data collected during the experiments were stored on tape and
later downloaded to a computer and analyzed offline. The sampling
rate was 200 samples/s for the position and acceleration signals and
20,000 samples/s for the single motor unit recordings.
Single motor unit discharges were identified on the basis of action
potential shape and amplitude. A computerized, spike-sorting algorithm (Spike2, Cambridge Electronic Design, Cambridge, UK) assisted in this endeavor. The interspike intervals were examined for
every trial, and those trials that contained abnormally short or long
interspike intervals due to discrimination error were reanalyzed on a
spike-by-spike basis. Motor units exhibited a tendency for a systematic increase or decrease in the discharge rate during shortening and
lengthening contractions. Therefore, the slope of the linear regression
line for the change in the interspike interval over time was subtracted
from the data to remove the trend. Subsequently, the SD and coefficient of variation for the interspike intervals were determined.
For the trials in which single motor unit discharges were discriminated, the fluctuations in motor output were measured with an
accelerometer attached to the lateral surface of the proximal interphangeal joint of the index finger. Each anisometric trial was analyzed
by marking the beginning, middle, and end of the movement to
indicate the lifting and lowering phases of the task. The SD of the
acceleration for both the whole phase (6 s) and middle 4 s of each
phase was determined and used to quantify the fluctuations in motor
output.
Statistical Analysis
The dependent variables were the maximal load lifted (1-RM load);
the Purdue pegboard test score; the SD of acceleration; the mean, SD,
and coefficient of variation for the interspike intervals of motor unit
discharge; and the slope of the mean interspike intervals during each
contraction.
The effect of training on strength (1-RM load) and manual dexterity
(Purdue pegboard test score) were assessed with one-way, repeated-
Fig. 2. Representative recordings during
anisometric contractions performed before
(left) and after (right) steadiness training. First
trace: instantaneous discharge rate. Second
trace: single motor unit recording. Third
trace: acceleration signal. Fourth trace: position of the index finger with the initial
position denoting 5° of abduction. Before
training, mean discharge rate was 9.7 pulses/s (pps) for the shortening contraction and
9.1 pps for the lengthening contraction, and
the mean coefficient of variation (CV) for
discharge rate was 35.2% for the shortening
contractions and 37.9% for the lengthening
contractions. After training, mean discharge
rate was 13.7 pps for the shortening contraction and 11.2 pps for the lengthening contraction, and the mean CV for discharge rate
was 23.4% for the shortening contraction
and 18.7% for the lengthening contraction.
J Appl Physiol • VOL
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line on the feedback monitor, while small increments of mass (ⱖ5 g)
were added to load the index finger in the direction of adduction. Mass
was added until an electrode detected the discharge of action potentials from one motor unit. The load was adjusted further to ensure
repetitive discharge of the unit without saturating the signal with
activity from neighboring motor units.
Anisometric task. After a rest period, subjects lifted and lowered
the same load identified by the recruitment threshold by using abduction-adduction movements of the index finger that were produced with
shortening and lengthening contractions of the first dorsal interosseus.
Subjects were encouraged to match index finger displacement to a
triangular template shown on the monitor; they were required to
produce slow, constant-velocity (1.7°/s) abduction-adduction movements over a 10° range of motion (Fig. 2). Each subject raised the load
during 6 s of abduction (shortening contraction) and lowered the load
during 6 s of adduction (lengthening contraction). Subjects repeated
this movement five times. The experimenters carefully monitored the
hand to ensure the movement was limited to abduction of the index
finger about the metacarpophalangeal joint. Only those trials where
motor units discharged repetitively throughout both the shortening
and lengthening phases of the anisometric task were accepted for
analysis. As well, only those trials in which the discharge of a single
motor unit could be measured were evaluated for steadiness. When a
motor unit could not be reliably followed through both phases of
movement, the recruitment threshold and anisometric tasks were
repeated or attempts were made to follow the discharge of another
motor unit. To record from a different motor unit, the pairs of
recording wires were either switched or pulled to a more superficial
location, and the recruitment threshold task was repeated.
1-RM load. At the conclusion of the experimental sessions, the
wires were removed, and the strength of the first dorsal interosseus
muscle was determined as the 1-RM load. The 1-RM load was the
maximal mass that could be lifted no more than one time without any
deviation in the required finger trajectory. The range of motion (5–15°
of abduction) and speed of movement were consistent with the
anisometric task in which motor units were recorded. The experimenters determined the initial load, and successive masses were added in
increments of 0.2 kg until the subjects were not able to lift the load.
At that point, adjustments were made down to the 10-g level until the
maximal load that could be lifted by a subject was identified. Subjects
received 2 min of rest between each 1-RM attempt.
PRACTICE REDUCES VARIABILITY
measures ANOVA (3 training sessions). The effect of training and
contraction type on steadiness (SD of acceleration) and motor unit
activity (mean, SD, coefficient of variation, and slope of discharge
trend) was assessed with a repeated-measures two-way ANOVA (2
contraction types ⫻ 3 time points).
Bivariate linear regressions were performed to examine the association between the coefficient of variation for motor unit discharge
and the SD of acceleration, the association between the change in the
coefficient of variation for motor unit discharge and the change in
Purdue pegboard test scores, the association between the change in the
SD of acceleration and the change in Purdue pegboard test scores, and
the association between the change in 1-RM strength and the change
in Purdue Pegboard scores. The ␣ level for all statistical tests (except
post hoc analysis) was set at 0.05, and all significant interactions were
examined with appropriate post hoc analyses; these included dependent t-tests with Bonferroni corrections to locate differences between
the shortening and lengthening contractions and differences between
sessions. Unless otherwise stated, means ⫾ SD are reported in the
text, whereas the figures depict means ⫾ SE.
The 1 RM of the men (1.03 ⫾ 0.57 kg) and women (0.91 ⫾
0.36 kg) was similar before training (P ⫽ 0.62) and increased
progressively over the course of the training (Fig. 3A) with
Fig. 4. The standard deviation (SD) of acceleration declined with training for
both the shortening and lengthening contractions. The SD of the acceleration
was reduced after 2 wk of practice, but no further reductions were observed
after the additional 4 wk of strength training. The SD of acceleration was
greater at all three time points for the lengthening contractions compared with
the shortening contractions. Values are means ⫾ SE. *P ⬍ 0.001 compared
with week 0 for both types of contractions. †P ⬍ 0.001 for contraction type.
significant improvements from week 0 (from 0.96 ⫾ 0.43 kg)
to week 2 (1.38 ⫾ 0.49 kg; P ⬍ 0.001) and week 6 (1.75 ⫾ 0.39
kg; P ⬍ 0.001).
Manual Dexterity
All subjects achieved a higher score on the Purdue pegboard
test (P ⫽ 0.002) for the right hand (13 ⫾ 3 pegs) compared
with the left hand (11 ⫾ 3 pegs) at the beginning of the study.
Furthermore, the score for the women with the left hand (12 ⫾
1 pegs) was greater than that for the men (9 ⫾ 3 pegs) at the
beginning of the study (P ⫽ 0.041). The score for the right
hand did not change (P ⫽ 0.116) over the 6 wk of training.
However, the score for the left hand improved significantly,
with the greatest changes occurring during the final 4 wk of
training (P ⫽ 0.004). The left and right hands achieved similar
scores on the Purdue pegboard test at week 6. There was a
weak, yet significant relation between improvements in 1-RM
strength and improvements in Purdue pegboard test scores
(r2 ⫽ 0.17, P ⫽ 0.03).
Steadiness Improvements
Fig. 3. Changes in strength and manual dexterity over the 6 wk of training.
Values are means ⫾ SE. A: one-repetition maximum (1-RM) load increased
progressively throughout the training. *P ⬍ 0.001 compared with week 0.
†P ⬍ 0.001 compared with week 2. B: the scores on the Purdue pegboard test
improved for the hand used in training (left) but not the other hand (right).
**P ⫽ 0.002 left hand compared with right hand. ‡P ⫽ 0.004 compared with
week 0 for the left hand only.
J Appl Physiol • VOL
The intervention decreased the fluctuations in acceleration
during shortening and lengthening contractions (Fig. 4). The
data for the full 6 s and the middle 4 s of each contraction were
similar, and, therefore, only the 6-s data are reported. The SD
of acceleration was greater for the lengthening contractions
(0.286 ⫾ 0.102 m/s2; P ⬍ 0.001) compared with the shortening
contractions (0.245 ⫾ 0.124 m/s2) and remained so throughout
training. The SD of acceleration decreased by similar amounts
at week 2 for both the shortening (0.125 ⫾ 0.077 m/s2) and
lengthening (0.140 ⫾ 0.056 m/s2) contractions (P ⬍ 0.001).
There was no change in the SD of the acceleration from week
2 to week 6 (shortening: 0.116 ⫾ 0.084 m/s2, lengthening:
0.136 ⫾ 0.045 m/s2).
Motor Unit Discharge
Discharge rates were determined for 111 motor units in the
three experimental sessions (week 0: 38 units; week 2: 39 units;
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RESULTS
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PRACTICE REDUCES VARIABILITY
Fig. 6. Association between the SD of index finger acceleration and the
variability in motor unit discharge rate. The SD of the acceleration was
positively correlated with the coefficient of variation for discharge rate for both
shortening (A; r2 ⫽ 0.24) and lengthening contractions (B; r2 ⫽ 0.14). The data
comprise 108 motor units recorded during 3 experimental sessions. Each data
point corresponds to an average value over multiple 6-s anisometric contractions.
contractions (30 ⫾ 9 ms; P ⫽ 0.001) and remained so throughout the training (week 2: 29 ⫾ 6 vs. 25 ⫾ 8 ms; week 6: 31 ⫾
9 vs. 25 ⫾ 9 ms; P ⬍ 0.001). There was a reduction in the SD
for both contraction types from week 0 to week 2 (P ⬍ 0.001)
with no further statistically significant (P ⬎ 0.05) changes
from week 2 to week 6. The coefficient of variation for
discharge rate was similar for both shortening and lengthening
contractions in all three experimental sessions (Fig. 5B). Similar to SD, the coefficient of variation declined significantly
from week 0 (33.8 ⫾ 6.8%) to week 2 (25 ⫾ 5.9%; P ⬍ 0.001).
There were no further statistically significant changes in the
coefficient of variation for either contraction type from week 2
to week 6.
Association Between Discharge Rate Variability
and Steadiness
Fig. 5. Changes in motor unit discharge rate during the 6-week intervention.
Values are means ⫾ SE. A: mean discharge rate remained constant across
sessions for shortening and lengthening contractions. Interspike intervals were
converted to frequency for ease of interpretation. *P ⬍ 0.001 for contraction
type. B: there was no difference in the mean CV for discharge rate for
shortening and lengthening contractions as it declined from week 0 to week 2
(*P ⬍ 0.001) with no further change at week 6.
J Appl Physiol • VOL
There was a weak yet significant positive correlation between the SD of acceleration and the coefficient of variation of
interspike intervals for both the shortening (r2 ⫽ 0.24; P ⫽
0.003) and lengthening (r2 ⫽ 0.14; P ⫽ 0.002) contractions
(Fig. 6). Approximately 20% of the variability in the SD of
acceleration was explained from the variability of single motor
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week 6: 34 units). The absolute load at which motor units were
recorded was similar for the three experimental sessions; the
mean load was 97.2 ⫾ 34.3, 72.3 ⫾ 22.4, and 109.2 ⫾ 62.6 g
for week 0, week 2, and week 6, respectively. Typically, motor
units displayed a systematic decrease in mean interspike interval during the shortening contractions and an increase during
the lengthening contractions. Therefore, the slope of a regression line was subtracted from the data to remove the trend
before the variability of motor unit discharge was calculated.
Although the trend differed with contraction type (shortening:
6.5 ⫾ 6.4 ms/s, lengthening: 10.7 ⫾ 2.9 ms/s; P ⬍ 0.001), it
was similar for all three sessions for each contraction type.
The mean, SD, and coefficient of variation for interspike
interval were calculated for each trial, and these values were
averaged over the trials in which the motor unit was recorded
(mean 4 ⫾ 1 trials). Mean interspike interval was longer for the
lengthening contractions (115 ⫾ 18 ms) compared with the
shortening contractions (93 ⫾ 18 ms; P ⬍ 0.001), which
corresponded to 9.1 ⫾ 2.1 pulses/s (pps) and 11.2 ⫾ 2.2 pps,
respectively. Mean discharge rate did not significantly change
across the three experimental sessions (Fig. 5A).
The SD for interspike interval was initially greater for the
lengthening contractions (40 ⫾ 9 ms) than for the shortening
PRACTICE REDUCES VARIABILITY
2077
the fluctuations in acceleration, but there were no further
improvements with the subsequent 4 wk of heavy-load training, which is consistent with prior observations (30). The novel
finding of the present study, however, was that a reduction in
the variability of discharge rates for motor units in a hand
muscle contributed to the improvement of manual dexterity in
old adults. Specifically, the variability in motor unit discharge
rate decreased in parallel with the fluctuations in index finger
acceleration, and the reductions in discharge rate variability
were significantly correlated with the decline in the SD of
index finger and consequent improvements in a functional test
of manual dexterity.
Practice vs. Strength Training
unit discharge. Furthermore, data obtained from 9 of the 10
subjects revealed a moderate significant negative correlation
(r2 ⫽ ⫺0.26; P ⫽ 0.005) between the change in coefficient of
variation for interspike interval (combined for both the shortening and lengthening contractions) and the changes in manual
dexterity scores (Fig. 7B). Thus ⬃26% of the improvement in
manual dexterity was explained by the reduction in the variability of single motor unit discharge. There was a stronger
significant negative correlation (r2 ⫽ ⫺0.56; P ⬍ 0.001)
between the change in SD of index finger acceleration with
training and the change in manual dexterity scores (Fig. 7A).
Approximately 56% of the improvement in manual dexterity
could be explained by the reduction in the SD of index finger
acceleration.
DISCUSSION
The purpose of this study was to assess the contribution of
motor unit discharge rate variability to the fluctuations in motor
output of the index finger and manual dexterity in older adults
during an intervention that involved light-load (practice) and
heavy-load training. The 2 wk of light-load training reduced
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Fig. 7. Functional significance of the fluctuations in motor output and CV for
discharge rate. The improvements in manual dexterity (Purdue pegboard test
score) were associated with declines in both the SD of index finger acceleration
(A; r2 ⫽ 0.56) and the variability in motor unit discharge rate (B; r2 ⫽ 0.26).
Data were obtained from 9 of 10 subjects, and each point denotes the average
value obtained from 1 subject for all trials and experimental sessions for either
the shortening or lengthening contractions.
Six weeks of training resulted in significant improvements in
strength, as indicated by an increase in 1-RM load. The initial
2 wk of light-load training was equally effective in increasing
the strength of the first dorsal interosseus muscle as the
following 4 wk of heavy-load training. The time course of
these improvements in strength was similar to that reported in
earlier training studies involving abduction of the index finger
(2, 25, 30). For example, Laidlaw and colleagues (30) observed
increases of almost 23% in 1-RM strength of the first dorsal
interosseus muscle after 4 wk of training, which compares with
a 44% increase in 1-RM load after the first 2 wk of practice and
a further increase of 27% after 4 wk of strength training in the
present study. Because improvements in strength occurred so
rapidly and with light loads, it is likely that the gains in
strength were due to an improved ability of the nervous system
to activate the involved muscles (1, 11).
The neural adaptations that contribute to rapid increases in
strength for the first dorsal interosseus muscle likely involve
the discharge characteristics of motor units within a muscle and
the coordination of muscles involved in establishing the posture of the body during the task. Although we did not measure
motor unit activity during the 1-RM task because of technical
limitations, it has been found that the maximal discharge rate
of motor units, which is reduced with aging (23), can be
increased with strength training (39). Even in young adults,
peak discharge rates of motor units do not appear to occur on
the plateau of the force-frequency relation (16, 33) and adjustments in discharge rate can have a profound effect on strength
activities (46). The strength gains can also be influenced by
adjustments in the activation of support musculature (31, 42).
Although we purposely chose abduction of the index finger due
to the relative simplicity of the action, a muscle can only exert
an effect on its surroundings when the body can provide the
relevant reaction forces (24, 36). For example, the inability to
match the maximal voluntary contraction (MVC) force by
electrical stimulation of a muscle in vivo (8, 12) is likely due,
at least in part, to the difference in postural support between the
two conditions. Therefore, changes in the maximal force exerted in the abduction direction by the index finger depends not
only on the contraction of the first dorsal interosseus muscle
but also on the postural contractions of other support musculature.
Consistent with findings in other studies involving older
subjects and light loads (3, 18, 29), the lengthening contractions initially exhibited greater fluctuations in acceleration.
After 2 wk of practice, however, the fluctuations decreased for
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PRACTICE REDUCES VARIABILITY
both contraction types while still maintaining differences in the
SD of acceleration between the shortening and lengthening
contractions. Because of the rapid adaptation (2 wk), it is likely
that these improvements were also mediated by changes in the
activation signal generated by the nervous system (6).
Motor Unit Discharge Characteristics
J Appl Physiol • VOL
Training and Changes in Discharge Rate Variability
In addition to the observation of associations between discharge rate variability, fluctuations in index finger acceleration,
and manual dexterity, the present study also demonstrated that
the training intervention had an influence on the variability in
motor unit discharge rate. Reductions in discharge rate variability, both the SD and coefficient of variation, occurred over
the first 2 wk of light-load training for both the shortening and
lengthening contractions. No further improvements were detected during the subsequent 4 wk of heavy-load training,
despite continued increases in muscle strength. Thus the improved capacity of motor units to discharge action potentials
regularly was related more to practice of the task, rather than
the strength gains achieved by the muscle.
The time between successive action potentials discharged by
a motor neuron depends on the recovery of its excitability after
the preceding action potential (40). The dominant factor influencing this recovery is the prolonged afterhyperpolarization
potential that occurs after each action potential, which is due to
the fast rise and slow decline of a calcium-dependent potassium conductance (43, 47). As a result, the afterhyperpolarization comprises a rapid shift of the membrane potential away
from threshold and a gradual recovery back toward threshold.
Generation of the next action potential occurs when the threshold is reached and depends, therefore, on the rate of change in
the membrane potential during the afterhyperpolarization and
the magnitude of the instantaneous fluctuations (or synaptic
noise) in the potential (4, 34). Consequently, one or more of
these mechanisms must mediate the observed reduction in
discharge rate variability. Because the effect was observed in a
large sample of motor units, the adaptation may have been
evoked by a broadly acting mechanism, such as descending
monoaminergic input from the brain stem (20) or a reduction of
synaptic noise caused by training-related adaptations in afferent input.
Functional Significance
The ability to reach, grasp, manipulate, and transport objects
is critical to performing activities of daily living, and, therefore, the Purdue pegboard test is an appropriate functional
assessment of hand control (9). Initially, performance on the
Purdue pegboard test was better for the right hand than for the
left hand and can be attributed to the degree of use and comfort
subjects exhibit with their dominant hand (all subjects reported
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In an earlier study that used a similar experimental arrangement and task (29), old adults exhibited greater fluctuations in
position and greater variability in motor unit discharge rate
than young adults during anisometric contractions. It also has
been demonstrated, in young women, during force matching to
a sinusoidal target that the accuracy of force production with
the first dorsal interosseus muscle is highly dependent on
discharge rate variability (26). The findings of the present
study demonstrated a weak association between the fluctuations in acceleration and variability of motor unit discharge
rate. The relation was characterized by the parallel declines in
discharge rate variability and the SD of acceleration fluctuations in response to training in individual subjects, as well as
by the correlations between the two variables when all the
experimental sessions were combined.
Although the observed associations between the fluctuations
in acceleration and discharge rate variability were statistically
weak, experimental limitations likely masked the magnitude of
the effect. Studies that combine experimental measurements
and computer modeling underscore the functional significance
of discharge rate variability. When experimentally measured
values for discharge rate variability were included in the
model, the variation in force fluctuations from 2 to 95% MVC
force was statistically similar to that measured experimentally
(35). Importantly, this result was achieved by manipulating
discharge rate variability of the entire motor unit population. In
contrast, the present study compared the discharge rate variability of a single motor unit with the fluctuations in motor
output due to the activity of many motor units. Furthermore,
the discharge was recorded with the motor unit operating close
to its recruitment threshold when the coefficient of variation for
discharge rate was the greatest and likely unrepresentative of
the average discharge rate variability for all the active motor
units. Taken together, these studies provide compelling evidence that the variability in motor unit discharge has a strong
influence on the fluctuations in motor output during steady
contractions.
There were no changes in the mean discharge rate for each
contraction type across the three sessions. The load supported
during the anisometric contractions was set to ensure a minimal
repetitive discharge rate for the isolated motor unit during both
the shortening and lengthening contractions. Discharge rate,
however, changed during each contraction and differed between the two contraction types. The systematic change in
discharge rate during each contraction was likely due to the
length-tension properties of the muscle rater than changes in
the length of the moment arm for first dorsal interosseus
relative to metacarpophalangeal joint of the index finger
throughout the range in motion. Because the moment arm is
maximal when the finger is fully abducted (5), the moment arm
increased during the shortening contraction as muscle length
decreased. The converse occurred during the lengthening contractions. Consequently, the change in discharge rate during
each contraction type complemented the change in muscle
length rather than the change in moment arm.
Mean discharge rate also differed for the two types of
contractions, as observed previously (28, 29, 44). Two factors
contributed to the lower mean discharge rates during the
lengthening contractions. First, muscles are able to exert a
greater force during lengthening contractions compared with
shortening contractions (13, 48). Second, the net muscle torque
must exceed the load torque to lift the load with a shortening
contraction, whereas the net muscle torque must be less than
the load torque to lower the load with a lengthening contraction. Therefore, the net muscle torque during the lengthening
contractions must have been less than that for the shortening
contractions, which must have involved lesser motor unit
activity.
PRACTICE REDUCES VARIABILITY
ACKNOWLEDGMENTS
The authors are grateful for contributions by Joel Enoka and Michael
Pascoe (training and analysis), Kevin Keenan, and Carol Mottram (analysis
programming).
Present address of K. W. Kornatz: Dept. of Kinesiology, Arizona State
Univ., Tempe, AZ 85287.
GRANTS
This study was supported by National Institute on Aging Award AG-09000
(to R. M. Enoka) and Minority Supplement PA-99-104 (to K. W. Kornatz).
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