Department of Kinesiology and Applied Physiology, University of Colorado, Boulder, Colorado 80309-0354
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ABSTRACT |
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Semmler, John G., Julie W. Steege, Kurt W. Kornatz, and Roger M. Enoka. Motor-Unit Synchronization Is Not Responsible for Larger Motor-Unit Forces in Old Adults. J. Neurophysiol. 84: 358-366, 2000. Motor-unit synchronization, which is a measure of the near simultaneous discharge of action potentials by motor units, has the potential to influence spike-triggered average force and the steadiness of a low-force isometric contraction. The purpose of the study was to estimate the contribution of motor-unit synchronization to the larger spike-triggered average forces and the decreased steadiness exhibited by old adults. Eleven young (age 19-30 yr) and 14 old (age 63-81 yr) adults participated in the study. Motor-unit activity was recorded with two fine-wire intramuscular electrodes in the first dorsal interosseus muscle during isometric contractions that caused the index finger to exert an abduction force. In a separate session, steadiness measurements were obtained during constant-force isometric contractions at target forces of 2.5, 5, 7.5, and 10% of the maximum voluntary contraction (MVC) force. Mean (±SD) motor-unit forces measured by spike-triggered averaging were larger in old (15.5 ± 12.1 mN) compared with young (7.3 ± 5.7 mN) adults, and the differences were more pronounced between young (8.7 ± 6.4 mN) and old (19.9 ± 12.2 mN) men. Furthermore, the old adults had a reduced ability to maintain a steady force during an isometric contraction, particularly at low target forces (2.5 and 5% MVC). Mean (±SD) motor-unit synchronization, expressed as the frequency of extra synchronous discharges above chance in the cross-correlogram, was similar in young [0.66 ± 0.4 impulses/s (imp/s); range, 0.35-1.51 imp/s; 53 pairs) and old adults (0.72 ± 0.5 imp/s; range, 0.27-1.38 imp/s; 56 pairs). The duration of synchronous peaks in the cross-correlogram was similar for each group (~16 ms). These data suggest that motor-unit synchronization is not responsible for larger spike-triggered average forces in old adults and that motor-unit synchronization does not contribute to the decreased steadiness of low-force isometric contractions observed in old adults.
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INTRODUCTION |
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When performing submaximal
contractions with hand, arm, and leg muscles, old adults have a reduced
ability to maintain a steady force (Galganski et al.
1993; Graves et al. 2000
; Laidlaw et al. 2000
; Tracy et al. 2000
). Fluctuations in the
force exerted during a sustained submaximal contraction are
attributable to the degree of fusion in the force contributed by the
most recently recruited motor units (Christakos 1982
).
Because the peak-to-peak force in the unfused contractions of single
motor units during low-force contractions is larger in old adults
(Galganski et al. 1993
), some of the decrease in
steadiness with age may be caused by factors that increase motor-unit
force. One such factor is the age-associated increase in the
innervation ratio of low-threshold motor units (Kadhiresan et
al. 1996
; Kanda and Hashizume 1989
). Another
possible factor is a change in the relative timing of motor-unit
activation: that is, an increase in the simultaneous activation of
motor units, commonly referred to as motor-unit synchronization.
The strength of synchronization among a group of motor units is
determined by the pattern of shared synaptic input onto the motoneurons, either directly or through last-order interneurons (Kirkwood et al. 1982; Sears and Stagg
1976
). Because of this association, the measurement of
motor-unit synchronization reveals details about the distribution and
plasticity of shared, branched-axon inputs to the motoneurons at the
spinal level (Datta and Stephens 1990
; Sears and
Stagg 1976
). As such, the measurement of motor-unit synchronization provides a window into the human nervous system during
the voluntary activation of muscle. Studies on motor-unit synchronization have indicated that its magnitude is influenced by such
factors as learning (Schmied et al. 1993
; Semmler
and Nordstrom 1998
), handedness (Schmied et al.
1994
; Semmler and Nordstrom 1995
), and recovery
from a lesion in the CNS (Farmer et al. 1993
).
Furthermore, synchronization is greater among motor units with smaller
and slower twitches (Schmied et al. 1993
,
1994
). These findings indicate that the shared synaptic
input onto motoneurons is influenced by the activities performed by the
involved motor units.
Because the daily levels of physical activity decline with advancing
age (Fiatarone and Evans 1993; Matousek et al.
1994
), we expected to find that motor-unit synchronization
would be greater in old adults and hence contribute to the decrease in
steadiness that they experience. The purpose of the study therefore was
to estimate the contribution of motor-unit synchronization to the larger spike-triggered average forces and the decreased steadiness exhibited by old adults. A preliminary account of these findings has
been published in abstract form (Semmler et al. 1999
).
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METHODS |
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Eleven young (19-30 yr of age) and 14 old (63-81 yr of age) healthy adults consented to participate in the study. Two different experiments were performed on separate days; one involved recording the activity of single motor units during low force isometric contractions, and the other consisted of steadiness measurements during constant-force isometric contractions. Seven young and 11 old subjects participated in both the single motor-unit and the steadiness experiments. One to three motor-unit experiments were performed with each subject on separate days. Only one session was required to measure isometric steadiness at four submaximal forces.
All subjects were right-hand dominant and were moderately active on a
daily basis. The Edinburgh Handedness Inventory (Oldfield 1971) was used to estimate the extent of hand preference during 12 commonly performed tasks. A value of zero represents no preference to use the right hand for most daily activities, and a value of one
represents a strong preference to use the right hand. The manual
dexterity of the subjects was assessed in a test with a Purdue Pegboard
(model 32020; Lafayette Instrument, Lafayette, IN), which required each
subject to place as many pegs as possible into the holes of the
pegboard in 30 s. The number of pegs placed in the holes was
measured three times for both the left and right hands.
Experimental arrangement
Each subject was seated facing a 14-in. computer monitor, which displayed signals directly from an oscilloscope. The left arm was placed prone on a manipulandum, and the elbow joint was flexed to approximately 90°. The index finger was placed in an individualized mold and strapped to an L-shaped aluminum splint so that the interphalangeal joints were kept extended. The splinted index finger made contact with a force transducer (Sensotec model 13) at the level of the proximal interphalangeal joint. The arm and hand were secured by restraints over the forearm, a support for the thumb, and a strap over the third to fifth digits. With this setup, the abduction force measured at the proximal interphalangeal joint was produced almost exclusively by contraction of the first dorsal interosseus muscle. The force exerted during a maximum voluntary contraction (MVC) was measured with a low-sensitivity transducer (range 0-220 N), whereas a more sensitive transducer (range 0-22 N) was used during the single motor unit and the isometric force steadiness trials. Signals from the force transducers were displayed on an oscilloscope and recorded in digital format (Sony PC 116 DAT recorder; bandwidth DC to 2.5 kHz).
The electromyogram (EMG) of the left first dorsal interosseus muscle was recorded with bipolar surface electrodes (4 mm diam; silver-silver chloride) that were placed ~2 cm apart on the skin overlying the muscle. A reference electrode was placed on the dorsal aspect of the hand. The surface EMG signals were amplified (1,000-2,000 times), band-pass filtered (20-800 Hz), displayed on an oscilloscope, and stored on tape. For the single motor-unit recordings, two bipolar, fine-wire intramuscular electrodes were inserted percutaneously into the first dorsal interosseus. Each electrode consisted of three formvar-insulated, stainless steel wires (50 µm diam) that were threaded through a disposable 27-gauge needle. Recordings were obtained from two wires within each electrode, while the third wire was used as an alternative bipolar configuration to sample from other motor units within the same muscle. The distance between the two intramuscular electrodes was usually 1-2 cm. Single motor-unit recordings were amplified (1,000-2,000 times), band-pass filtered (20 Hz to 8 kHz), displayed on an oscilloscope, and stored on digital tape.
Experimental procedures
MVC FORCE. The force exerted by the index finger during an MVC was measured at the beginning of every session. The task involved a gradual increase in the abduction force to its maximum value over 2-3 s, after which the maximal force was maintained for another 2-3 s. Subjects were aided in this task by visual feedback of the index finger force on a computer screen and by a verbal count given by the experimenter. Two to four MVC trials were recorded at the start of each session. Rest periods of at least 60 s were given between each MVC trial.
SINGLE MOTOR-UNIT EXPERIMENTS. The activity of single motor units was examined while subjects exerted a steady abduction force with the index finger. Subjects were asked to slowly increase the index finger force until each electrode detected at least one motor unit that was discharging action potentials repetitively. The force required to sustain the discharge was then maintained for 2-5 min with the aid of a target line placed on the oscilloscope screen. The target force was occasionally adjusted during these trials so that at least one motor unit could be readily identified with each electrode. At the beginning of the contraction, one motor unit was selected to have its discharge rate remain constant (usually between 8 and 12 Hz) throughout the trial. The subjects were provided with audio feedback of the discharge of the selected unit, which was discriminated on-line using a computer-based, template-matching algorithm (SPS 8701; Signal Processing Systems, Malvern, South Australia, Australia). The subject rested for at least 60 s between trials. New motor units were identified by manipulating at least one of the intramuscular electrodes, either by varying the pair of wires used to record the potentials or by displacing the wires, and the discharges of the new pairs of motor units were recorded for 2-5 min. This process was repeated to detect as many different pairs of motor units as possible in a given experiment. New motor units were classified during the experiment based on changes in motor-unit waveform shape, recruitment threshold, and individual motor-unit discharge characteristics.
FORCE-STEADINESS EXPERIMENTS. A separate set of experiments was performed to determine the steadiness with which each subject could maintain an abduction force with the index finger. The subject's MVC force was used to calculate four different target forces: 2.5, 5, 7.5, and 10% of MVC. This range of forces encompassed most of the target forces used in the motor-unit experiments. The target force was displayed on a computer screen along with the abduction force exerted by the index finger. The subjects gradually increased the abduction force during an isometric contraction until it matched the target force displayed on the oscilloscope, and then held the force as steady as possible for 30 s. The sensitivity of the force display was varied for each force level so that the target force was always five vertical divisions above baseline on the oscilloscope. The target forces were presented randomly. Subjects were given a 30- to 60-s rest between each trial and performed two to three trials at each target level.
Data analysis
MOTOR-UNIT EXPERIMENTS. All analyses were performed off-line from the taped records. For the MVC tasks, peak force and the maximum rectified EMG (AEMG) for 0.5 s were measured during each contraction. The single motor-unit recordings were digitized (10 kHz) along with the associated surface EMG (2 kHz) and the abduction force exerted by the index finger (200 Hz). Single motor units were discriminated using a computer-based, spike-sorting algorithm (Spike2; Cambridge Electronic Design, Cambridge, UK), which identifies the action potentials belonging to a particular motor unit based on waveform shape. To ensure discrimination accuracy, the interspike intervals of identified motor units were examined for every trial. Abnormally short and long interspike intervals that were clearly the result of discrimination error were excluded from statistical analysis. For the remaining discharge times, the mean, standard deviation, and coefficient of variation of the interspike intervals were determined using custom-designed software written in Matlab (Mathworks, Natick, MA).
Estimates of motor-unit size were obtained from the spike-triggered average force. For this analysis, the identified action potential was used as the trigger event to estimate the contribution of the motor unit to the net force exerted by the index finger. All motor-unit discharges were included in the analysis provided the mean discharge rate for the motor units was <12 Hz. The duration of the spike-triggered average was 200 ms with a pretrigger average of 50 ms. Measurements of spike-triggered average force were accomplished with the Spike2 data analysis system. Motor units detected with separate electrodes during the same trial were paired for cross-correlation analysis to assess motor-unit synchronization. All cross-correlograms had binwidths of 1 ms and spanned a period 100 ms before and 100 ms after the discharge of the reference unit. The cumulative sum (CUSUM) (Ellaway 1978FORCE STEADINESS DATA. The target forces of 2.5, 5, 7.5, and 10% MVC were established based on the MVC performed in that experimental session. The coefficient of variation of the force fluctuations was measured for the middle 30 s of each contraction. The reported data represent the average of two steadiness trials.
Statistical analysis
A two-factor (age × gender) ANOVA was used to compare the dependent variables for laterality quotient, Purdue Pegboard score, and age. For the motor-unit experiments, a two-factor ANOVA was used to compare age (young, old) and gender (men, women) effects. The dependent variables were 1) MVC force, 2) MVC AEMG, 3) mean discharge rate, 4) mean coefficient of variation of discharge rate, 5) synchronization strength (CIS), and 6) spike-triggered average force of the motor units. For the force steadiness experiments, a two-way ANOVA was used to compare age (young, old) and load (2.5, 5, 7.5, and 10% MVC) effects. Dependent variables for the force steadiness experiments were 1) MVC force, 2) MVC AEMG, and 3) mean coefficient of variation of the force fluctuations. The data are reported as means ± SD in the text and means ± SE in the figures, unless otherwise stated.
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RESULTS |
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The extent of hand dominance (LQ value) was similar between young and old adults (Table 1). All subjects preferred to use the right hand for more than 50% of the 12 daily activities listed on the questionnaire. When using the left (experimental) hand, the Purdue Score was greater (P < 0.001) for young subjects compared with the old subjects, which indicated that the young subjects were able to place more pegs into holes on the Purdue Pegboard than old subjects in the allotted time (90 s). Furthermore, the strength of the left first dorsal interosseus for the old subjects was significantly less than that of the young subjects (Table 1). Post hoc tests indicated that the lower MVC force for the old subjects was primarily due to a difference between the young and old men (P < 0.05).
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Spike-triggered average force
The force contributed by single motor units discharging at minimal
rates (12 imp/s) was assessed by spike-triggered averaging. The data
comprised 37 motor units from young adults and 51 motor units from old
adults. Examples of spike-triggered average force for a young man and
an old man are shown in Fig. 1. The
discharge times of the two motor units from the young adult (Fig. 1,
A and B) were used to derive the
cross-correlogram shown in Fig. 3A, while those from the old
adult (Fig. 1, C and D) contributed to the
cross-correlogram shown in Fig. 3B. For the young subject, the spike-triggered average force was 10.6 mN (0.026% MVC) in Fig.
1A and 10.9 mN (0.027% MVC) in Fig. 1B. For the
old subject, the spike-triggered average forces were 24.3 mN (0.059%
MVC) in Fig. 1C and 34.0 mN (0.059% MVC) in Fig.
1D. The time-to-peak force was similar in both motor units
of the young (75 and 66 ms) and the old (73 and 75 ms) adults.
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The mean discharge rate, coefficient of variation of discharge rate, and the number of trigger events used to determine the spike-triggered average force were similar in young and old adults (Table 2). A two-factor ANOVA revealed significant differences in absolute spike-triggered average force between age groups (F = 11.5, P < 0.001), between genders (F = 16.5, P < 0.001), and for the age × gender interaction (F = 5.6, P < 0.05). For normalized spike-triggered average force (%MVC), significant effects were observed for age group (F = 8.6, P < 0.01) and in the age × gender interaction (F = 12.1, P < 0.001). These data show that the spike-triggered average forces were approximately twice as large in old adults, and that the differences between young and old men were primarily responsible for this effect (Table 2). There were no age (F = 1.6, P > 0.05) or gender (F = 2.4, P > 0.05) differences in the time-to-peak of the spike-triggered average force, although a significant group × gender interaction (F = 17.7, P < 0.0001) indicated that the time-to-peak was significantly greater in young men compared with both young women (Scheffe's post hoc test; P < 0.01) and old men (P < 0.01).
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Isometric force steadiness
The coefficient of variation of force during the isometric contractions was greatest for the lowest target force (2.5% MVC) and decreased as force increased in both groups (Fig. 2). A two-factor, repeated measures ANOVA revealed significant differences in the coefficient of variation of force for age group (F = 9.78, P < 0.01), force level (F = 17.76, P < 0.0001), and the interaction (F = 2.88, P < 0.05). The mean coefficient of variation was greater (unpaired t-tests with Bonferroni correction) for the old subjects at the 2.5 and 5% MVC target forces.
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Discharge properties of individual motor units
The discharge rates of individual motor units examined in first dorsal interosseus were similar for young and old adults. Mean discharge rate was 11.1 ± 1.6 Hz (mean ± SD, n = 70) for young subjects and 11.1 ± 2.4 Hz (n = 85) for old subjects. In contrast, there was a small but significant difference in the mean coefficient of variation of discharge rates between young and old adults (F = 4.4, P < 0.05). The mean coefficient of variation was 18.7 ± 4.0% (n = 70) for young subjects and 17.5 ± 3.5% (n = 85) for old subjects. This difference was primarily due to a larger mean coefficient of variation for young women (19.6 ± 4.3%, n = 33) compared with old women (17.4 ± 3.7%, n = 34).
Motor-unit synchronization
A typical example of a cross-correlogram and the corresponding CUSUM for a young man and an old man are shown in Fig. 3. In each case, there was a significant peak in the cross-correlogram due to motor-unit synchronization. For the young subject (Fig. 3A), the synchrony index CIS was 0.57 impulses/s (imp/s), and the width of the central synchronous peak was 15 ms. For the old subject (Fig. 3B), the synchrony index CIS was 0.56 imp/s, and the width of the peak was 11 ms. Although, in this example, the strength of synchronization for each motor-unit pair was similar, the spike-triggered average forces were much larger for the old adult (Fig. 1).
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The strength of motor-unit synchronization was similar in young and old adults. Mean CIS was 0.66 ± 0.4 imp/s (n = 53) for young subjects and 0.72 ± 0.5 imp/s (n = 56) for old subjects. The mean CIS varied over a fourfold range (0.35-1.51 imp/s) in the 11 young subjects and a fivefold range (0.27-1.38 s imp/s) in the 14 old subjects. Furthermore, the mean width of the significant synchronization peaks was similar in young (16.2 ± 5.0 ms, n = 52) and old (16.2 ± 6.2 ms, n = 50) adults.
The associations between motor-unit discharge pattern and motor-unit synchronization were different for the young and old adults (Fig. 4). The synchronization index CIS for pairs of motor units was not related to the geometric mean discharge rate for the unit pairs of young adults (Fig. 4A; R2 = 0.02, P > 0.05), whereas there was a significant, albeit weak relationship for the old adults (Fig. 4C; R2 = 0.11, P < 0.05). The significant association for the old adults indicated that the central synchronous peak in the cross-correlogram was larger when motor units discharged at lower mean rates. Conversely, the geometric mean of the coefficient of variation of discharge rate for the two motor units contributing to the cross-correlogram was significantly related to the synchrony index for the young adults (Fig. 4B; R2 = 0.57, P < 0.0001) but not the old adults (Fig. 4D; R2 = 0.05, P > 0.05). The significant association for the young subjects indicates that the CIS index was greater when discharge rate was more variable.
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The association between spike-triggered average force for single motor
units and the strength of motor-unit synchronization is shown in Fig.
5. For this analysis, the spike-triggered
average force for each individual motor unit was plotted against the
CIS value that was obtained from the cross-correlogram in a motor-unit pair. For motor units that were included in more than one
cross-correlogram, the average CIS value from all the
cross-correlograms was included in the distribution. The absolute
spike-triggered average force (mN) was significantly correlated with
the strength of motor-unit synchronization for all motor units (,
Fig. 5A; R2 = 0.15, P < 0.001) and for motor units from old adults
(- - -, Fig. 5A;
R2 = 0.16, P < 0.01). Similarly, the normalized spike-triggered average force (%MVC)
was significantly correlated with the strength of motor-unit
synchronization for all motor units (
, Fig. 5B; R2 = 0.17, P < 0.0001), and for motor units in young (· · ·, Fig. 5B; R2 = 0.41, P < 0.0001) and old (- - -, Fig. 5B;
R2 = 0.09, P < 0.05)
adults. These data suggest that from 9 to 41% of the variation in
spike-triggered average force could be explained by differences in the
strength of motor-unit synchronization as measured from the
cross-correlogram. Therefore, although the effect is only minor, it
does indicate that differences in the strength of motor-unit
synchronization can influence the amplitude of the spike-triggered
average force. Obtaining a more representative estimate of motor-unit
synchronization by restricting the analysis to motor units that were
used in more than one cross-correlogram did not significantly improve
the correlation. From a total of 34 motor units (17 young, 17 old) that
were used in this analysis, the absolute spike-triggered average force
was significantly correlated with the strength of motor-unit
synchronization for all motor units
(R2 = 0.12, P < 0.05). In addition, the normalized spike-triggered average force was
significantly correlated with the strength of motor-unit
synchronization for all motor units
(R2 = 0.14, P < 0.05) and for motor units from young adults
(R2 = 0.37, P < 0.01).
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Isometric force steadiness and motor-unit synchronization
The relationship between the strength of motor-unit synchronization and steadiness was examined for each motor-unit pair in young and old adults (Fig. 6). To facilitate the comparison, the strength of motor-unit synchronization for each motor-unit pair was correlated with the average isometric steadiness obtained at the force level that was closest to the mean force during the motor-unit trial. Because steadiness measures were not obtained from all subjects who participated in the motor-unit experiments, the number of cross-correlograms available for this analysis was 33/53 for young subjects and 49/56 for old subjects. For young subjects, there was a significant, albeit weak, linear correlation between motor-unit synchronization and the coefficient of variation for force (fitted line in Fig. 6, R2 = 0.14, P < 0.05). However, the relationship was not significant for the old subjects (R2 = 0.004, P > 0.05).
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The distribution of mean abduction forces exerted by the index finger during the motor-unit experiments in young and old adults are shown in Fig. 7. For the young subjects, more motor units were examined at relatively low target forces than for the old subjects. The mean force during the motor-unit experiments was 1.9 ± 1.3 N (4.2 ± 2.5% MVC) for the young subjects and 2.4 ± 1.3 N (7.4 ± 4.7% MVC) for the old subjects. The normalized forces exerted during the motor-unit experiments were significantly larger (F = 10.9, P < 0.01) in old adults. When the coefficient of variation of force during the steadiness experiments was matched to the mean force during the motor-unit experiments for each subject, the coefficient of variation of force was 3.7 ± 1.6% for the young subjects and 4.9 ± 2.5% for the old subjects; this difference was significant (F = 4.9, P < 0.05). These data suggest that the old adults were less steady at the mean forces exerted during the motor-unit experiments, even though they exerted more force to activate the recorded motor units.
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DISCUSSION |
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As anticipated, the old adults had reduced manipulative capabilities (measured with the Purdue Pegboard), diminished strength of the first dorsal interosseus muscle, decreased steadiness when exerting low abduction forces with the index finger, and increased spike-triggered average forces for motor units. The new findings involved the associations between motor-unit synchronization, spike-triggered average force, and steadiness. Although the young and old adults exhibited similar levels of motor-unit synchronization, the associations between motor-unit discharge pattern and synchronization were different for the two groups. Furthermore, despite the presence of a weak relationship between the spike-triggered average force and motor-unit synchronization, there was no association between motor-unit synchronization and the steadiness of low-force isometric contractions for the old adults.
Motor-unit synchronization in young and old adults
Motor-unit synchronization is a measure of the correlated
discharge of action potentials among motor units. It arises from the
near simultaneous generation of excitatory postsynaptic potentials in
the motoneurons from common presynaptic neurons, which slightly increases the probability that the motoneurons will discharge action
potentials within a few milliseconds of each other (Datta and
Stephens 1990; Sears and Stagg 1976
). The amount
of synchronization depends on the number and rate of the shared inputs
and the size of the unitary excitatory postsynaptic potentials evoked
in the motoneurons (Nordstrom et al. 1992
).
Several lines of evidence indicate that the most significant
contributor to motor-unit synchronization is the direct projection from
the motor cortex to spinal motoneurons via the lateral corticospinal tract (Farmer et al. 1991, 1993
;
Schmied et al. 1999
; Smith et al. 1999
).
Neurons in the lateral corticospinal tract, however, appear to be
altered with advancing age. For example, approximately 40% of cortical
neurons are lost or become nonfunctional after 60 yr of age
(Henderson et al. 1980
), and there is a reduction in the
amplitude (Eisen et al. 1991
) and latency (Eisen
and Shtybel 1990
) of motor-evoked potentials in older adults.
Accordingly, we expected to find a difference in the level of
motor-unit synchronization in old adults. To the contrary, we found no
difference in the strength of motor-unit synchronization between young
and old adults, which suggests that there was no effect of advancing
age on the relative divergence of the corticospinal projections. This
finding is in agreement with a recent study indicating that motor-unit synchronization is similar in young and old adults when recorded at
high forces (Kamen and Roy 2000
).
Spike-triggered average force and motor-unit synchronization
Changes that occur in the human neuromuscular system with aging
include the progressive death of -motoneurons (Gardner
1940
; Tomlinson and Irving 1977
) and the
reinnervation of some abandoned muscle fibers by the surviving
motoneurons (Campbell et al. 1973
; Kadhiresan et
al. 1996
; Kanda and Hashizume 1989
;
Masakado et al. 1994
), which increases the force exerted
by individual motor units.
When motor-unit force is estimated with spike-triggered averaging,
however, the presence of synchronized discharges among motor units
probably inflates the actual force for a given motor unit. Although we
found that the spike-triggered average forces were larger in old adults
(Table 2), which is in agreement with previous studies
(Galganski et al. 1993; Keen et al.
1994
), there was no difference between the two groups in the
amount of motor-unit synchronization. Similarly, although the pattern
of motor-unit discharge can influence the amplitude of the
spike-triggered average force (Nordstrom et al. 1989
),
there was no difference in the mean discharge rate, coefficient of
variation of discharge rate, or number of trigger events for motor
units in young and old adults. Therefore differences in the degree of
fusion for individual motor units cannot be responsible for the larger
spike-triggered average forces observed in older adults. Furthermore,
while there was a significant association between the strength of
motor-unit synchronization and spike-triggered average force (Fig. 5),
the effect was relatively weak (R2 = 0.09 to 0.41). These findings suggest that the larger spike-triggered average forces exhibited by the old adults, particularly old men, were
due primarily to the reorganization of motor-unit territories, presumably with the increase in the innervation ratio being the dominant factor.
Relationship between motor-unit discharge properties and motor-unit synchronization
Based on conventional indexes of motor-unit synchronization,
Nordstrom et al. (1992) suggested that the relationship
between discharge rate and synchronization is a consequence of the
mathematical procedures used to estimate the amount of synchrony from
the cross-correlogram peak. They proposed a new index to quantify the
strength of synchronization (CIS) that was mathematically independent
of discharge rate. Consistent with this proposition, we found in young
subjects that the discharge rate of the contributing motor units does
not influence the strength of motor-unit synchronization as measured by
the CIS index (Fig. 4A). In the old adults, however, a small
but statistically significant proportion (11%) of the variation in
synchronization could be accounted for by differences in the discharge
rate of the contributing motor units (Fig. 4C). This weak
association indicated that motor-unit synchronization was greater when
the contributing motor units were discharging at lower mean rates,
which suggests that the ratio of common-to-independent inputs is
greater in old adults when the contributing motor units discharge slowly.
For young adults, the strength of synchronization was greater when the
discharge rate of the contributing motor units was more variable (Fig.
4B). It is often suggested that discharge rate variability
is related to the degree of fluctuation in the membrane potential about
its mean trajectory, and that the asynchronous arrival of postsynaptic
potentials from many different sources gives rise to these fluctuations
(Matthews 1999). Because increases in the amplitude of
the unitary excitatory postsynaptic potentials will increase the
fluctuations in membrane potential, the association between discharge
variability and motor-unit synchronization could be related to the
unitary excitatory postsynaptic potential amplitudes (Nordstrom
et al. 1992
). However, minor alterations in afferent input have
no effect on discharge variability (Stålberg and Thiele 1973
), which suggests that extrinsic factors (source and
location of inputs) are unlikely to be responsible for large
differences in discharge variability and synchrony among motoneurons in
a single pool. In contrast, it has been suggested that intrinsic motoneuron properties related to repetitive discharge of a motoneuron, such as the amplitude of the afterhyperpolarization and repolarization, could produce a link between discharge rate variability and synchrony (Nordstrom et al. 1992
). A stronger association between
motor-unit synchrony and discharge rate variability may be observed in
neurons that express a wider range of discharge rates; such an
association has been observed in
-motoneurons in the decerebrate cat
following spinal cord section (Davey and Ellaway 1988
).
In the present study, the typical association between synchrony and
discharge rate variability was observed in young subjects but not in
old subjects. The absence of an association in the old adults may be a
consequence of the changes that occur in the biophysical properties of
motoneurons with advancing age (Morales et al. 1987
).
Relationship between motor-unit synchronization and force steadiness
Motor-unit synchronization has the potential to influence the
steadiness of low-force isometric contractions. Although modeling studies have shown that motor-unit synchronization is not necessary to
produce fluctuations in force (Christakos 1982), these
studies predict that the amplitude of the force fluctuations would be enhanced by motor-unit synchronization. This has been confirmed in a
recent study involving simulated contractions of a hand muscle, where
the addition of physiological levels of motor-unit synchronization increased the amplitude of the force fluctuations without influencing the magnitude of the average force (Yao et al. 2000
).
Furthermore, the simulation showed that the effect of synchronization
on the normalized force fluctuations was greatest at low forces, as has been observed experimentally (Galganski et al. 1993
;
Laidlaw et al. 2000
).
Despite these theoretical findings, there is some uncertainty
based on experimental studies on the relationship between motor-unit synchronization and force variability in human subjects. Some reports
indicate that motor-unit synchronization may contribute to the force
fluctuations (Dietz et al. 1976; Halliday et al. 1999
; McAuley et al. 1997
), while others have
not found such an association (Logigian et al. 1988
;
Semmler and Nordstrom 1998
). We found a weak
relationship between motor-unit synchronization and the steadiness of
low-force isometric contractions in young adults but not in old adults.
Furthermore, the old adults were less steady at the mean forces exerted
during the motor-unit experiments, although there was no difference in
the strength of motor-unit synchronization in young and old adults.
These findings suggest that other mechanisms, such as motor-unit size
and number (Christakos 1982
), agonist-antagonist
coactivation (Vallbo and Wessberg 1993
), or discharge
rate characteristics (Laidlaw et al. 2000
), underlie the
enhanced force fluctuations observed in old adults. We conclude that
motor-unit synchronization does not contribute to the decreased steadiness observed in old adults when performing low-force isometric contractions with a hand muscle.
In summary, we found that the strength of synchronization between motor units in the first dorsal interosseus muscle is similar in young and old adults. This finding indicates that motor-unit synchronization is not responsible for the larger spike-triggered average forces in old adults and that differences in motor-unit synchronization cannot explain the decrease in steadiness exhibited by old adults during low-force isometric contractions.
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ACKNOWLEDGMENTS |
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This work was supported by National Institute on Aging Grant AG-09000 to R. M. Enoka.
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FOOTNOTES |
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Address for reprint requests: R. M. Enoka, Dept. of Kinesiology and Applied Physiology, University of Colorado, Boulder, CO 80309-0354 (E-mail: roger.enoka{at}colorado.edu).
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.
Received 31 January 2000; accepted in final form 5 April 2000.
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REFERENCES |
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