Motor-Unit Synchronization Is Not Responsible for Larger Motor-Unit Forces in Old Adults

John G. Semmler, Julie W. Steege, Kurt W. Kornatz, and Roger M. Enoka

Department of Kinesiology and Applied Physiology, University of Colorado, Boulder, Colorado 80309-0354


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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).


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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 1978) technique was used to aid in visually judging the location of the central synchronous peak. The statistical significance of the central peak was assessed with the method described by Wiegner and Wierzbicka (1987). Cross-correlation histograms with a mean bin count <4 were not analyzed. If the peak was not significant, then a standard peak width of 11 ms, centered at time 0, was used for quantification of the strength of synchrony for the pair of motor units. The magnitude of the central synchronous peak was quantified using the synchronization index Common Input Strength (CIS) (Nordstrom et al. 1992), which is the number of synchronous discharges in excess of chance divided by the duration of the trial when both motor units were tonically active. The index represents the frequency of extra synchronous discharges and is mathematically independent of discharge rate (Nordstrom et al. 1992).

FORCE 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.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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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Table 1. Subject characteristics

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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Fig. 1. Examples of spike-triggered average force for motor units in a young man (A and B) and an old man (C and D). The 2 traces in each panel are the spike-triggered average force at the top and the averaged motor-unit potential that was used as the trigger event at the bottom. The mean discharge rates of the motor units were 11.2 Hz in A, 7.4 Hz in B, 8.6 Hz in C, and 10.7 Hz in D. The number of trigger events were 2,622 in A, 1,154 in B, 745 in C, and 1,611 in D. This example demonstrates that spike-triggered average forces were larger in old adults.

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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Table 2. Spike-triggered averaging of motor units in young and old adults

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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Fig. 2. Measures of normalized force fluctuations (coefficient of variation) during isometric contractions about each mean target force for young (open circle ) and old () adults. The target forces correspond to the mean abduction force exerted by the index finger during the motor-unit trials. These data indicate that the older subjects had a reduced ability to maintain a steady abduction force at the lowest target forces used in the motor-unit experiments. *, P < 0.05.

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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Fig. 3. Examples of motor-unit synchronization in 1 young man and 1 old man. A: cross-correlogram (bottom trace) and the corresponding cumulative sum (CUSUM; top trace) of the discharge times for 2 motor units in 1 young subject. The 2 motor units that created the cross-correlograms for each subject correspond to the motor units shown in Fig. 1. The dotted vertical lines respresent the width of the central synchronous peak as indicated by the cusum. B: cross-correlogram and CUSUM from an old subject, arranged as in A. Although 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).

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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Fig. 4. Relationships between the synchrony index Common Input Strength (CIS) and motor-unit discharge pattern in young (A and B) and old (C and D) adults. The data show the synchrony index CIS plotted against the geometric mean discharge rate (A and C) and the geometric mean of the coefficient of variation of discharge rate (B and D) of the motor units in the cross-correlogram. Linear regression revealed a negative correlation between the geometric mean discharge rate and the synchrony index CIS for old (fitted line in C; R2 = 0.11, P < 0.05) but not young adults (A). In contrast, there was a positive correlation between the geometric mean of the coefficient of variation and the synchrony index CIS for young (fitted line in B; R2 = 0.57, P < 0.0001) but not old adults (D). These results demonstrate that the typical relationship between the synchrony index CIS and motor-unit discharge properties in young adults is not observed in old adults.

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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Fig. 5. Relationship between the strength of motor-unit synchronization (synchrony index CIS) and spike-triggered average (STA) force of single motor units in young (open circle ) and old () adults (A, absolute forces; B, normalized forces). These data indicate a weak relationship between the strength of motor-unit synchronization and the spike-triggered average force of individual motor units. ---, all subjects; · · · , young subjects; - - -, old subjects.

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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Fig. 6. Relationship between the strength of motor-unit synchronization and isometric force steadiness in young (open circle ) and old () adults. These data indicate that motor-unit synchronization was weakly related to isometric steadiness in young (fitted line, R2 = 0.14, P < 0.05) but not old adults.

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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Fig. 7. Distribution of absolute index finger abduction forces (A) and the normalized forces (B) exerted during the motor-unit experiments in young () and old () adults. The difference in the distributions indicate that more motor units were examined at relatively low target forces in young compared with old adults.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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 alpha -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 gamma -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.


    ACKNOWLEDGMENTS

This work was supported by National Institute on Aging Grant AG-09000 to R. M. Enoka.


    FOOTNOTES

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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