Older Adults Use a Unique Strategy to Lift Inertial Loads With the Elbow Flexor Muscles

Andrew E. Graves, Kurt W. Kornatz, and Roger M. Enoka

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


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Graves, Andrew E., Kurt W. Kornatz, and Roger M. Enoka. Older Adults Use a Unique Strategy to Lift Inertial Loads With the Elbow Flexor Muscles. J. Neurophysiol. 83: 2030-2039, 2000. The purpose of this study was to determine the effect of age on the ability to exert steady forces and to perform steady flexion movements with the muscles that cross the elbow joint. An isometric task required subjects to exert a steady force to match a target force that was displayed on a monitor. An anisometric task required subjects to raise and lower inertial loads so that the angular displacement around the elbow joint matched a template displayed on a monitor. Steadiness was measured as the coefficient of variation of force and as the normalized standard deviation of wrist acceleration. For the isometric task, steadiness as a function of target force decreased similarly for old adults and young adults. For the anisometric task, steadiness increased as a function of the inertial load and there were significant differences caused by age. Old adults were less steady than young adults during both shortening and lengthening contractions with the lightest loads. Furthermore, old adults were least steady when performing lengthening contractions. These behaviors appear to be associated with the patterns of muscle activation. These results suggest that different neural strategies are used to control isometric and anisometric contractions performed with the elbow flexor muscles and that these strategies do not change in parallel with advancing age.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Advancing age is associated with alterations in the biophysical properties of motor neurons, the remodeling of motor unit territories, a decreased maximum discharge rate of motor neurons, and a decline in sensory capabilities (Katzman 1995). Such adaptations presumably provide the foundation for some of the reductions in motor performance that are experienced by elderly adults (Enoka and Laidlaw 1998). For example, changes in motor unit properties probably mediate the diminished ability of older adults to exert steady submaximal forces during both isometric and anisometric contractions (Cole 1991; Galganski et al. 1993; Keen et al. 1994; Kinoshita and Francis 1996). The features of motor output that could reduce the steadiness exhibited by old adults include increased motor unit force, changes in the discharge behavior of motor units, and low frequency modulation of the coactive agonist and antagonist muscles (Laidlaw et al. 2000).

Observations that older adults are less steady when lifting light loads and exerting low forces have been based on relatively simple tasks, such as abduction of the index finger. Such tasks, however, might exacerbate the observed decrease in steadiness for two reasons. First, the movement is largely controlled by a single agonist muscle (first dorsal interosseous) and a single antagonist muscle (second palmar interosseous). In contrast, tasks that are controlled by several muscles whose individual mechanical properties and levels of activation vary over the range of motion are less susceptible to variations in the behavior of individual muscles (Latash et al. 1998a,b). Second, the gradation of force up to intermediate values involves the recruitment of a greater proportion of the motor unit pool in hand muscles than in limb muscles (DeLuca et al. 1982; Kukulka and Clamann 1981). Because fluctuations in force are influenced by the unfused contractions of the most recently recruited motor units (Allum et al. 1978), the compressed recruitment range of motor units exacerbates this effect in hand muscles (Fuglevand et al. 1993; Galganski et al. 1993; Keen et al. 1994).

The purpose of the present study was to determine the effect of age on the ability to exert steady forces and to perform steady flexion movements with the muscles that cross the elbow joint. Because several muscles can contribute to these tasks (An et al. 1989; Buchanan and Lloyd 1995; Nakazawa et al. 1993), we expected to find less of a difference in steadiness due to age than has been observed in hand muscles. Consistent with this expectation, we found no differences caused by age in the steadiness of isometric contractions that were performed using the elbow flexor muscles. However, older adults were significantly less steady when raising and lowering light loads. Some of these results were presented in abstract form (Enoka et al. 2000; Graves et al. 1999).


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Thirty-two right-handed subjects were recruited for this study. They were 17 young subjects (7 men, 10 women) and 15 old subjects (7 men, 8 women). The young subjects ranged in age from 19 to 30 (22.9 ± 3.5, mean ± SD) years and the old subjects were between 60 and 81 (71.2 ± 7.8) years old. The health status of the subjects was determined with a written questionnaire, and none were aware of any neuromuscular disorder or arthritis affecting the left arm. Furthermore, levels of daily activity ranged from sedentary to moderately active, but no subject had performed any strength-training activities in the six months before participation in the study. Written informed consent was obtained from all subjects in accordance with the requirements of the Institutional Review Board at the University of Colorado.

All subjects were seated in a modified chair (Fig. 1) and their left arms were constrained to perform isometric contractions or to lift inertial loads. Two wide nylon straps were placed vertically over each shoulder to restrain the subject and minimize shoulder movement. The tested arm was placed in a sagittal plane with the upper arm parallel to the trunk and the shoulder slightly abducted (0.17 rad). The isometric contractions were performed with the elbow joint at an angle of 1.57 rad. The anisometric contractions were performed over an intermediate range of motion from an elbow angle of 1.30 rad, up to 1.83 rad, and back to 1.30 rad.



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Fig. 1. Schematic drawing of a subject in the experimental apparatus for the constant-load task. The left forearm was placed in an orthosis to which a load could be attached. The elbow of the left arm was kept on a padded support throughout the task. Both of the subject's shoulders were restrained with straps. For the constant-force task, the orthosis was attached to a force transducer with the elbow joint at a right angle.

Electrical recording

Surface electromyographic (EMG) signals were recorded with bipolar electrodes (silver-silver chloride, 8-mm diameter) from the long head of the biceps brachii, the short head of the biceps brachii, the brachioradialis, and the medial head of the triceps brachii. The distance between the pairs of surface electrodes was 20 mm. The EMG activity of the brachialis was measured with an intramuscular bipolar electrode inserted into the muscle ~3 cm proximal to the antecubital fold. The electrode consisted of two stainless steel fine wires (100 µm diameter) that were insulated with polyvinyl acetal (Formvar, California Fine Wire Company, Grover Beach, CA). A surface electrode (8 mm diameter) served as the reference. The EMG data were amplified as necessary (×1000-3000), band-pass filtered (20-800 Hz), recorded on digital tape, and displayed on an oscilloscope.

Experimental procedures

Each subject was asked to perform two tests of maximal muscle strength with the elbow flexor muscles: a one-repetition maximum (1-RM) load and a maximum voluntary contraction (MVC). These performances were used to set target levels for submaximal isometric and anisometric contractions.

1-RM LOAD. The 1-RM load was defined as the amount of weight that could be lifted no more than once without using extraneous body movements. The 1-RM load was determined with the subject seated in the experimental chair (Fig. 1). The range of motion for the task was from complete extension of the elbow joint (0 rad) to a right angle (1.57 rad). The experimenter chose the initial weight and successive weights were increased in increments of 5-20 N until the 1-RM load was identified. When the movement was not performed correctly, the subject was given a chance to repeat the attempt. If the subject still could not perform the task correctly, then the last successfully completed weight was taken as the 1-RM load. Subjects were given three minutes of rest between each attempt.

MVC FORCE. The MVC task consisted of a ramp increase in flexion or extension force from zero to maximum in ~3 s and then a sustained contraction at the maximum for 2-3 s. Subjects monitored the increase in force on the monitor. The timing for the task was provided verbally by the experimenter. The subjects performed three MVC trials in both the flexion and extension directions, and the force was recorded on tape. Additional MVC trials were performed if the amounts of force from two of the three trials were not within 5% of each other. The greatest force exerted by the subject was taken as the MVC force. Subjects were given two minutes of rest between all trials and an additional four minutes of rest before performing the constant-force trials.

CONSTANT-FORCE TASK. Subjects performed isometric contractions at target forces of 5, 10, 20, 35, 50, and 65% MVC. The forces exerted during the isometric tasks were detected by a force transducer (JR-3 Universal Force-Moment Sensor System, JR-3 Inc., Woodland, CA) mounted on a customized manipulandum. The left arm of each subject was attached to the force transducer by a modified wrist-hand-thumb orthosis (Orthomerica, Newport Beach, CA) that held the forearm in a neutral position between pronation and supination. Output from the force transducer was recorded on a digital tape recorder (Sony PC 116) and displayed on a 14-inch computer monitor located 1 m in front of the subject.

The contractions were performed in quasi-random order with the 20-65% MVC trials assigned randomly followed by the 5 and 10% MVC trials. Rest periods of one or two minutes were allowed between each trial. Subjects were required to exert steady elbow flexion force for 15 s at the target force. The horizontal target line on the oscilloscope remained in the same location for all force levels by adjusting the gain of the vertical axis. By doing this, the subjects were given feedback that was approximately proportional to the required target force. The force exerted by the subject was shown as a horizontal line on the oscilloscope and the subject was instructed to overlap the force trace with the target line. Two consecutive trials were performed at each target force.

CONSTANT-LOAD TASK. Subjects performed anisometric contractions with loads that were 10, 15, 25, and 35% of the 1-RM load. Subjects were seated in the experimental chair with their left elbows resting on a padded support. With the left forearm in the neutral positon, a modified plastic hand-wrist-thumb orthosis was placed on the left hand. Weights were attached on the underneath side of the orthosis in line with the metacarpophalangeal joints. A platform on the top surface of the orthosis served as a mount for a uniaxial accelerometer (7265A-HS, Endevco, San Juan Capistrano, CA) with its axis aligned perpendicular to the long axis of the forearm.

Subjects raised and lowered the load in a sagittal plane through a 0.52 rad (30°) range of motion from 1.30 to 1.83 rad (0 rad = full extension). Angular displacement of the elbow was measured with an electrogoniometer (XM110 and K100, Penny and Giles, Cwmfelinfach, Gwent, UK) taped across the medial side of the elbow joint. The output of the electrogoniometer was displayed on the monitor. Subjects were instructed to match the angular displacement of the elbow to a triangular template, which required them to lift the load in six seconds and to lower it in six seconds, with constant-velocity shortening and lengthening contractions, respectively. These flexion-extension movements were performed without any internal-external rotation of the humerus. The subjects performed as many trials as necessary to obtain three acceptable attempts. The standard deviation of acceleration and the EMG were averaged across the three trials for each subject.

Data analysis

The recorded signals were downloaded onto the hard drive of a computer using an analog-to-digital board (CED 1401) at either 200 Hz (position and force) or 1000 Hz (EMG, acceleration, and high-sensitivity force). All data were analyzed off-line using the Spike2 data analysis system (Cambridge Electronic Design Ltd., Cambridge, UK). The EMG from the MVC was full-wave rectified and the average EMG was calculated for the 500 ms interval in which the EMG amplitude was greatest. For the constant-force task, the mean force during the middle 10 seconds of each trial was determined with subsequent calculation of the coefficient of variation (SD/mean force ×100). EMG was averaged over a user-selected window of 500-ms duration. The constant-load data were analyzed by placing cursors at the beginning, middle, and end of the movement to mark the raising and lowering phases of the task, and then calculating the standard deviation of the acceleration for both the whole phase (6 s) and the middle four seconds of each phase. The standard deviations for acceleration were normalized to the absolute load (kg) that was lifted.

Statistical analysis

Two-factor analysis of variance (ANOVA) was used to compare 1-RM load and MVC force between groups (age and gender). Within each age group, ANOVAs were performed to determine the effect of gender on steadiness and EMG during isometric and anisometric contractions. With one exception, there were no differences because of gender for any of the outcome variables for either the young or the old adults. The exception was the amount of triceps brachii EMG (antagonist muscle) during the anisometric contractions; it was significantly greater (P < 0.05) for the old men (4.6% MVC) compared with the old women (2.3% MVC). This difference was not considered to be central to the principal findings and therefore the groups were collapsed across gender and the analysis focused on the differences caused by age.

To determine the effects of age and force level on isometric steadiness, a two-factor ANOVA with a repeated-measures design was performed on the coefficient of variation for force. The EMG for the isometric contractions (constant force) was analyzed with a three-factor ANOVA (age × muscle × target force) with a repeated-measures design. To analyze steadiness during the anisometric task, a three-factor ANOVA (age × phase × load) with a repeated-measures design was performed. The EMG during the constant-load task was analyzed by a four-way repeated-measures ANOVA (1 between factor and 3 within factors). The level of significance was set at P < 0.05 for all statistical comparisons and Tukey-Kramer post hoc tests were used to locate differences when ANOVAs yielded significant interactions. Unless otherwise stated, all values are reported as mean ± SE.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The strength of left elbow flexors in the older adults was significantly less (P < 0.05) than that of the younger subjects for the 1-RM load (10.6 ± 0.8 vs. 13.4 ± 0.9 kg), but not for the MVC force (old = 239 ± 20 N; young = 258 ± 21 N). The greater 1-RM loads lifted by the young subjects were mainly due to a difference between the young and old men (Table 1). The lack of a difference in 1-RM loads between the young and old women was due to the presence of an outlier who had a value that was 25% greater than the next strongest old woman and 9% greater than the strongest young woman. When the data from this subject were excluded, there was a difference in 1-RM load between the young and old women (P < 0.01). As expected, the men were stronger than the women for both strength measures (P < 0.05).


                              
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Table 1. Subject characteristics

Constant-force task

The ability to sustain a constant force was compared at six different target forces (5, 10, 20, 35, 50, and 65% MVC). Figure 2A shows a representative performance of an old subject for a constant-force trial along with the EMG for the major elbow extensor and flexor muscles. When subjects attempted to exert a steady force (Fig. 2A, bottom trace), the force fluctuated around some relatively constant value. The variability of the mean force around each target level was expressed as the coefficient of variation, which was used as an index of the steadiness for the isometric contraction.



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Fig. 2. Representative data for two old adults, one from a constant-force trial at 35% maximum voluntary contraction (MVC; A) and the other from a constant-load trial at 15% one-repetition maximum (1-RM) load (B). The first 5 traces in each column are interference electromyographic (EMG) signals from the triceps brachii, the brachialis, the brachioradialis, the long head of the biceps brachii, and the short head of the biceps brachii, respectively. A, bottom trace: force exerted during the constant-force trial. B, bottom two traces: wrist acceleration and elbow-joint angle, respectively. The upward slope on the elbow-angle trace indicates flexion as the load was raised, which corresponded to a shortening contraction by the elbow flexor muscles. When the load was lowered, these muscles performed a lengthening contraction. The fluctuations in the acceleration record were greater during the lengthening contraction.

Figure 3A shows the coefficient of variation across target forces for the young and old subjects. There was no age-related difference in the coefficient of variation (P = 0.08) across these target forces. The average coefficient of variation for all subjects increased with target force (P < 0.01), ranging from 1.64 ± 0.14% at the 5% force to 3.13 ± 0.15% at the 65% force. However, the differences between 5 and 10% MVC and between 20 and 35% MVC were not statistically significant. Correspondingly, the EMG increased with target force (P < 0.001) except between the 5 and 10% MVC forces (Fig. 3, B and C). The average EMG for the four elbow flexor recordings (short and long heads of biceps brachii, brachialis, and brachioradialis) ranged from 3.91 ± 0.38% at the 5% force to 57.2 ± 1.61% at the 65% force for the young subjects and from 4.84 ± 0.45% at the 5% force to 55.1 ± 1.84% at the 65% force for the old subjects. The average EMG for the triceps brachii was less than those for the elbow flexor muscles at all target forces (P < 0.001). In agreement with the lack of differences between groups for the coefficient of variation, no group differences were found (P = 0.11) for the average EMG (Fig. 3, B and C). Additionally, the average EMG covaried among the four flexors for both groups across the five target forces (P = 0.72).



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Fig. 3. A: coefficient of variation (CV) for constant-force contractions performed by young and old adults. Values are means ± SE. CV indicates normalized variability in force exerted by the elbow flexor muscles at 6 target forces. The average (young + old) CVs at the 6 target forces were 1.64 ± 0.14, 1.56 ± 0.13, 2.11 ± 0.09, 2.31 ± 0.13, 2.77 ± 0.16, and 3.13 ± 0.15%. B and C: average EMG across target forces for young and old subjects, respectively. The average EMGs collapsed across 4 elbow flexor recordings, and for both groups of subjects at the 6 target forces the EMGs were 4.39 ± 0.30, 6.69 ± 0.39, 12.3 ± 0.53, 22.4 ± 0.68, 38.7 ± 1.14, and 56.1 ± 1.22%. This figure shows that there were no age-related differences in isometric steadiness or EMG. BBS, short head of biceps brachii; BBL, long head of biceps brachii; BRR, brachioradialis; BRA, brachialis; TRI, triceps brachii.

Constant-load task

The ability to perform steady, constant-velocity shortening and lengthening movements was assessed at loads of 10, 15, 25, and 35% of 1 RM. Figure 2B shows representative data from an old subject performing a constant-load trial. Steadiness was characterized as the standard deviation of acceleration (Fig. 2B, second from bottom trace). For comparison across loads and subjects, the standard deviation of acceleration was normalized relative to the load that was lifted. For each subject, the standard deviation for the middle four seconds of each phase (lifting and lowering) was averaged across the three trials at each load. The average values of the normalized standard deviations for acceleration were determined at each load and compared between the two groups of subjects (Fig. 4). For the shortening contractions, the old subjects were less steady than the young subjects at the 10 and 15% 1-RM loads (Fig. 4A). The normalized standard deviations for the old subjects were 0.108 ± 0.015% at the 10% load and 0.076 ± 0.011% at the 15% load compared with 0.068 ± 0.008% and 0.046 ± 0.005%, respectively, for the young subjects. For both groups of subjects, however, the standard deviation at the 10% 1-RM load was significantly greater than the standard deviations for the 25 and 35% loads. Furthermore, the standard deviation at the 15% 1-RM load was greater than the standard deviations for the 25% and 35% loads for the old subjects.



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Fig. 4. Normalized standard deviation (SD) of acceleration during shortening (A) and lengthening (B) contractions performed by young and old adults during the constant-load task. Values are means ± SE for the middle 4 seconds of each phase of the task. The normalized SDs of acceleration for the shortening contractions at the 4 loads were as follows: young, 0.068 ± 0.008, 0.046 ± 0.005, 0.042 ± 0.006, and 0.047 ± 0.006%; old, 0.108 ± 0.015, 0.076 ± 0.011, 0.049 ± 0.007, and 0.040 ± 0.004%. The normalized SDs of acceleration for the lengthening contractions at the 4 loads were as follows: young, 0.072 ± 0.008, 0.050 ± 0.005, 0.035 ± 0.003, and 0.037 ± 0.006%; old, 0.140 ± 0.021, 0.099 ± 0.016, 0.061 ± 0.010, 0.and 042 ± 0.006%. Old subjects were less steady than young subjects when raising and lowering light loads. *, significantly different from young subjects, P < 0.05.

Similarly, the standard deviations for the lengthening contractions were significantly greater (P < 0.01) for the old subjects compared with the young subjects at all loads except the 35% 1-RM load (Fig. 4B). Across loads within each age group, subjects were less steady at the 10% load than at the 25 and 35% loads during the lengthening contraction. The normalized standard deviation at the 10% load was 0.072 ± 0.008% for the young subjects compared with 0.037 ± 0.006% at the 35% load, whereas the values ranged from 0.140 ± 0.021 to 0.042 ± 0.006% for the old subjects. Additionally, the old subjects were less steady at the 15% load (0.099 ± 0.016%) than at the 25 and 35% loads. There were also some statistically significant differences in the normalized standard deviations across contraction types (shortening and lengthening) at each load. The standard deviation for the old subjects was greater when they performed the lengthening contraction at the 10 and 15% loads and the standard deviation was greater for the young subjects when they performed the shortening contraction at the 35% load.

These differences in the normalized standard deviations of acceleration between the two groups of subjects were accompanied by differences in the average EMGs of the involved muscles. For each trial, the EMG was rectified and an average value was determined for each 100-ms interval, which yielded 60 data points for each phase of the movement (Fig. 5). The first 50% of the movement involved the shortening contraction whereas the second 50% corresponded to the lengthening contraction. These 120 data points were averaged across the subjects in each group for each of the four loads. To perform statistical analyses on these EMG data, the five 100-ms data points in the middle of each phase were averaged for each trial. These data were then averaged between the three trials for each subject and the subject data were averaged within each age group for each phase. Figure 5 shows the resulting average EMG records for the young and old subjects at the lightest and heaviest loads. For all the elbow flexor muscles, the average EMG increased from a minimum at the onset of the movement to a peak at the transition (50%) from the shortening to the lengthening contraction. For most muscles, the average EMG decreased in amplitude at the onset of the lengthening contraction because of the lesser EMG that is required to exert the same muscle force with a lengthening contraction (Bigland and Lippold 1954).



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Fig. 5. Average EMG for elbow flexor and extensor muscles of young and old subjects during the constant-load task for the lightest (10% 1-RM) and heaviest (35% 1-RM) loads. Each panel includes the average EMG for the 3 main elbow flexor muscles (biceps brachii, brachialis, and brachioradialis) and the antagonist (triceps brachii). Each data point corresponds to a 100-ms average of the EMG record, averaged across subjects .

The distribution of activity among the elbow flexor muscles during the constant-load task was different between the two groups of subjects. The most pronounced difference was for the brachialis muscle. The relative activation of brachialis was greatest among the muscles for the young subjects and least for the old subjects across the four loads that were examined (Fig. 5). For the young subjects, the average EMG was significantly less for brachioradialis compared with brachialis (P = 0.007), but there was no difference for biceps brachii (P = 0.09 and 0.13 for the short and long heads, respectively). In contrast, the average EMG for brachialis and brachioradialis was less than that for the short and long heads of biceps brachii for the old subjects.

The old subjects relied most on the two heads of the biceps brachii when lifting the 10% 1-RM load (P < 0.05 vs. brachialis), but activated both the biceps brachii and the brachioradialis at similar levels when lifting the heavy load (35% 1-RM). Nonetheless, the amplitude of the average EMG was much less (P < 0.01) for the old adults compared with the young adults for the heavy load (compare the peak values at 50% time in Fig. 5). The young subjects exhibited an interesting pattern during the lengthening contraction with the light load when the average EMG for the biceps brachii declined at a lesser rate than that for the brachialis and brachioradialis. When performing the lengthening contraction, both groups of subjects decreased the EMG of the biceps brachii to a lesser extent than that for the brachialis and brachioradialis muscles (P < 0.01). Both groups of subjects used minimal activation of the triceps brachii muscle with no difference between the age groups (P = 0.97).

When the average EMG records were compared across loads for each muscle, it was obvious that the young subjects scaled the activity proportionately (Fig. 6). As a percentage of the EMG recorded during the MVC, the brachialis EMG for the young subjects reached the greatest value at each load compared with the other muscles. In contrast, the old subjects scaled the activity of the brachioradialis to the greatest extent (Fig. 6B) and that of the brachialis the least (Fig. 6C). The average EMG for the brachialis only reached ~20% of the MVC value with the heaviest load (35% 1-RM). The old subjects used a similar amount of biceps brachii EMG for the two lightest loads. These differences in the distribution of activity among the synergist muscles is illustrated in Fig. 7, which shows the covariation in average EMG for the biceps brachii and the brachialis when the subjects lifted and lowered the 25% 1-RM load. Not only were the peak values of the EMG different for the two groups of subjects, but the slope of the relationship was also different. The reduced slope exhibited by the old adults was due to a diminished role for the brachialis muscle in the task. In contrast, both groups activated the antagonist muscle to similar levels and the amplitude of the EMG for the triceps brachii never reached >12% of that value recorded during an extension MVC.



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Fig. 6. Average EMG for biceps brachii (A), brachioradialis (B), brachialis (C), and triceps brachii (D) for young and old subjects performing the constant-load task. In each panel, the 4 records correspond to the average EMG for the 4 loads (10, 15, 25, and 35% 1-RM).



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Fig. 7. Covariation in average EMG for biceps brachii and brachialis when lifting (black symbols) and lowering (white symbols) a 25% 1-RM load. Each data point represents the average EMG for 200 ms.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The main findings of this study were that 1) age had no effect on the ability of adults to maintain steady, submaximal isometric forces with the elbow flexor muscles; 2) the normalized variation in isometric force around a submaximal target was least at low forces in the elbow flexor muscles, which is opposite to that observed for a hand muscle; 3) age influenced the fluctuations in wrist acceleration during slow anisometric contractions, particularly during the lengthening phase with light loads (10, 15, and 25% 1-RM); and 4) the reduced steadiness exhibited by the old adults was accompanied by differences in the relative EMG of the elbow flexor muscles. Contrary to expectations, these results indicate that steadiness does vary with age for tasks involving a flexor torque around the elbow joint. The absence of a common effect on the isometric and anisometric tasks is consistent with previous reports of different control strategies for these two tasks (Buchanan and Lloyd 1995; Tax et al. 1989, 1990a,b). However, the distribution of muscle activity among the elbow flexor muscles during the anisometric tasks differed for the young and old subjects.

Comparison with steadiness of hand muscles

Previous studies indicated that old adults are less steady than young adults when exerting low abduction forces with the index finger (Burnett et al. 2000; Galganski et al. 1993; Keen et al. 1994). In contrast, during isometric contractions with the elbow flexor muscles for submaximal forces up to 65% MVC, we found no differences in steadiness caused by age. This difference between the first dorsal interosseous muscle and the elbow flexor muscles was characterized by the relationship between normalized steadiness (coefficient of variation) and exerted force (% MVC). The coefficient of variation was least at low forces and increased with force for the elbow flexor muscles (Fig. 3) whereas the coefficient of variation is greatest at low forces and decreases with force for the first dorsal interosseous muscle (see Fig. 2B in Galganski et al. 1993). This difference, however, was attributable to differences in the standard deviation of the force fluctuations across the submaximal forces. Because the standard deviations were relatively constant (~0.3 N) for the first dorsal interosseous muscle for target forces up to 50% MVC (Galganski et al. 1993), calculation of the coefficient of variation declined as the target force increased. Conversely, the standard deviations increased substantially with target force for the elbow flexor muscles. For example, for the young subjects the standard deviation increased from 0.28 N at the lowest target force (5% MVC) to 5.45 N at the highest target force (65% MVC). The increase in the standard deviations was greater than the relative increase in target force, which resulted in an increasing coefficient of variation as a function of target force.

There are at least two possible explanations for the differences in steadiness between these muscles: the discharge characteristics of motor units and muscle redundancy. The first possible factor has to do with the relative contributions of discharge rate modulation and recruitment of motor units to the net muscle force. The gradation of muscle force in hand muscles seems to depend primarily on the recruitment of motor units during isometric contractions up to ~50% MVC (DeLuca et al. 1982; Kanosue et al. 1979; Kukulka and Clamann 1981). In contrast, the upper limit of motor unit recruitment in proximal arm muscles is ~85% MVC. The reduced recruitment range of hand muscles means that low forces involve the recruitment of relatively larger motor units. For example, based on the exponential relation between recruitment threshold and motor unit force (Stuart and Enoka 1983; Walmsley et al. 1978), the exertion of force at 10% MVC with a hand muscle would involve a greater proportion of the motor unit pool than would a proximal arm muscle. At 10% MVC force therefore, the last-recruited motor unit in the hand muscle would have a larger relative peak-to-peak force than would the proximal arm muscle (Fuglevand et al. 1993). Because fluctuations in force are influenced by the unfused contractions of the most recently recruited motor units (Allum et al. 1978), the recruitment of larger motor units at the same relative force would likely contribute to greater force fluctuations. However, the standard deviation of the force fluctuations remained relatively constant for the first dorsal interosseus muscle but increased for the elbow flexor muscles.

The second potential factor that may contribute to differences in isometric steadiness between the first dorsal interosseous muscle and the elbow flexor muscles is the number of muscles that contribute to the net force. The first dorsal interosseous muscle by itself accounts for most of the abduction force exerted by the index finger (Chao et al. 1989), which is the task associated with differences caused by age in isometric steadiness at low forces (Burnett et al. 2000; Galangski et al. 1993; Keen et al. 1994). In contrast, when older adults were required to exert low isometric forces using a precision grip that utilized multiple intrinsic and extrinsic hand muscles (Maier and Hepp-Reymond 1995a,b), there were no age-related differences in steadiness (Cole and Beck 1994). These findings suggest that tasks involving several muscles, such as the elbow flexor tasks examined in this study, are associated with lesser fluctuations in force. However, the ability to sustain constant forces with precision grip appears to vary across tasks. For example, old adults exhibit greater force fluctuations than do young adults when grasping an object (Cole 1991; Kinoshita and Francis 1996), but not when matching the same absolute target forces (Cole and Beck 1994).

Steadiness of anisometric contractions

In contrast to the opposing slopes of the relation between steadiness (coefficient of variation) and target force for the first dorsal interosseous muscle and the elbow flexor muscles for isometric contractions, the slope of the relation was similar for these two sets of muscles when subjects performed slow anisometric contractions. Steadiness (standard deviation of acceleration) improved with an increase in magnitude of the inertial load that was lifted. Nonetheless, the old subjects were less steady than the young subjects when lifting and lowering light loads, and the old adults were less steady when performing lengthening contractions compared with shortening contractions.

The greatest difference in muscle activity between the two age groups during anisometric contractions was in the overall amplitude of the brachialis EMG. Although the brachialis EMG was recorded with an intramuscular electrode and the EMG for the other muscles was recorded with surface electrodes, this difference is unlikely to account for the observed difference in EMG amplitude. First, the EMG of all muscles scaled proportionally with the net force during isometric contractions for both groups of subjects (Fig. 3). Second, we observed no group differences in absolute EMG during maximal voluntary contractions for any muscle (P < 0.05).

Another difference between the two groups of subjects was in the magnitude of EMG used to lift the same relative loads. This difference was most evident at the two heaviest loads (25 and 35% 1-RM; Figs. 5 and 7) and was probably caused by the lower 1-RM strengths of the old subjects. There was no difference between the young and old subjects in MVC force and EMG, which served as the denominator for normalization of the EMG. However, the 1-RM load for the old adults was significantly less than that for the young adults (Table 1). This meant that the loads lifted with anisometric contractions were a lower fraction of MVC force compared with that for the young subjects. As a consequence, the old adults did not need to activate as much muscle mass to lift the lower relative loads.

Despite the capacity of all subjects to scale muscle activity proportionally (Fig. 3), the old adults did not use this strategy when lifting various submaximal loads (Fig. 7). They did scale the EMG of the brachioradialis as a function of load (Fig. 6C) but not that of the biceps brachii (Fig. 6A) or the brachialis (Fig. 6C) muscles. The old adults activated the biceps brachii similarly with the two lightest loads and modulated the level of the brachialis EMG minimally across loads. Because the cross-sectional areas of the biceps brachii and the brachialis are similar and much greater than the brachioradialis (An et al. 1981; van Bolhuis and Gielen 1997; van Bolhuis et al. 1998), these EMG data suggest that the old adults relied most on the biceps brachii to lift the various loads. In contrast, the young subjects activated the brachialis muscle to greater relative levels when lifting these submaximal loads (Fig. 5). The different strategies used by the young and old adults undermine the existence of a general scheme that can account for the role of mono- and biarticular muscles in motor performance (van Bolhuis et al. 1998).

This difference in the distribution of muscle activity probably contributed to the greater fluctuations in acceleration exhibited by the old adults during anisometric contractions. Because the distal attachment of the biceps brachii is farther from the elbow joint than the brachialis (An et al. 1989; Ettema et al. 1998; Murray et al. 1995), the greater moment arm for the biceps brachii would enhance acceleration at the wrist because of a given fluctuation in muscle force. The greater wrist accelerations exhibited by the old adults therefore may be at least a partial consequence of their greater reliance on the biceps brachii to perform anisometric contractions.

The finding that steadiness was less during lengthening contractions than during shortening contractions for old adults, but was not different for young adults, is consistent with our results for the first dorsal interosseous muscle (Burnett et al. 2000; Laidlaw et al. 2000). We found a strong association between steadiness (standard deviation of position) and variability in the rate at which motor units discharge action potentials when performing anisometric contractions with light loads. For example, when old adults changed from a shortening to a lengthening contraction with the first dorsal interosseus muscle, the average discharge of motor units decreased from 16.5 to 12.1 Hz and the coefficient of variation increased from 30 to 42%. Such discharge rate characteristics would likely place the motor unit low on its frequency-force relation (Fuglevand et al. 1999) and exacerbate the contribution of these units to fluctuations in force and acceleration. Based on these associations, it appears that the differences in anisometric contraction steadiness caused by age are at least partially influenced by the discharge behavior of the active motor units. This possibility, however, needs to be examined directly in the elbow flexor muscles.

In conclusion, there are significant task-dependent differences in steadiness between young and old adults using elbow flexor muscles. We found no differences caused by age when subjects performed isometric contractions. However, there were significant effects caused by age when subjects lifted light loads with anisometric contractions. The differences in anisometric steadiness appear to be associated with differences in the activation of the elbow flexor muscles. These results suggest that the ability to control isometric and anisometric contractions with the elbow flexor muscles does not change in parallel with age.


    ACKNOWLEDGMENTS

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


    FOOTNOTES

Address reprint requests to R. M. Enoka.

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 20 September 1999; accepted in final form 10 January 2000.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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