The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 58:M536-M541 (2003)
© 2003 The Gerontological Society of America
Bilateral Index Expressions and iEMG Activity in Older Versus Young Adults
Juliane P. Hernandez,
Nicolle L. Nelson-Whalen,
Warren D. Franke and
Scott P. McLean
Department of Health and Human Performance, Iowa State University, Ames.
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Abstract
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Background.This study investigated the hypothesis that expressions of maximal and submaximal bilateral indices would not differ between older and young participants.
Methods.Twenty older (73.3 ± 4.4 years) and 21 younger (22.4 ± 0.9 years) participants performed maximal voluntary isometric contractions of the elbow flexor muscles, using the right arm only, left arm only, and both arms simultaneously. The participants were asked to repeat these contractions at what they perceived to be 25%, 50%, and 75% of their maximal voluntary isometric contraction levels.
Results.Significant bilateral deficits (p <.05), defined as a bilateral index <0, existed at maximal and submaximal intensities, but the submaximal deficits (14–18%) were larger than the maximal deficits (11%). Normalized integrated electromyographic values tended to be higher for unilateral trials than for bilateral trials at all submaximal intensity levels. There were no significant differences between the older and young participants.
Conclusions.Despite the decrease in the size of fast twitch motor units associated with aging, bilateral deficits exist in older adults, do not differ from those observed for younger adults, and remain larger for submaximal intensities.
MUSCULAR forces produced during maximum voluntary contractions (MVCs) can be 3–25% smaller during simultaneous bilateral exertions than during independent unilateral exertions of homologous limbs (1). This phenomenon, described as a bilateral deficit, has been observed in young adults using small muscles (2,3) and large muscles (4,5) during isometric (3,5) and isokinetic contractions (4,6,7). Bilateral deficits suggest a neuromuscular limitation preventing maximal stimulation of all motor units during bilateral contractions. Specifically, several authors have attributed the bilateral deficit to an inability to recruit high threshold motor units (4,7–11,15).
If the bilateral deficit is due to the inhibition of fast twitch motor units, older people should have a reduced bilateral deficit compared with younger people because aging has been associated with a decrease in size of high threshold motor units (12–14). However, the existing data are equivocal. Hakkinen and colleagues (9–11) demonstrated no bilateral deficit in older participants during maximal effort isometric knee extension. Conversely, Owings and Grabiner (15) reported the existence of bilateral deficits of 11.1% and 12.9% for the left leg and right leg, respectively, during maximal effort isometric knee extension.
To date, the majority of investigations have focused on maximal exertions during bilateral tasks (1–11,15,17–21). However, the existence of a bilateral deficit at maximal effort has little influence on the performance of most activities of daily living. Given that the bilateral deficit may be caused by an inability to fully recruit high threshold motor units during a bilateral task, the bilateral deficit should not exist at submaximal intensities of effort because the use of fast twitch motor units would be minimal at low intensities (e.g., 25% MVC). However, the observations that the bilateral deficit exists at maximal and submaximal intensities (16) and that submaximal deficits tended to be larger than maximal deficits (22) contradicted the explanation that the bilateral deficit is due to an inhibition of fast twitch motor units. Furthermore, it contradicted the suggestion that the bilateral deficit should decrease in older adults as a result of an atrophy of fast twitch motor units as age increases.
The presence of a bilateral deficit could have a profound effect on older adults' ability to perform bilateral activities and in some instances could place them at a greater risk of injury. Given the equivocal nature of data on bilateral maximal exertions and lack of data on bilateral submaximal exertions in older adults, a need exists to better understand how older adults perform bilateral exertions. Therefore, the purpose of this investigation was to determine if older adults exhibit bilateral deficits at maximal and submaximal levels of intensity similar to those of younger adults. We hypothesized that bilateral deficits exist at maximal and submaximal levels of effort in older adults and would not differ from those in younger adults. Furthermore, we hypothesized that the magnitude of the bilateral deficit would increase with decreasing effort.
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Methods
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Participants
Twelve female and 8 male healthy, physically active adults over the age of 60 years and 16 female and 5 male physically active college age adults volunteered for this experiment (Table 1). The older adults were recruited from an on-campus exercise program and were involved in a regular regimen of bilateral strength training. Informed consent, as approved by the Institutional Review Board of Iowa State University, was obtained from each participant prior to study participation. The participants reported no prior musculoskeletal or neuromuscular disease or injury. Three of the 41 participants were left-hand dominant on the basis of verbal inquiry as to the preferred hand for writing.
Instrumentation
The instrumentation and protocol were similar to those described previously (16,22). Each participant performed right and left unilateral and bilateral isometric contractions of the elbow flexors. Participants were seated on a "preacher curl" bench (Figure 1) with upper arms parallel and elbows flexed to 90°. Separate cables instrumented with strain-gauge force transducers (Interface, Inc., Scottsdale AZ) were attached between wristbands and a wall to measure pulling force (Figure 1). Participants were instructed to supinate their forearms until their palms faced inward and make soft fists with their hands. They then exerted isometric muscle contractions by pulling on the wristbands. Force transducers were sampled at a frequency of 1000 Hz.
Electromyographic (EMG) activity of the biceps brachii was measured by means of bipolar surface electrodes and recorded from each arm independently. At each site, two Ag–AgCl differential surface electrodes with a diameter of 8 mm were attached on the skin over the center of the muscle belly along the long axis of the muscle. The electrode centers were placed 2.5 cm apart. A single reference electrode was placed on the distal end of the left ulna. EMG data were collected at a rate of 1000 Hz and high-pass filtered with a cutoff frequency of 5 Hz to remove movement artifact. Force data and EMG data were collected simultaneously for a period of 3 seconds.
Procedures
Participants were asked to perform maximal exertion trials of isometric elbow flexion while seated in the previously described apparatus. They gradually increased force from rest to a maximal effort within a 3-second period. Participants verbally signaled when they had achieved maximal effort, at which time the 3-second trial was collected. Participants performed three trials each of the following maximal effort conditions: bilateral, unilateral with the dominant arm, and unilateral with the nondominant arm. A counterbalance design determined the order of the conditions among participants.
The remaining trials of the experiment involved a series of isometric elbow flexion contractions of submaximal effort in which participants produced bilaterally and unilaterally (with dominant and nondominant arms) what they perceived to be 25%, 50%, or 75% MVC. Participants were asked to generate each contraction three times, with a minimum of 60 seconds of rest between trials. Heart rate was monitored continuously to ensure that appropriate rest was taken to minimize fatigue effects. The order of the submaximal trials was determined by a counterbalance design.
Initially, a single submaximal trial was provided as a practice trial for participants. They were instructed to produce the designated level of contraction and received feedback about the percentage of maximal force achieved on this trial. Following the practice trial, participants were no longer given feedback regarding their performance, nor were they given verbal encouragement during the data collection period. Prior to each trial, participants were instructed to gradually increase force from rest to the specified force level within 5 seconds (a longer ramp period was provided to allow the participants to evaluate their efforts consciously). When they felt they had achieved and were maintaining the appropriate level of exertion, they verbally signaled to the experimenter to begin data collection.
Analysis
Force data from each trial were processed by averaging the final 2.5 seconds of data. The direct current bias was removed from the EMG data, which were then full-wave rectified and integrated over the 2.5 second interval identified from the force signal. Data were averaged over three trials. A 2 x 2 x 2 x 4 (Group x Arm x Mode x Level) mixed model analysis of variance (ANOVA) was conducted by using force as the dependent measure. Here, group was young versus old, arm was dominant versus nondominant, mode was unilateral versus bilateral, and level was 25, 50, 75, and 100% MVC.
Bilateral index (BI) values were calculated as originally defined by Howard and Enoka (21) for each intensity level by using absolute forces:
where RBL was the force produced by the right arm during bilateral exertion, LBL was the force produced by the left arm during bilateral exertion, RUL was the force produced by the right arm during unilateral exertion, and LUL was the force produced by the left arm during unilateral exertion. When the BI is calculated, a positive value reflects a bilateral facilitation, whereas a negative value reflects a bilateral deficit. The BI was subsequently parsed into perceptual and physiological components. As a way to define the perceptual component, mode forces were computed by normalizing measured absolute forces by their respective mode (unilateral or bilateral) maximum. The mode BI (MBI) was then computed by using Equation 1, substituting mode forces for absolute forces. The physiological component (PBI) was then defined as the difference between the BI and MBI (22).
Separate 2 x 4 (Group x Level) mixed model ANOVAs were used to evaluate the BI calculated by using absolute forces and forces normalized to their respective mode maximum (MBI). Biceps integrated EMG (iEMG) data were analyzed by using a 2 x 2 x 2 x 4 repeated measures ANOVA (Group x Arm x Mode x Level). Pair-wise comparisons using estimated marginal means were used when post hoc procedures were necessary to locate significant differences. Statistical significance was set at p <.05.
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Results
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No significant age effect was found for absolute force, mode force, BI, MBI, PBI, or muscle activity. Force decreased (p =.000) as perceived effort decreased from maximal effort to 25% maximal effort (Figures 2 and 3). Participants produced 50% perceived effort most accurately while underestimating 75% perceived effort and overestimating 25% perceived effort (Figures 5 and 6). Unilateral exertions produced more force than bilateral exertions for dominant and nondominant arms at each intensity level for both groups (p =.000) (Figures 2–5
). Normalized iEMG activity paralleled the changes in force production, increasing for both groups as effort increased (Figures 7 and 8) (p =.000). For all submaximal efforts, iEMG activity was significantly higher in the dominant unilateral trial than in the bilateral trial (p =.000). Although the relationship was the same for the submaximal trials with the nondominant arm, the values failed to achieve statistical significance (p =.060).
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Figure 2. Absolute force values at each intensity level for the young participants (mean ± SEM). MVC = maximum voluntary contraction
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Figure 3. Absolute force values at each intensity level for the older participants (mean ± SEM). MVC = maximum voluntary contraction
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Figure 5. Mode force values at each intensity level for the young participant (mean ± SEM). MVC = maximum voluntary contraction
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Figure 6. Mode force values at each intensity level for the older participants (mean ± SEM). MVC = maximum voluntary contraction
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Figure 4. Bilateral index (BI) values (BI, mode BI, physiological component BI) at each intensity level for young (Y) and older (E) participants (mean ± SEM). MVC = maximum voluntary contractions
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Figure 7. Integrated electromyographic (iEMG) activity of the biceps brachii at each intensity level for the young (mean ± SEM). MVC = maximum voluntary contraction
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Figure 8. Integrated electromyographic (iEMG) activity of the biceps brachii at each intensity level for the older participants (mean ± SEM). MVC = maximum voluntary contraction
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Significant bilateral deficits existed at all intensity levels (p = 0.027) for both groups (Figure 4). The BI varied across effort, but it was not significantly different. However, across the range of perceived efforts, these values ranged from -11.1 to -17.4 for the young participants and from -11.9 to -15.9 for the older participants and were consistent with the previously reported values (22).
The physiological component of the BI remained relatively constant at approximately 11% across effort levels while the perceptual component decreased from maximal effort to 25% effort, suggesting that the greater deficit observed in lower effort actions was associated with deterioration in the perceptual aspects of the activity (Figure 4).
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Discussion
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The purpose of this study was to investigate the existence of the bilateral deficit in maximal and submaximal actions in younger and older adults. It was hypothesized that the bilateral deficit would exist in older adults and that, as in younger adults (22), the magnitude of the bilateral deficit would increase as the level of effort decreased. Both of these hypotheses were supported. These observations have important implications for older adults. Given the decline in strength associated with increasing age (12–14), the bilateral deficit would further compromise strength, thereby placing this population at increased risk of injury when simultaneous bilateral activity is necessary to complete a movement (e.g., rising from a chair).
Maximal Voluntary Contraction
Evidence of a bilateral deficit in older adults has been equivocal (9,10,15). Whereas Hakkinen and colleagues (10) reported no bilateral deficit in the older adults for a knee extension task, Owings and Grabiner (15) reported a significant bilateral deficit when a similar task was used. However, the use of a knee extension task may have contributed to the equivocal nature of the data in previous studies. A recent review found that the bilateral deficit is more consistently observed in the upper extremities than the lower extremities (23), suggesting that using an upper extremity exercise may improve the ability to establish whether the bilateral deficit can exist in older adults. From a practical standpoint, the investigation of upper extremity activities is useful because many activities of daily living are performed with the upper extremities (e.g., opening a jar or using one's arms for assistance when rising from a chair). In addition to bilateral deficits found in two-hand tasks, force deficits have been observed for finger groups within a hand (24). A finger force deficit occurs when a finger produces less force in a multifinger maximal task than in its single-finger maximal task. Li and colleagues concluded that bilateral deficits and force deficits, although being of different origin, have a summation effect that could cause further detriment in the performance of activities of daily living in the older population (25). The present study used an elbow flexion task that was familiar to the participants and conformed to the recommendation of Jakobi and Chilibeck (23). Our results suggest that older individuals do experience a bilateral deficit and that it is similar to the deficit observed in younger individuals. The significant bilateral deficit of 11.9% experienced by the older adults was not statistically different from the 11.1% deficit in the younger adults and is comparable in magnitude with previously reported values (15,16,22).
Although 12 of the 20 participants in the older group were male and only 5 of the 21 young participants were male, there was no difference in the overall group strength values. Our older participants had been involved in a regular strength and cardiovascular exercise program for at least 1 year prior to the study. This may explain the lack of difference in BI measures. Both Owings and Grabiner (15) and Hakkinen and associates (9–11) reported subjects who were living independently and who were recreationally active, but who were not performing regular bilateral strength training movements.
Submaximal Muscle Strength
Recently, Vint and McLean (22) showed that bilateral deficits were larger during submaximal than maximal efforts in young, healthy adults. The physiological component of the bilateral deficit was approximately 11% for all effort levels. Given the stable nature of this component of the deficit, it was concluded that the physiological component was not under conscious control and therefore would always compromise the ability to produce bilaterally activated force. Furthermore, Vint and McLean concluded that the decrease in the BI with decreasing effort must have been due to the subjects' perceiving the submaximal effort levels as more difficult under the bilateral condition. A similar, nearly constant 11% physiological deficit component was observed in the present study while the perceptual component varied across effort levels supporting Vint and McLean's findings (Figure 4). Furthermore, age did not affect this.
Given the reliance of submaximal efforts on perception, it would be possible for a submaximal deficit to exist in older adults even though fast twitch fibers may be compromised by sarcopenia. However, given the constant physiological component found in our older participants, it appears that no such statement can be validated. The current investigation demonstrated the expected increase in deficit for the younger participants as level of effort was decreased. Although no significant differences were noted between groups, a comparison of older participants and younger participants revealed a similar deficit at 75% MVC, a tendency toward a greater deficit at 50% MVC, but a tendency toward a smaller deficit at 25% MVC. In light of the constant physiological component, the erratic nature of these data suggests that perception was an issue for the older adults. For example, the discrepancy at 25% MVC in the older population could indicate a greater decrease in the ability of the older group to perceive lower intensity levels accurately. When asked to produce a force of 25% MVC, the older individuals actually produced forces closer to 50% MVC (Figure 5).
Despite the reduction in the bilateral deficit at 25% MVC, it was still more than 14%. For young adults this poses few problems, but for older adults (particularly frail older adults) who may have a decreased functional capacity caused by decreased overall strength (26), the performance of any submaximal task is nearer to their functional limit than for young adults. Given the existence of a submaximal bilateral deficit, the performance of a coupled bilateral action (i.e., similar actions performed by both limbs, simultaneously) would require effort closer to the functional capacity. Although no problems should prevent completion of the task if no unexpected events occur, the reduced physiological reserve caused by performing at a higher relative force may put them at risk in situations where they have to adapt to unexpected stimuli during the movement. To better understand the implications of the submaximal bilateral deficit and perceptual issues in older adults, we must evaluate how efforts of equal absolute intensity performed under bilateral and unilateral conditions are perceived. Furthermore, future work should consider the implication of the bilateral deficit on activities of daily living such as the sit-to-stand movement and whether any strategies could be employed to decouple the bilateral actions of the movement.
Conclusions
In summary, given the constant physiological component of the bilateral deficit, these data suggest that the inability to fire fast twitch motor units under bilateral activation was not the explanation of the bilateral deficit. Furthermore, the similarity in the deficit in older and younger adults supports this conclusion. More importantly, the data presented here substantiate the existence of a submaximal bilateral deficit and that this deficit is minimally affected by age in our participants.
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Acknowledgments
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Address correspondence to Juliane P. Hernandez, MS, 283 Forker Hall, Department of Health and Human Performance, Iowa State University, Ames, IA 50011. E-mail: juliane{at}iastate.edu
Received June 25, 2002
Accepted October 18, 2002
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Abstract
Methods
