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a Biomechanics Laboratory, East Carolina University, Greenville, North Carolina
Tibor Hortobágyi, 251 Sports Medicine Building, East Carolina University, Greenville, NC 27858 E-mail: hortobagyit{at}mail.ecu.edu.
Decision Editor: John A. Faulkner, PhD
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Abstract |
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IT is well established that the magnitude and rate of maximal force production are substantially reduced in old, compared with young, skeletal muscle (1)(2)(3)(4)(5)(6)(7). These impairments in maximal strength capabilities have been attributed to a reduced muscle mass, stemming largely from fast-twitch fiber atrophy (8)(9)(10). Increasing maximal strength of aged muscle is therefore important, but it is surprising that most often the gains in maximal strength are not related to improvements in functional capacity (6)(11)(12)(13)(14).
Indeed, one would not expect that the decline in one specific measure of maximal capability of the aged neuromuscular system would account for most or all of the variability in declines of function. This is because aging causes a decline, not only in the quantity of muscle that would affect maximal strength, but also in the sensory system. Impairments in the sensory system would affect feedback mechanisms that are important in the control of submaximal forces. With age, joint-position sense, touch, kinesthesis, and proprioception become impaired (15)(16)(17)(18)(19)(20). In addition, aging-induced motor unit remodeling increases innervation ratio, which in turn increases motor unit force (21). Such changes in the sensory and motor systems make the hypothesis conceivable that aging impairs the regulation of submaximal force. Increased variability of submaximal finger abduction forces in elderly, compared with young, adults provides direct evidence to support this hypothesis (22)(23). One aim of the present work was to expand on these findings by examining the accuracy and steadiness at submaximal quadriceps forces in young and older subjects. We were especially interested in force accuracy and steadiness at low forces as most daily activities occur at a fraction of maximal strength (1) and previous studies also have shown that both force error and force variability increase with decreasing levels of force (21)(24).
Strength training has been used to moderate the losses of muscle mass, maximal strength, and functional capacity (9)(10)(11)(22)(25)(26)(27)(28)(29)(30)(31). Until recently, the greatest increases in strength and muscle mass have been observed after HI training, using about 80% of the one-repetition maximum (1-RM) load (9)(10)(25)(26)(27). Even though recent recommendations have endorsed HI strength training for aged adults (25), there is accumulating evidence that in disease- and pain-free elderly subjects, low-intensity (LI) training programs can also be effective in increasing neuromuscular performance (11)(22)(28)(29)(30)(31). However, the effectiveness of LI and HI training programs cannot be directly compared in terms of the outcome measures because, except for the findings of one study (32), the total load as well as the intensity of the contractions were both different between the training groups. Therefore, the second aim of the present work was to determine whether an LI versus an HI training program would be similarly effective in moderating the age-related losses in maximal strength. Because the practice of a specific movement is the common element that causes neural adaptation in LI and HI resistive-training programs (22), it is reasonable to hypothesize that LI and HI training programs will be similarly effective to improve submaximal force control assessed by force accuracy and steadiness.
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Methods |
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Older subjects were randomly assigned to an LI, an HI, or a nonexercising control group. All subjects underwent an initial testing session; older subjects in the training groups participated in 30 sessions of leg-press training over a period of 10 weeks and then underwent a posttraining testing session. The testing involved maximal strength, explosive strength, force accuracy, and force steadiness measurements of the quadriceps muscle. Young subjects were used as a comparison group and were tested once.
Testing Procedures
Force accuracy and steadiness.--
As a warm-up, subjects rode a bicycle ergometer at 60 rpm for 5 minutes at 1 to 2 kg resistance and performed 3 minutes of lower extremity stretching. After the warm-up, subjects were seated on the dynamometer seat with a hip angle of 1.92 radians (Kin-Com AP125, Chattecx, Inc, Chattanooga, TN). The dominant leg was tested. The center of the knee joint was aligned with the axis of the dynamometer's power shaft. Crossover shoulder straps, a lap belt, a knee strap, and an ankle cuff were used to minimize extraneous movements. The leg was fastened to the dynamometer's lever arm just above the lateral malleolus with a padded cuff that contained the strain gauge. The position of the cuff on the lever arm was adjusted individually to accommodate subjects of different size. The distance between the strain gauge and the lever arm's axis of rotation was recorded and entered in the computer as the lever arm length. The knee angle anatomical zero was set at 2.88 radians, and leg weight was measured in this position. Using these procedures, the dynamometer's software corrected the force exerted by the subject for the gravitational effects of leg mass.
Quadriceps force accuracy and steadiness were determined during isometric contractions at 1.14 radians of knee flexion as well as during isokinetic (0.262 radians · second-1) concentric and eccentric contractions over a 1.31-radian range of motion. Thus, all dynamic and isometric trials were of 5-second duration. We selected the 25-N target force because, in a pilot experiment (n = 6), some subjects were unable to complete the task at 50 N. In the pilot study, we also determined that after 10 trials, there were no further significant improvements in accuracy and steadiness within one session or in a follow-up session repeated 4 weeks later. Thus, subjects performed at least 10 familiarization trials. Five trials performed after these familiarization trials were included in the data analysis.
During testing, subjects watched the computer monitor. Horizontally across the monitor, a clearly distinguishable white line indicated the 25-N target force. Subjects were instructed to match their force production with the 25-N target force. In addition, they were instructed to attain and sustain the force being produced as smoothly and steadily as possible. Subjects did not receive any verbal feedback in addition to the visual feedback from the screen. The order of eccentric, isometric, and concentric conditions was rotated between subjects.
Maximal voluntary strength.-- After the accuracy and steadiness tests, maximal voluntary isometric and isokinetic eccentric and concentric quadriceps strength was measured on the same dynamometer described previously. These tests were done to assess the changes in muscle strength, independent of the learning that occurs with weight training, and to estimate the relationship between measures of force accuracy and steadiness. Additional warm-up included two trials of 50%, 75%, and 90% of perceived maximal intensity isometric, eccentric, and concentric contractions, separated by 1 minute of rest. Subjects were not allowed to grasp the seat and kept their hands in their laps.
Maximal isometric force was measured at 1.14 radians of knee flexion. Subjects performed three maximal effort 5-second trials with 1 minute of rest between trials. Subjects were instructed to exert maximal isometric force as fast as they could to assess explosive force characteristics of the quadriceps muscle. Subjects also performed three maximal effort eccentric and concentric isokinetic quadriceps contractions at 1.57 radians per second. We used this specific testing speed because it resembled the estimated knee-joint angular velocity of the leg press used during exercise training. Each quadriceps contraction was followed by a hamstring contraction with a 1-second pause between the efforts. There was 1 minute of rest between conditions. The order of isometric and dynamic testing was systematically alternated between subjects. The highest force value of the three trials was used in the statistical analyses. The measurements of force accuracy, force steadiness, and maximal voluntary strength were completed in one 45-minute session.
In a separate session, a 1-RM bilateral leg press was assessed in the supine position (model 7412, Cybex, Inc, Owatonna, MN). Familiarization with the equipment and the testing protocol was done in a session that preceded testing, using little or no resistance. Subjects warmed up by riding a bicycle ergometer at 60 rpm for 5 minutes at 1 to 2 kg resistance and performed 3 minutes of lower extremity stretching. After the warm-up, subjects performed ten repetitions at about 50% of the estimated 1-RM and five repetitions at 75% of the estimated 1-RM. Weight was then progressively added in increments of 10 to 45 N until the 1-RM was reached; there were approximately 3 minutes of rest between efforts. For this study, 1-RM was defined as the weight subjects could press one time. Subjects needed no more than six attempts to reach 1-RM.
Data analysis.-- Fig. 1 illustrates representative force-time curves from a young and an older subject and from another older subject, before and after exercise training. Force accuracy was defined as the absolute error from the 25-N target force for each repetition. The force signal was sampled at 1 kHz. For each data point, the absolute difference from the 25-N target force was computed. These differences were averaged within one trial, resulting in the mean absolute error. This error was then averaged for the five trials and used in the statistical analysis.
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For the maximal voluntary force efforts, forces were digitized at 1.14 radians of knee-joint position. The maximal rate of tension development (RTDmax) was determined based on the steepest rising section of the force-time curve (5)(33)(34). RTD200ms was the force subjects produced in 200 milliseconds, and RTD150N was the time it took for the subjects to attain 150 N of force on the force-time curve. Of the three maximal effort trials, the highest value was used in the statistical analysis.
Exercise training.-- All 18 subjects in the two training groups completed 10 weeks of strength training consisting of 30 sessions, using bilateral supine leg press as the exercise. Subjects were ranked based on their initial level of maximal leg press strength and randomly assigned to either an LI or HI training group, forming nine across-group subject pairs. Subjects in the HI group performed five bouts of four-to-six repetitions with 80% of the 1-RM. Subjects in the LI group performed five bouts of 8 to 12 repetitions at 40% of their maximal weight. At 2.5-week intervals, the maximal leg press was evaluated and the weights were adjusted. Because the weights were adjusted every 2.5 weeks, the number of repetitions in the LI group were also adjusted so that the total weight lifted by a given pair of subjects in the LI HI groups could be equated. Knee range of motion was about 1.57 radians. Subjects flexed and extended their lower extremity joints in about 2 to 3 seconds in response to the beats of a metronome. There were 2 minutes of rest between bouts, but subjects remained in the supine position for the duration of the exercise session. Blood pressure was monitored before, during, and after exercise.
Statistical analyses.-- All data analyses were performed with BMDP PC-90 (BMDP, Los Angeles, CA) software. Reliability of the dependent variables was determined with a paired t test from the test and retest measurements of the nonexercising older control group (n = 9). Multivariate analyses of variance were used to compare young (n = 9) and older (n = 27) subjects' maximal and explosive strength, respectively, followed by one-way univariate analyses of variance (ANOVAs). For force accuracy and steadiness, significant Hotelling's T 2 values from the multivariate ANOVAs (MANOVAs) were followed by an age (young or older) by contraction mode (eccentric, isometric, or concentric) univariate ANOVA. When appropriate, Tukey's post hoc contrast was used to determine the means that were different (p < .05).
Changes in mean training weights, the mean number of repetitions, and the mean volume of weights were analyzed with a 2 (intensity, LI or HI) by 4 (time, 2.5, 5, 7.5, or 10 weeks) ANOVA, and the 1-RM loads were analyzed with a 2 (intensity, LI or HI) by 5 (time, 0, 2.5, 5, 7.5, or 10 weeks) ANOVA. Changes in the dependent variables following 10 weeks of training were analyzed with a 2 (intensity, LI or HI) by 2 (time, before or after training) ANOVA, with repeated measures on the second factor. Significant interaction terms were followed with Tukey's post hoc contrasts. The relationship between two variables was estimated with a linear regression. The slopes of two linear regression lines were compared with a small sample t test for parallelism. For all analyses, the level of significance was set at p < .05.
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Results |
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At weeks 2.5, 5, 7.5, and 10, the mean number of repetitions per session performed by LI subjects was 43 ± 3, 48 ± 7, 54 ± 8, and 59 ± 12, respectively; HI subjects performed 23 ± 1, 26 ± 5, 27 ± 7, and 25 ± 4 repetitions, respectively. The rate of change was significantly greater in the LI than in the HI group (Group x Time interaction, p = .0164). The LI group, compared with the HI group, used significantly more repetitions: 51 ± 7 versus 25 ± 4 (group effect, p = .0001).
Fig. 3 shows that the grand mean of training volume over 10 weeks of training was similar in the LI and HI groups (19.48 ± 6 kN vs 20.2 ± 8 kN, respectively; group effect, p = .6485). Fig. 3 shows that the improvements in 1-RM load during training were similar in the two groups (Group x Time interaction, p = .0727).
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Table 3 shows that after exercise training the amount of force error associated with eccentric, isometric, and concentric force was reduced by an average of -33% ± 24% (T 2 = 31.4, p = .0039), but older subjects were still 39% less accurate than young subjects (T 2 = 67.7, p = .0003). Table 4 shows that exercise training improved older subjects' force steadiness during the initial 1 second by 21% ± 18% (T 2 = 29.4, p = .0081). For the entire 5 seconds, the improvements averaged 22% ± 21% (T 2 = 35.7, p = .0229). Overall, for the initial 1 second and entire 5 seconds of the three types of muscle contractions, older subjects were, respectively, 12% and 21% less steady than young subjects (T 2 = 22.3, p = .0033).
Fig. 4 shows the relationship between maximal isometric quadriceps force and the weight subjects achieved during the 1-RM leg press. The relationship was linear between the two variables before training, and it remained linear after training (small sample t test: t = 1.2, p = .3462 of the slopes of the two regression lines).
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Discussion |
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We do not think that the differences in relative effort required to reach the 25-N target force between the elderly and young adults can account for the large age-related differences in force error. First, the target force represented a very small fraction of the maximal force. In young subjects, the 25-N force represented only about 6%, and in the el-derly adults about 12%, of the maximal force. Second, we observed statistically nonsignificant correlations between maximal force and the amount of error. Third, maximal eccentric force was about 70% greater than the concentric force in the aged participants, so that the 25 N represented about 7% of the maximal eccentric versus the 13% of concentric force, yet the force error was almost three times greater during eccentric contractions. This latter point would then indicate that the nature rather than the magnitude of force production was more important in the amount of force error. Thus, we suggest that the observed age differences in force accuracy are not the results of methodological artifacts, but are a reflection of age-related differences in neuromuscular function.
Force accuracy has been examined under a few conditions in the upper extremity but not in the lower extremity muscles in young and old subjects (18)(24)(35). For example, Cole demonstrated that elderly subjects exerted about twice the amount of pinching force needed to prevent the slipping of an object (18). In addition, elderly, compared with young, adults used not only larger forces, but they exerted these forces for a longer-than-necessary time during precision grip tasks (35). With advanced age, computer mouse manipulation, hence, regulation of low force, becomes highly inaccurate and nonlinear compared with that seen in young people (36). One common element in these studies and the data of the present work is that force error was always in the positive direction (i.e., elderly persons under each condition applied too much force). More than necessary force used during a task makes the movement uneconomical.
We observed significantly greater error during eccentric than concentric contractions in our older, compared with young, subjects. Some subjects had great difficulty in controlling eccentric forces and produced up to 30 N of error (i.e., 25 N target force plus 30 N of error). These data may have some functional implications. Eccentric contraction of the quadriceps compared with the ankle or hip muscles is more important during various locomotory tasks, including level walking (37). An accurate scaling of these forces is especially crucial during stair descent (38) and downward stepping (39) as these motions are dominated by eccentric contraction and are associated with the highest rate of falling (40). Future studies will have to determine whether force inaccuracies actually occur in the stance phase of gait.
We also observed significantly greater force variability (i.e., less steady force production) of the quadriceps muscle in older compared with young subjects. Force variability was not related to maximal strength. Similar to the force accuracy data, we noticed that force steadiness was especially impaired in the elderly subjects during eccentric contractions, less impaired during concentric, and unimpaired during isometric efforts, compared with young subjects. These data are qualitatively similar to the impaired steadiness observed in aged subjects' hand and elbow flexor muscles using isotonic contractions (22)(23). However, the lack of differences in steadiness between young and older subjects under isometric contraction of the quadriceps is in contrast to the differences observed in the hand muscles (21). We noticed that elderly subjects had about the same amount of force variability during the initial 1 second and over the entire 5 seconds of the test contraction, suggesting that movement initiation was not more difficult for them than sustaining force. In total, it appears that elderly persons' force production is more variable under dynamic muscle contractions in upper and lower extremity muscles, including the plantar flexors (T.H., unpublished observations, 1999).
Strength training significantly reduced the amount of force error without significant changes occurring in the control group. After exercise training, older subjects were still 39% less accurate in matching 25 N of force. The significant reductions in force error with training were limited to dynamic contractions as both older and young subjects had little force error in the isometric condition (41). The training effects were independent of training intensity. As was the case before training, the error came from overshooting the target. After training, there still was three times more force error (18 N) during the eccentric compared with the concentric (6 N) task. Force error was probably not reduced by the increase in maximal strength because these two variables, as was the case before training, were uncorrelated after training. We are not aware of previous data concerning the effects of exercise training on force accuracy and aging.
Strength training also reduced the variability of force. No changes occurred in isometric force variability, but large reductions occurred in the variability of eccentric (40%) and concentric (20%) forces. These training-induced adaptations were independent of training intensity. After training, the magnitude of force fluctuation was similar during the initial 1 second and over the entire 5 seconds of the contraction. The present data confirm recent reports on improved steadiness of hand muscles after strength training in aged individuals (22). However, our observation that force fluctuation during eccentric contraction (SD of 10 N) was still twice of that during concentric contraction (SD of 5 N) after training is in contrast to the data of Laidlaw and colleagues (22). These authors reported that training eliminated the differences in steadiness between these two contraction modes. We suspect that because the magnitude of force fluctuation and maximal strength were unrelated before, and remained uncorrelated after, training and the reduction in force variability was independent of training intensity, the practice of contracting the quadriceps muscle must have played a role in the significant reductions in force variability.
Force error positively correlated with force variability before and after training. That is, the more force error a subject produced, the more variable that force was. This was the case in the aged subjects under dynamic conditions, but not under isometric conditions. Even though force error and force variability were positively correlated, it is unclear whether the same mechanism would mediate these age-related impairments.
The functional significance of reduced force accuracy and steadiness is unclear. Force error and variability both decrease with increasing force in the muscles of the arm and hand (21)(24). In the quadriceps, we also observed large force errors and variability at low forces. Future studies will have to determine whether such impairments of force regulation occur at higher quadriceps forces, resulting in the slowed and inaccurate execution of daily tasks by elderly people. Preliminary data from our laboratory suggest moderate correlations between a variety of mobility test scores and force error and force variability of the quadriceps (unpublished observations).
Muscle Strength and Rate of Tension Development
In the present study, older subjects had 42% and 72% lower maximal and explosive strength in comparison with young subjects. These data are in agreement with the age-related differences in quadriceps strength reported previously (1)(2)(3)(4)(5)(6). Because older subjects had 14.4 kg greater mean body mass than young subjects, the absolute versus relative differences in quadriceps strength between the two age groups are even more important with regard to functional activities that involve the support of body weight.
Recently published recommendations on the intensity of exercise in elderly subjects stated that approximately 80% of the 1-RM load should be used to maximize strength and functional gains following resistive exercise training (25). Indeed, there are numerous studies that reported large increases in maximal strength following HI strength training (9)(10)(26)(27)(28). However, there is also evidence to suggest that LI and very LI as well as low-frequency resistive training programs are surprisingly effective in increasing maximal strength in young and older adults (22)(28)(29)(30)(42) and may improve function in aged individuals (11)(31). For example, 4-week index finger abduction training at 10% and 80% of 1-RM significantly increased 1-RM by 23% and 38% (22), and 12-month programs at 40% and 80% of 1-RM intensity each increased the leg press of 1- RM by approximately 45% (32).
One can argue that adaptations caused by LI and HI training programs are not directly comparable because the total work done is different in the two groups. We are aware of only one study in which the subjects in the LI and HI groups performed an equal amount of total work (32). In the present study, although the intensity of exercise in the HI group was two times greater than the intensity in the LI group, maximal strength gains were virtually identical at 30%, with the total weight lifted being the same in the two groups. We observed substantially smaller strength gains than Pruitt and colleagues (32) who reported 48% and 42% gains after LI and HI training, although that program lasted 12 months. Thus, it appears that it is not the intensity of the contraction alone (43), but the total load or the practice of a certain movement (22)(42) that could also increase maximal strength. Thus, less discomfort and the reduced injury potential make LI exercise a viable alternative for elderly adults to increase muscle strength. We had one person who dropped out of the study because of the discomfort associated with HI exercise. We also noticed that at about the 8th week of HI training, all nine subjects reached a plateau, and we were unable to increase training weight thereafter (Fig. 3).
The strength training programs used in the present study had a nonspecific effect on muscle force production. This is illustrated by the finding that the linear relationship between maximal isometric force and leg press 1-RM before training remained linearly related after training; this was also noticed in a previous study in older subjects (4)(22), but not in young subjects (44). Gains in 1-RM load normally exceed the gains in isometric force (10). We interpret our data to mean that, although neural adaptation in the form of improved coordination is critical in strength gains in the early phase of training (42), the concomitant changes in maximal isometric force and 1-RM load must be an indication of changes in the muscle itself. Indeed, there is at least one study that reported significant muscle hypertrophy after only 3 weeks of strength training in humans (45). In addition, after a few hundred contractions, muscle hypertrophy occurred with voluntary or artificial neural drive (46)(47). Taken together, these data indicate that perhaps the view of early strength adaptations in young and older subjects being exclusively mediated by neural mechanisms is oversimplified.
Our data confirm previous findings that, with age, the rate of tension development (RTD) declines more than maximal strength (33)(48). Such a decline may be related to the preferential atrophy and a loss of fast contracting muscle fibers (3)(8)(49). Slowing this decline is important for elderly people because an impaired RTD seems to be associated with the reduced ability to make sudden turns and stops (7) and to maintain balance control (6). Strength training that incorporated slow contractions did not improve RTD substantially in either young or older subjects (34)(42)(50)(51)(52). We observed significant improvements in Force200ms of 46%, whereas the 15% and -23% changes in RTDmax and Time150N were not significant. Perhaps RTD variables are resistant to change in response to strength training because the test itself, being an isometric test, is not specific enough to detect changes caused by dynamic contractions. Indeed, when elderly subjects performed explosive strength training, changes in RTD parameters were significant (5). In agreement with previous data, we also noticed large variability in the changes of the RTD variables, making it difficult to detect significant changes.
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Acknowledgments |
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This study was supported, in part, by research and creative activity grants from the East Carolina University Faculty Senate (T.H. and P.D.), the North Carolina Institute on Aging (P.D.), and National Institute of Aging (AG16192) (T.H.).
Received April 17, 2000
Accepted July 27, 2000
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