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a University of Illinois at Urbana-Champaign
Evangelos A. Christou, Neural Control of Movement Lab, Department of Kinesiology and Applied Physiology, University of Colorado at Boulder, Boulder, CO 80309-0354 E-mail: echristo{at}colorado.edu.
Decision Editor: John A. Faulkner, PhD
| Abstract |
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ONE factor that can influence the quality of voluntary movements is motor output variability. The appropriate application of force, including the magnitude, direction, and the timing of force, is required to minimize motor output variability and consequently spatial error (kinematic error; 1,2). Several studies have shown that old adults exhibit increased kinematic variability compared with young adults during functional movements (3)(4) and that they prefer to slow down to eliminate errors and loss of balance (3)(5). From these and other observations, it has been suggested that the elderly population's increased tendency to fall could also be related to a reduced ability to control muscle force (5)(6)(7).
Force control appears to be reduced in elderly adults compared with young adults, particularly at low levels of force (7)(8)(9)(10)(11)(12). These age-related differences, however, are not consistent across limbs (13) and become smaller when old adults participate in strength training (9) or physical activities such as T'ai Chi (14)(15). One of the factors that might be associated with the decreased ability of the elderly population to control force is the reorganization of small motor units (16)(17), which can alter the strategies used by the nervous system to control muscle force (18)(19).
Traditionally, motor output variability has been measured by using continuous (7) and discrete isometric tasks (2). In continuous tasks the participant attempts to match a constant force level for an extended period of time, whereas in discrete tasks the participant attempts to match a forcetime parabola with a short duration by controlling force output. The standard deviation (SD) and coefficient of variation (CV) have been used frequently to measure the within-subject variability in motor output characteristics such as the level of force, time to peak force, impulse, and impulse duration. It is generally accepted that for both continuous and discrete isometric contractions, the SD of force increases as the level of force increases, and the CV of force decreases as the level of force increases (2)(7)(8)(11)(20). In addition, it appears that the most appropriate way to compare individuals from different strength groups is to compare the normalized variability (i.e., CV) as a function of the normalized muscle activation level (percentage of maximum voluntary contraction [%MVC]) (21).
Studies that examine age-related differences in motor output variability have focused on slow- and low-force continuous isometric and anisometric contractions (7)(8)(9)(10)(11)(12). To our knowledge, there are no studies that have examined age-related differences by using a rapid discrete task. Rapid discrete contractions differ from continuous contractions in many respects. The rate of force production is higher, the motor command must be repeated over trials, and the use of kinesthetic feedback is minimized. From the existing literature and the above observations, we hypothesized that age will impair control of both continuous and discrete isometric contractions; however, this impairment will be greater during discrete isometric contractions. A secondary hypothesis was that the control of force would be significantly worse during discrete contractions than during continuous isometric contractions.
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Procedures
Strength and motor output variability were assessed by using continuous and discrete isometric contractions of the quadriceps femoris muscle group. Participants attended two separate sessions: one for continuous and one for discrete isometric contractions. For each type of contraction the level of maximum voluntary contraction was determined. Based on the MVC produced, target forces, expressed as %MVC, were determined.
The participants were seated on the isokinetic dynamometer chair for testing with the backrest angle at 90°. The axis of rotation of the right knee (lateral epicondyle of the femur) was aligned with the axis of rotation of the dynamometer armature. The ankle cuff (load cell assembly) was positioned so that the lowest part of the cuff was 2.5 cm above the talus bone. To eliminate postural instability, stabilization straps were placed over the pelvis and chest. In addition, are participants positioned their arms across their chests during each trial to eliminate other variables that could have influenced MVC and variability of force (e.g., arm strength). The knee angle was set to 90° for all trials, and a soccer shin guard was placed over the right shin to protect the participants from any potential discomfort caused by the large number of leg extensions performed during each session.
The order of contraction types was counterbalanced. The MVC trials and the trials at the various %MVCs were blocked. The order of the %MVC levels within a contraction type were randomly determined. Prior to each session, participants warmed up by walking for 5 minutes and stretching their quadriceps femoris, hip flexors, and gastrocnemius muscles. The MVC of each participant for each type of contraction was measured at the completion of the warm-up. Specific warm-up (three submaximal trials) was given to the participants before testing their MVCs to familiarize them with the apparatus and task.
Maximum Voluntary Continuous Contractions
As a way to identify the maximum voluntary isometric force production for continuous tasks, young and elderly participants were asked to produce maximal leg-extension force for 5 seconds. This procedure was repeated twice with a 30-second rest between trials. Trials were accepted only if the highest recorded forces between trials were within 5% of each other (the highest number of trials performed by a participant was five). Participants monitored the force produced on the monitor of the isokinetic dynamometer. Similar to other investigations, the average of the 10 highest force values produced over all three trials was considered the maximum voluntary continuous isometric contraction level for the participant (27). Following each contraction session, each subject performed another MVC to identify whether fatigue had taken place.
Maximum Voluntary Discrete Contractions
For discrete isometric contractions, participants were asked to produce maximal effort force pulses with brief durations. The criterion of time to peak force for each trial was 200 milliseconds. Because longer times to peak force can increase maximum force (28)(29), the 200 millisecond time to peak force was used to identify the MVC. A rapid time to peak force also eliminates any potential changes to the force produced by the participant that are due to feedback. Participants were able to monitor the gradation of force on the monitor of the isokinetic dynamometer. Maximum effort trials were repeated with a 30-second rest between the trials until three trials with a time to peak force of 200 milliseconds (±10%) were produced (the highest number of attempts required by a participant was 10 trials). The highest of the three force values produced from the three accepted trials was considered the maximum voluntary contraction. Similar to the continuous contractions, at the end of the contraction session each subject performed another MVC to identify whether fatigue had taken place.
Continuous and Discrete Isometric Contraction Tasks
The positioning of the participant was the same as that used for the MVCs. For the whole range of muscle activation to be examined, eight target-force levels were determined based on the maximum isometric force produced by each participant. These forces were 5%, 10%, 20%, 35%, 50%, 65%, 80%, and 90% of MVC, and they were selected because they represent a wide range of muscle activation levels. The order of target forces was determined randomly for each participant.
Continuous task.-- For the continuous isometric task the target force for a %MVC level was displayed as a horizontal line on the computer monitor located 50 cm in front of the participant (Fig. 1). The force exerted by the participant was also displayed on the monitor as a function of time (a different colored line was used for target and force produced). Participants were instructed to match the leg-extension force with the target force. Trials lasted 15 seconds for levels of force below 50% MVC and 10 seconds for all higher levels of force. Visual feedback was provided for the first 5 seconds for guidance. At the end of the fourth second, the monitor was covered and the participant was asked to maintain the same leg-extension force for the remainder of the trial. One practice trial was given to each participant so that he or she would feel comfortable in completing the task and matching the target force for that %MVC level. The same procedure was used for each target force for two experimental trials. A brief rest period of 30 seconds was given between data-collection trials, and 120 seconds of rest was given between target forces.
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Experimental Design and Data Reduction
Means, SD, and CV of several force and time parameters were computed from the experimental trials. For continuous isometric contractions, a preliminary analysis indicated that mean force significantly decreased and SD and CV significantly increased at times over 7.5 seconds. This trend was greater at levels of force over 50% MVC. As a way to eliminate shifts in mean force values caused by fatigue within each trial, only force values from 5 to 7.5 seconds were used in the calculations for the continuous isometric task. For the discrete isometric task, a number of trial characteristics were analyzed from the 40 experimental trials. These included peak force, impulse (the integral of force/time), time to peak force, and impulse duration.
An initial examination of force variability (SDF) indicated that males were more variable than females. This was expected because males had greater MVCs; therefore, the criterion force level at any %MVC was greater compared with that of the female participants. Normalizing the variability of force to the level of force produced by each participant (CV) resulted in a nonsignificant effect for gender, for continuous isometric contractions, and peak force, impulse, time to peak force, or impulse duration for discrete isometric contractions (all p > .05). Therefore, the two gender groups were combined for further analyses.
Statistical Analysis
Maximum force produced (MVC) was examined by using a three-factor complete factorial analysis of variance (ANOVA; 2 Age groups x 2 Genders x 2 Contraction types), with repeated measures on contraction type. As a way to identify whether fatigue occurred during each contraction session, the MVC was examined by using a paired t test between the MVC before and the MVC recorded after the contraction session. A three-factor complete factorial ANOVA (2 Age groups x 2 Contraction types x 8% MVC), with repeated measures on contraction type and %MVC, was used to examine the variability of force (SDF) and the coefficient of variation of force (CVF). For the continuous isometric contractions, mean force, SDF, and CVF were based on two-trial averages. For discrete isometric contractions, mean, SD, and CV of peak force (based on the last 40 trials) were analyzed. A two-factor complete factorial ANOVA (2 Age groups x 8% MVC), with repeated measures on %MVC, was used to examine the SD and CV of impulse, time to peak force, and impulse duration for discrete contractions. The alpha level for all statistical tests was set at 0.05 and paired contrasts (t tests) were used to locate differences between age groups and contractions when ANOVAs yielded significant interactions. A summary of the ANOVAs used and their results are in Table 2 .
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| Results |
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Matching of Targets
Mean peak force and impulse increased systematically with increases in level of force. The mean peak force and impulse error indicated that, on average, young and old subjects produced higher peak forces and impulses than the goal force at low percentages of MVC and lower peak forces than the goal at high percentages of MVC. The temporal error indicated that, on average, both age groups performed slightly shorter-duration contractions than the goal time at low forces and longer-duration contractions than the goal time at high forces.
Motor Output Variability for Age and Contraction Type
SD of force..--
Young participants exhibited greater variability than elderly participants, and discrete isometric contractions were more variable than continuous isometric contractions. As expected, the SDF increased as the level of force increased. The interactions between age group and contraction type, and age group and level of force, indicated that young adults were more variable than elderly adults for both continuous and discrete contractions at all levels of force; however, age differences were greater for discrete isometric contractions and at lower levels of force (Table 3 ). Variability during discrete isometric contractions was significantly higher across all eight levels of force compared with continuous isometric contractions; nevertheless, differences were greater in the middle range of target-force levels (Fig. 2).
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CV of impulse duration..-- Elderly participants exhibited greater CVs than young participants, and the CV for impulse duration decreased as the level of force increased. The interaction between age group and level of force (Fig. 6) indicated that elderly participants exhibited significantly greater CVs at levels of force up to 35% MVC; however, at levels of force of 50% MVC and beyond, no significant differences were found between the two groups.
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| Discussion |
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Compared with the young participants in this study, the elderly participants consistently produced higher relative variability (CV) during rapid discrete isometric contractions when the level of force was expressed as %MVC. This finding was robust for peak force, impulse, time to peak force, and impulse duration. The inability of the elderly participants to control force (CV) and timing (SD and CV) only during rapid contractions supports previous results suggesting that elderly people perform as accurately as young people during slow-speed continuous movements (31); however, movement control is reduced with increases in speed and complexity of movement (32)(33).
There is accumulating evidence that discharge-rate variability is primarily responsible for greater motor output variability in the elderly population (11)(34)(35). One physiological mechanism that could increase the variability in the discharge rate of motor units in the elderly population is decreases in the transmission velocity from corticospinal and reflex pathways to the motor neurons (36)(37). This transmission impairment can be caused by the 2535% reduction in the total number of cortical motor neurons (38), the lumbosacral (spinal cord) motor neurons (20), and particularly the loss of the largest alpha motor neurons and their myelinated axons (19). Other mechanisms, such as increased average force produced by motor units (39), the pattern of coactivation by the agonist and antagonist muscles (40), and synchronization of motor units (30), have been refuted as the explanations for the increased variability exhibited by elderly individuals.
The differences between young and older adults did not appear to be due to differences in the speed of learning a new motor skill. Older adults, compared with young adults, have reduced motor learning abilities only when the task requires a strategy (41)(42). In addition, young and old adults appear to use knowledge of results similarly to learn a new motor task (43). The discrete isometric task used in this study was nonstrategic (matching a line or parabola with a single joint movement), and the same knowledge of results was given to both young and old participants. A preliminary examination of our discrete isometric data suggests that both age groups improved accuracy of the motor output at a similar rate. We believe, therefore, that age-related learning impairments did not influence the results of this study.
Contraction Differences
The present experiment demonstrated that variability in force production (SD and CV) is significantly greater during discrete isometric contractions than it is during continuous isometric contractions. This finding was consistent across levels of force ranging from 5% to 90% MVC. Greater variability for discrete isometric contractions may be related to several factors.
One difference between the two tasks is feedback utilization caused by the temporal requirements. Continuous isometric contractions are slow and have no temporal constraints; therefore, kinesthetic feedback is a potential factor that can provide additional information, enhance corrections, and reduce variability of force (closed-loop control system). The discrete isometric contractions used in the present experiment were fast and had very short temporal constraints (time to peak force was 200 milliseconds), and this minimized the ability of the neuromuscular system to use kinesthetic feedback and allow corrections within the contraction time (open-loop control system) (44).
A second factor that may account for the greater variability for discrete isometric contractions is the influence of rate of force production. The rate of force production has a significant effect on motor output variability, and experiments that have manipulated the rate of force production have demonstrated systematic changes in variability of force impulse, especially for higher levels of force (1)(2)(28)(29)(45)(46). Longer contraction times have been associated with decreases in variability of force and impulse (2)(45)(46).
Other possible factors that may account for the greater variability found during rapid discrete isometric contractions are the type and discharge-rate variability of motor units. The orderly recruitment of motor units is preserved during both slow continuous and rapid discrete isometric contractions; however, during rapid contractions, motor units are recruited at an earlier %MVC (47)(48) and with more variable discharge rates (49). Large motor units (50) and higher discharge-rate variabilities of motor units (51) have been associated with greater variability in force.
Another potential factor that can increase variability of force during discrete isometric contractions is the change in the neuromuscular system that is due to repetition of the motor command. During continuous isometric contractions, each level of force was maintained for approximately 10 seconds and was repeated only once by each participant. During discrete isometric contractions, however, the repetition of the motor command (40 trials) can slightly alter the number, size, and discharge rate of motor neurons recruited for each trial.
Several possible explanations have been suggested for the differences in variability between continuous and discrete isometric contractions. Although a single factor may account for these differences, it is also possible that a combination of differences in feedback availability, recruitment, and task characteristics may account for the up to sixfold increase in variability for discrete isometric contractions.
Received January 16, 2001
Accepted August 13, 2001
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